Catherine L Jackson
email: cathy.jackson@ijm.fr

Julie Ménétrey
email: julie.menetrey@i2bc.paris-saclay.fr

Mandeep Sivia

Joel B Dacks
email: dacks@ualberta.ca

Marek Eliáš
email: marek.elias@osu.cz

An evolutionary perspective on Arf family GTPases

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Introduction

Arf family proteins are key regulators of cellular organization in eukaryotic cells, functioning in the secretory and endocytic pathways, at mitochondria, in cilia and flagella, in actin cytoskeleton regulation, and in microtubule dynamics. This family of GTPases includes Arf, Arl, and Sar proteins, as well as Arfrp1 and ARD1/TRIM23 (Box 1). Arf family GTPases are found throughout eukaryotes, and many are highly conserved across a broad range of animals, plants, fungi and protists [START_REF] Li | Functional genomic analysis of the ADP-ribosylation factor family of GTPases: phylogeny among diverse eukaryotes and function in C. elegans[END_REF]. Here we review the latest developments in the evolution and functions of Arf family GTPases in eukaryotes.

____________________________ Box 1

The different names of Arf family proteins (Arf, Arl, Sar, Arfrp1, ARD1, etc.) does not indicate fundamental differences in their cellular functions. Arf1 (for ADP ribosylation factor 1), the first Arf protein identified, was discovered as a factor stimulating ADP ribosylation of the a subunit of the heterotrimeric G protein Gs (Gsa) by cholera toxin, stimulating the production of the second messenger cAMP [START_REF] Kahn | Purification of a protein cofactor required for ADP-ribosylation of the stimulatory regulatory component of adenylate cyclase by cholera toxin[END_REF]. Later it was found that a major cellular function of Arf1 is in regulation of the secretory pathway [START_REF] Stearns | ADP-ribosylation factor is functionally and physically associated with the Golgi complex[END_REF], as well as other cellular processes [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF][START_REF] Sztul | ARF GTPases and their GEFs and GAPs: concepts and challenges[END_REF], and its ADP ribosylation co-factor activity does not appear to contribute to these normal cellular functions. As more proteins related to Arf family proteins were identified, the lack of a systematic approach led to problems in assigning names. In 2006, a consensus nomenclature was agreed upon [START_REF] Kahn | Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins[END_REF]. We will refer to all of these GTPases as "Arf family proteins". The SRb proteins are phylogenetically related to the Arf family proteins [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF], but are not included here in our definition of Arf family proteins.

____________________________

As for small G proteins in general, Arf family proteins act as molecular switches, inactive in their GDP-bound form, and active when bound to GTP (Figure 1a). Arf1, and many other members of the family, are soluble in their GDP-bound form but are tightly membrane-bound in their active GTP-bound form [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF][START_REF] Sztul | ARF GTPases and their GEFs and GAPs: concepts and challenges[END_REF]. The change in membrane association does not rely on other proteins, but is due to a second conformational change within the protein itself upon GTP binding (Figure 1a). Unique to Arf family proteins is the presence of an N-terminal amphipathic helix (AH), often myristoylated, that mediates membrane binding (Figure 1a). Although the majority of Arf family proteins have this mechanism of membrane association, there are some exceptions [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF][8][9].

Effectors, proteins which interact with the active GTP-bound form, carry out the cellular functions of Arfs. The majority of Arf family proteins, whose GTP-bound form is membrane-bound, recruit effectors to the membrane surface, making the membrane an important component of Arf function (Figure 1a). The major classes of effectors are vesicle coats, membrane tethering proteins, lipid modifying and transfer proteins, cytoskeleton components (actin and microtubule), and microtubule motors and their adaptors.

Arf family proteins in eukaryotes require regulators, guanine nucleotide exchange factors (GEFs) and GTPase activating proteins (GAPs), to accelerate release of GDP and hydrolysis of GTP, respectively (Figure 1a). Sec12 was identified as a GEF for Sar1 on the ER membrane [10], and Sec7 domain proteins were identified as GEFs for Arf1 [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF]. Whereas only one family of Sec12 GEFs has been found, multiple subfamilies of Sec7 domain proteins were identified, with activities on Arf1-6 and Arl1 [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF]11,12]. It is only recently that new families of Arf GEFs have been identified. Arl13b and BART are both required for GEF activity on Arl3 in cilia [9,13], and AMPK has been found in both yeast and mammalian cells to activate Arf6 (called Arf3 in yeast) [14,15]. In both organisms, AMPK activates Arf6/yArf3 in response to glucose depletion [14,15]. Sec23, a component of the COPII coat, acts as a GAP for Sar1, and the Zn-finger domain containing proteins are GAPs for Arf1-6 and Arl1, comprising 11 subfamilies [START_REF] Sztul | ARF GTPases and their GEFs and GAPs: concepts and challenges[END_REF]16,17]. Three additional families of Arf GAPs were subsequently identified. The ELMOD proteins have a relatively broad range of activities on Arf family proteins, including Arf1-6, Arl1, Arl2 and possibly ciliary Arl3 and Arl13b [18,19]. RP2 is a GAP that acts on Arl2 and Arl3, and has been characterized in animal cells and yeast [20]. Recently, an Arf GAP complex containing longin domains, the C9orf72 complex, was described that functions on Arf1, Arf5 and Arf6 [21,22].

Sculpting ancestral complexity by gene loss is a major pattern of Arf family evolution

A recent comprehensive phylogenetic analysis of Arf family proteins has provided new insights into these important regulators of eukaryotic cellular organization (Figure 1b) [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF].

The most notable result was the reconstruction of the complement of Arf family members in the last eukaryotic common ancestor (LECA), which turned out to be larger than previously suspected (Figure 2). In addition to paralogs typified by metazoan, usually well-studied proteins (Arf1 and 6, Arl1, 2, 3, 5, 6, 8, 13, and 16, Arfrp1, and Sar1), the LECA seems to have encoded three additional Arf family members that are absent from virtually all metazoans and which were denoted Arl17, Arl18 and SarB. Thus, these three proteins qualify as socalled jotnarlogs, proteins that are ancient in eukaryotes yet (secondarily) missing from opisthokonts [START_REF] More | Evolution and Natural History of Membrane Trafficking in Eukaryotes[END_REF]. In total, the LECA was most likely endowed with 15 different Arf family genes, a complement larger than that present in many extant eukaryotes. Indeed, gene loss has been pervasive in the evolutionary history of the Arf family, with some of the ancestral members lost many times independently across the eukaryote phylogeny. As an example, let us take you on a journey through time, following the fate of the Arf family along the organismal line of descent from the LECA to one of the most extensively studied biological model systems, the yeast Saccharomyces cerevisiae. We base the narrative on the previous published data [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF] with updates that fill in critical gaps in the taxon sampling (Figure 2).

The first change to the LECA's Arf family gene set was the loss of Arl18 deep in the eukaryote tree (prior to the divergence of Amoebozoa). The last common ancestor of the eukaryote supergroup Opisthokonta thus inherited a nearly complete ancestral set of Arf family members. From this point on, the yeast lineage experienced a stepwise reduction of the set, with Arl16 loss having occurred immediately after the divergence of the Holozoa lineage (containing metazoans and their closest protist relatives), followed by loss of the SarB gene after the divergence of Nucleariida (a group of amoeboid protists). As the yeast ancestors were still flagellated at this point, they had retained the flagellum-associated GTPases Arl3, Arl6, and Arl13, but these vanished with the loss of the capability to build flagella later in the evolution of fungi. Arl5 was then lost in the stem branch of the major fungal phylum Ascomycota, and Arl17 in the stem branch of its subphylum Saccharomycotina. The final loss event, removing Arl8, occurred late in the S. cerevisiae evolutionary lineage. As a result, budding yeast has retained only six out of the 15 ancestral Arf family members.

Gene duplication also shapes the Arf family in a taxon-specific manner

The final event in the genesis of the S. cerevisiae Arf family gene set was duplication of the ancestral Arf1 gene yielding a pair of lineage-specific paralogs (Arf1 and Arf2), which was part of the whole genome duplication (WGD) that occurred in the common ancestor of Saccharomyces and several related genera [START_REF] Purkanti | Genome doubling enabled the expansion of yeast vesicle traffic pathways[END_REF] (Figure 2). Although not the case for S. cerevisiae, taxon-specific expansions of the Arf family by gene duplication have been pervasive across eukaryotes in general. Let us illustrate this general pattern by again following the evolutionary trajectory of the Arf family in a single specific organismal lineage, this time the one leading to us, humans (Figure 2).

We start with the last common ancestor of opisthokonts, when the human lineage, as part of the clade Holozoa, diverged from that leading to yeasts. In contrast to the yeast lineage, the stem branch of Holozoa was instead evolutionarily creative, as emergence of three novel Arf family members can now be mapped to it: Arf4, Arl15 and Arl19. Arf4 and probably Arl19 emerged via duplication of the ancestral Arf1 gene, whereas the origin of Arl15 has been obscured by extreme sequence divergence. At a later point of the holozoan phylogeny but still during its "protist stage", another paralog, Arl20, emerged again presumably from a duplicated Arf1 gene.

In contrast to numerous novel paralogs in the Rab family of GTPases evolved during the transition to multicellularity in the stem branch of Metazoa [START_REF] Elias | Sculpting the endomembrane system in deep time: High resolution phylogenetics of Rab GTPases[END_REF], the history of the Arf family is marked only with the addition of a single new gene, Arl10, and also by loss, namely of SarB. Two additional novel family members, Arl4 and the multidomain protein TRIM23, evolved in early metazoan evolution, the former from a duplicate of Arl19 and the latter perhaps from a duplicated Arf1 gene by its fusing to a region encoding additional protein domains [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF]. Around the same time, Arl17 was lost from the human ancestors, later followed by loss of Arl20 before the emergence of vertebrates.

The composition of the Arf family set was then affected by two WGD rounds in early vertebrate evolution, one most likely preceding the divergence of cyclostomes and the other specific for jawed vertebrates [START_REF] Simakov | Deeply conserved synteny resolves early events in vertebrate evolution[END_REF]. These events together with post-WGD losses of some of the duplicates seem to be the major cause for some of the Arf family genes inherited from the invertebrate ancestor being represented by two or three different copies in the genome of humans and other vertebrates (Figure 2). The nomenclature of the WGDderived copies (also known as ohnologs [START_REF] Singh | OHNOLOGS v2: a comprehensive resource for the genes retained from whole genome duplication in vertebrates[END_REF]) reflects their common origin in an inconsistent way, with, eg., the Arl8a/Arl8b pair being not different in this regard than, eg., the Arf4/Arf5 pair. Another pair of ohnologs, Arl11 and Arl14, itself seems to have emerged from a vertebrate-specific parental gene that evolved before the WGD rounds from a duplicated Arl4 gene by its substantial sequence divergence. The final steps towards the Arf family gene complement as represented in the human genome were losses of the Arl19 and Arf2 genes at different nodes of mammalian evolution (Figure 2).

In general, the outcomes of the duplication events in the Arf family history span a broad gradient from augmenting the Arf family by extra copies of some of the genes that are identical or extremely similar at the protein sequence level, to the emergence of "novel" paralogs that have diverged from their parental gene to such an extent as to effectively obscure the specific origin of the gene. We will provide examples below of the functional significance of duplications, which can be more or less asymmetric. The emergence of "novel" paralogs is not exclusive for the human (holozoan) evolutionary lineage, as divergent Arf family members dissimilar to any of the 15 ancestral paralogs are common in diverse eukaryotes [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF].

Evolution of Arf family regulators

As compared with the Arf family of GTPases, our understanding of the diversity and evolution of its regulators is less developed. Nonetheless, the work to date brings out several key points of both contrast and parallel. Whereas the Arf family is derived from a common ancestor, the same is not true of either GEFs or GAPs, which have arisen from different non-homologous protein families. Still, the themes of protein family expansion, loss, and novel paralogs are also found in the regulators (Figure 3).

Reaching back to the LECA, we see that of the eight subfamilies of Sec7 domain Arf family GEFs in humans, three (GBF, BIG, and cytohesin) [11], along with the Sar1 GEF Sec12 [START_REF] Schlacht | Unexpected Ancient Paralogs and an Evolutionary Model for the COPII Coat Complex[END_REF] and AMPK [START_REF] Roustan | An evolutionary perspective of AMPK-TOR signaling in the three domains of life[END_REF], were already present. The Sar1 GAP Sec23 was present in at least one copy [START_REF] Schlacht | Unexpected Ancient Paralogs and an Evolutionary Model for the COPII Coat Complex[END_REF], seven subfamilies of Zn-finger domain Arf GAPs were present [17], and at least one (possibly two) ELMOD Arf GAPs were present in LECA [19]. ELMOD family proteins have recently been functionally characterized in Arabidopsis [30] and localized in Trypanosoma brucei (http://tryptag.org/?id=Tb927.9.2670) [31].

There are several novel domain architectures of both GEFs and GAPs found in various eukaryotic lineages (Figure 3). ArfGAP_C2 has not been found in humans or other opisthokonts, making it a jotnarlog, but is present in plants, haptophytes, apusomonads, and members of the SAR clade [17]. ArfGAP_C2 possesses the canonical Zn finger Arf GAP domain, followed by a C2 lipid-binding domain. Novel cytohesin-derived Arf GEFs (ARCC) with multiple N-terminal ankyrin domains exist in amoebozoans, haptophytes, and alveolates [11]. Careful analysis showed that ARCC Arf GEFs must have evolved independently in amoebozoans and alveolates, at least [11].

Loss has also clearly shaped the complements of Arf family regulators. One of the starkest examples of reductive evolution is the regulator complement found in the metamonad lineage leading to the gut parasite Giardia (Figure 3). In this case, both the freeliving and parasitic organisms sampled encoded only two SEC7 Arf GEF subfamilies and three Zn finger Arf GAP domain subfamilies [START_REF] Pipaliya | The reduced ARF regulatory system in Giardia intestinalis pre-dates the transition to parasitism in the lineage Fornicata[END_REF]. And yet with loss also came paralog expansion. While the Arf6 subfamily has been lost from this lineage, the Arf1 subfamily has been expanded at multiple time points [START_REF] Pipaliya | The reduced ARF regulatory system in Giardia intestinalis pre-dates the transition to parasitism in the lineage Fornicata[END_REF] Jumping to the ancestor of animals and fungi (opisthokonts), we see another point of contrast between the GTPases and their regulators. While there is little emergent novelty between the LECA and the opisthokont ancestor in the Arf family, several new GEFs and GAPs have appeared on the scene by this time (Figure 3). The EFA6 subfamily (PSD in animals) is a cytohesin derivation and had clearly already evolved at this point. Similarly, though ArfGAP_C2 has been lost, the Arf GAP ASAP emerges by this time [17]. Finally, by this time, through gene duplication and novel domain fusions, the ELMO proteins arose.

However, these proteins are not Arf GAPs because their ELMO domains have lost the catalytic arginine [19].

The ancestor of animals is the border between uni-and multi-cellularity in this lineage and an area of active and exciting research into the under-appreciated diversity of small predatory flagellates that were our ancestral form [START_REF] Tikhonenkov | New Lineage of Microbial Predators Adds Complexity to Reconstructing the Evolutionary Origin of Animals[END_REF]. Here both the GTPases and their regulators have undergone duplications to produce new members of each family, although the new regulators have not emerged to regulate only the newly evolved Arf family members. Just as several new GTPases are on scene by this time, the ArfGEFs IQSEC7 and BRAG, both cytohesin derived, had appeared by this stage [11], as did the Arf GAP subfamilies GIT and ARAP [17]. Finally, the complement of Arf regulators was shaped extensively by the WGDs around the evolution of vertebrates, with between two and four paralogs of each of the regulators appearing by the time of the vertebrate common ancestor [11,17,19].

Functions of Arf family proteins

Of the 15 Arf family proteins already present in the LECA (Figure 1b), 12 have known functions [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF]. These functions include coat recruitment by Sar1, Arf1, Arl6; microtubule dynamics by Arl2, Arf1, Arf6, Arl8; Golgi tethering by Arf1, Arl1, Arl5, and Arfrp1; cilia function by Arl3, Arl6, Arl13, Arl16 (in addition to Arl2, Arf4 and Arf6); regulation of the actin cytoskeleton by Arf1 and Arf6; and lipid dynamics and homeostasis by Arf1, Arf6, Arl5 and Arfrp1. A full discussion of Arf family function is beyond the scope of this review, so we will focus on core functions and key advances made in the past two years in understanding these functions, at the molecular level.

Arf1 and Sar1 were found in every one of the eukaryotic genomes examined in Vargová et al. [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF]. Both Sar1 and Arf1 regulate recruitment of vesicle coats for vesicle formation in the early secretory pathway -anterograde ER-Golgi COPII vesicles in the case of Sar1, and retrograde Golgi-ER COPI vesicles in the case of Arf1. Secretion is an essential function in eukaryotic cells, and recruitment of the COPI and COPII coats by Arf1 and Sar1, respectively, has been demonstrated experimentally in all eukaryotes examined, including animals, fungi, plants and protists [START_REF] Gomez-Navarro | COP-coated vesicles[END_REF][START_REF] Yorimitsu | Molecular mechanisms of Sar/Arf GTPases in vesicular trafficking in yeast and plants[END_REF][START_REF] Herman | Identification and characterisation of a cryptic Golgi complex in Naegleria gruberi[END_REF][START_REF] Brandizzi | Organization of the ER-Golgi interface for membrane traffic control[END_REF][START_REF] Singh | A single class of ARF GTPase activated by several pathwayspecific ARF-GEFs regulates essential membrane traffic in Arabidopsis[END_REF]. Arf1 also recruits at least four other coat complexes to trans-Golgi and endosomal membranes, AP-1/clathrin, GGA/clathrin, AP-3 and AP-4. Three of these vesicle coats, in addition to COPI and COPII, are all inferred to have been present in LECA [START_REF] Dacks | Outerwear through the ages: evolutionary cell biology of vesicle coats[END_REF]. Hence coat recruitment for vesicle formation represents a core function of Arf family proteins, which was likely present in the LECA.

Arf6 functions in endosome-plasma membrane trafficking pathways and not at the Golgi as Arf1 does [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF][START_REF] Sztul | ARF GTPases and their GEFs and GAPs: concepts and challenges[END_REF]. Arf1 and Arf6 were both present in LECA, indicating an ancient division of functions [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF]. The four human Arf1 paralogs (Arf1-5, Arf2 is missing due to loss, see above) have been shown to promote formation of COPI vesicles in vitro, although only Arf1, Arf4 and Arf5 are found on COPI vesicles purified from cells [START_REF] Popoff | Several ADP-ribosylation Factor (Arf) Isoforms Support COPI Vesicle Formation[END_REF]. Systematic knockouts of the four paralogs in HeLa cells revealed a high level of redundant function [START_REF] Pennauer | Shared and specific functions of Arfs 1-5 at the Golgi revealed by systematic knockouts[END_REF]. Single deletions of Arf1 or Arf4 were viable, but the double deletion mutant was inviable, indicating redundant functions essential for growth. This result illustrates the principle that after gene duplication during evolution, a certain degree of functional redundancy of the copies may persist over long periods (Figure 2). However, analysis of individual knockout phenotypes indicated that Arf1 and Arf4 have specialized functions as well: Arf4 in retrieval of resident ER proteins from the cis-Golgi and Arf1 in exit pathways from the Golgi mediated by COPI, AP-1 and AP-3 coats [START_REF] Pennauer | Shared and specific functions of Arfs 1-5 at the Golgi revealed by systematic knockouts[END_REF].

After Arf1 and Sar1, Arl2 is the next most widely distributed Arf family member among eukaryotes, with its loss so far encountered only in the genus Entamoeba [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF]. The most universal function of Arl2 is as a chaperone for the folding of aand b-tubulin. As a result, Arl2 is involved in numerous microtubule-dependent processes. In addition, Arl2 shares functions with the closely related Arl3 in cilia and flagella, as well as regulating mitochondrial function [8,[START_REF] Newman | The abundance of the ARL2 GTPase and its GAP, ELMOD2, at mitochondria are modulated by the fusogenic activity of mitofusins and stressors[END_REF][START_REF] Turn | Roles for ELMOD2 and Rootletin in ciliogenesis[END_REF].

Multiple Arf family GTPases regulate movement of organelles along microtubules, including movement of Golgi elements to the cell center by Arf1 [START_REF] Yadav | Golgin160 Recruits the Dynein Motor to Position the Golgi Apparatus[END_REF], and bidirectional movement of endosomes at the midbody by Arf6 [START_REF] Isabet | The structural basis of Arf effector specificity: the crystal structure of ARF6 in a complex with JIP4[END_REF][START_REF] Montagnac | ARF6 Interacts with JIP4 to Control a Motor Switch Mechanism Regulating Endosome Traffic in Cytokinesis[END_REF]. Recently, a series of papers have demonstrated the mechanisms by which Arl8 regulates bidirectional movement of lysosomes along microtubules. Arl8 interacts with SKIP on lysosomal membranes to couple them to kinesin-1, thus promoting movement of lysosomes towards the periphery of cells [START_REF] Keren-Kaplan | ARL8 Relieves SKIP Autoinhibition to Enable Coupling of Lysosomes to Kinesin-1[END_REF]. Arl8 can also interact with RUFY3 and RUFY4, which interact with dynein-dynactin to mediate movement of lysosomes towards the minus end of microtubules at the cell center [START_REF] Keren-Kaplan | RUFY3 and RUFY4 are ARL8 effectors that promote coupling of endolysosomes to dyneindynactin[END_REF]49]. In this way, Arl8 can regulate bidirectional movement along microtubules, through binding to different effectors. Together, these results show that Arf family proteins have a prominent role in microtubule dynamics.

Arl1, Arl5 and Arfrp1 are found in all of the main eukaryotic lineages, but are lost more frequently (mainly in terminal branches) compared to Sar1, Arf1 and Arl2 [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF]. Arl1 shares a number of functions with Arf1, and they also share a GEF and GAP [12,16], but Arl1 and Arl5 are more closely related phylogenetically (Figure 1b where they are loaded with cargo (for example, signalling molecules to be removed from the cilium) and then transported back to base of the cilium. Arl6 functions to recruit the BBSome to membranes, after which it enters the cilium, and then connects to the IFT machinery [START_REF] Sztul | ARF GTPases and their GEFs and GAPs: concepts and challenges[END_REF]. Two recent studies in Chlamydomonas reinhardtii report new roles for Arl3 and Arl13b in promoting BBSome-mediated export from the cilium [54,55]. Arl3-GTP binds to retrograde BBSomes shed from the IFT train, which specifically contain phospholipase D (PLD) [START_REF] Liu | Bardet-Biedl syndrome 3 protein promotes ciliary exit of the signaling protein phospholipase D via the BBSome[END_REF], an effector of Arl3 [54,55]. In addition to the cilia/flagella-specific Arf family proteins, Arl2 and Arf4 also function in cilia [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF][START_REF] Sztul | ARF GTPases and their GEFs and GAPs: concepts and challenges[END_REF]8]. Recently, Arf6 has also been shown to function with its GEF EFA6A and Arl13b in early steps of ciliogenesis [START_REF] Partisani | EFA6A, an exchange factor for Arf6, regulates early steps in ciliogenesis[END_REF].

Arf family proteins regulate the actin cytoskeleton [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF][START_REF] Sztul | ARF GTPases and their GEFs and GAPs: concepts and challenges[END_REF]. The small GTPase Rac is particularly important in actin cytoskeleton regulation, and Arf6 recruits effectors that contain Rac regulatory domains [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF][START_REF] Sztul | ARF GTPases and their GEFs and GAPs: concepts and challenges[END_REF]. In addition, both Arf1 and Arf6 cooperate with Rac to activate the WAVE regulatory complex (WRC), a crucial actin nucleation promotion factor. A recent study shows that Arf1 and Arf6 directly interact with WRC to promote actin nucleation [START_REF] Yang | Arf GTPase activates the WAVE regulatory complex through a distinct binding site[END_REF]. The WAVE complex was present in the LECA [START_REF] Kollmar | Evolution of the eukaryotic ARP2/3 activators of the WASP family: WASP, WAVE, WASH, and WHAMM, and the proposed new family members WAWH and WAML[END_REF], raising the possibility that Arf family regulation of actin nucleation is ancient.

A major class of Arf family effectors is comprised of lipid modifying and transfer proteins [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF]. Arf6 regulates plasma membrane composition through recruitment of phospholipase D1 (PLD1) and PI4P-5 kinase [START_REF] Donaldson | ARF family G proteins and their regulators: roles in membrane transport, development and disease[END_REF][START_REF] Jang | Understanding of the roles of phospholipase D and phosphatidic acid through their binding partners[END_REF]. PLD1 is also an effector for Arf1, and PI4 kinases are recruited to the Golgi by Arf1 [START_REF] Jang | Understanding of the roles of phospholipase D and phosphatidic acid through their binding partners[END_REF][START_REF] Venditti | PI(4)P homeostasis: Who controls the controllers?[END_REF][START_REF] Highland | Arf1 directly recruits the Pik1-Frq1 PI4K complex to regulate the final stages of Golgi maturation[END_REF]. In a global Arf effector screen [START_REF] Li | Defining the proximal interaction networks of Arf GTPases reveals a mechanism for the regulation of PLD1 and PI4KB[END_REF], Li et al. demonstrated that Arl11 and Arl14 have PLD1 as an effector. Both Arf1 and Arf6 interact with and stimulate PLD1 activity in vitro, but Li et al. found that PLD1 is much more strongly associated with Arl11 and Arl14 than Arf6 in co-immunoprecipitations from cells. Moreover, Arl11 and 14 colocalized with PLD1 in cells, and stimulated its activity in vitro [START_REF] Li | Defining the proximal interaction networks of Arf GTPases reveals a mechanism for the regulation of PLD1 and PI4KB[END_REF]. Arl11 and Arl14 are closely related, as described above [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF]. Similarly, although Arf1-GTP has been previously reported to interact with PI4kinase b, Li et al. found that Arl5a and Arl5b interact to a higher level in co-immunoprecipitations with PI4kinase b than Arf1 does [START_REF] Li | Defining the proximal interaction networks of Arf GTPases reveals a mechanism for the regulation of PLD1 and PI4KB[END_REF]. An independent study identifying interacting partners of Arl5b did not identify PI4kinase b, but did find Acyl-CoA-binding domain-containing protein 3 (ACBD3), which has been shown to recruit PI4kinase b to the trans-Golgi [START_REF] Houghton | Interacting partners of Golgi-localized small G protein Arl5b identified by a combination of in vivo proximity labelling and GFP-Trap pull down[END_REF].

Structural insights into Arf family function

Although 3D structural analyses were essential to elucidate the mechanisms of the GDP/GTP cycle of Arf family proteins, as well as to visualize interactions with their protein partners, the crystallographic approach is limited, especially because of the absence of membranes, which are essential for the functioning of many Arf family proteins. Cryogenic electron microscopy (cryo-EM) and tomography (cryo-ET) approaches have been used to address this limitation. These approaches were used to resolve the structure of the Sar1-COPII coat complex reconstituted on membranes, permitting visualization of the Sar1 AHs embedded in the membrane and determining how the inner COPII coat deforms the membrane to form a vesicle [START_REF] Hutchings | Subtomogram averaging of COPII assemblies reveals how coat organization dictates membrane shape[END_REF]. Recently, the cryo-ET structure of Arf1 bound to AP-1 complexes on liposomes, in the absence of clathrin, was visualized [START_REF] Hooy | Self-assembly and structure of a clathrin-independent AP-1:Arf1 tubular membrane coat[END_REF]. AP-1 complexes form the inner layer of clathrin coats, but also play roles in clathrin-independent membrane trafficking. These data reveal that myristoylated Arf1 and AP-1 are able to form a tubular coat on membranes independently of clathrin, through an Arf1 dimer interface [START_REF] Hooy | Self-assembly and structure of a clathrin-independent AP-1:Arf1 tubular membrane coat[END_REF].

The seven-subunit COPI complex associated with Arf1 has been visualized on membranes, revealing that Arf1 occupies two distinct sites in very different molecular environments in the COPI coat [START_REF] Dodonova | 9Å structure of the COPI coat reveals that the Arf1 GTPase occupies two contrasting molecular environments[END_REF]. The basic unit of the assembly is a triad of the multimeric COPI complex containing six Arf1 molecules. The complete binding site for ArfGAP2, near the central Arf1 molecule, was predicted to form only when the coat is assembled, in a "niche" between two leaves within the triad [START_REF] Dodonova | 9Å structure of the COPI coat reveals that the Arf1 GTPase occupies two contrasting molecular environments[END_REF], a hypothesis supported by the fitting of the recent crystal structure of ArfGAP2 bound to Arf1 [START_REF] Xie | The Glo3 GAP crystal structure supports the molecular niche model for ArfGAPs in COPI coats[END_REF] into the cryo-ET density. In a different, but equally exciting direction, cryo-ET can be used to visualize complexes in their native environment within cells. In the case of COPI, Chlamydomonas provided the ideal system to visualize coated vesicles, and allowed the structure of the COPI coat within cells to be resolved to 20 Å resolution [START_REF] Bykov | The structure of the COPI coat determined within the cell[END_REF]. An important conclusion from these studies is that the structure of the COPI coat is remarkably similar in distantly related organisms, including mammals, fungi and Chlamydomonas.

Cryo-EM and cryo-ET have also been used to determine the 3D structures of Arf family proteins bound to very large, multidomain complexes [22] or multisubunit proteins [START_REF] Muccini | Structural basis for activation of Arf1 at the Golgi complex[END_REF], which often have disordered regions or interdomain flexibility that make crystallization difficult. The three-subunit Arf GAP complex (C9orf72:SMCR8:WDR41) described above belongs to a family of dimeric longin-DENN domain complexes [21,22]. The cryo-EM structure of Arf1 bound to the C9orf72:SMCR8:WDR41 complex showed that the longin domains of C9orf72 and SMCR8 form the binding site for Arf1 and act together to stimulate Arf1 GTP hydrolysis by an arginine finger mechanism [22]. This complex is the first multisubunit GAP to be identified for Arf famiy proteins.

Conclusions and future directions

In this review, we have described some key aspects of the evolution of the Arf family GTPases and their regulators in eukaryotes, and highlighted the latest advances in understanding their major functions. The last eukaryotic common ancestor (LECA) contained an unexpectedly large number of Arf family proteins, and thus many organisms have undergone significant loss of this ancient set. Even the human Arf family gene set records a history of gene loss, thus lacking three ancestral paralogs as well as two novel Arf family members (Arl19 and Arl20) that emerged more recently. Being absent also from other wellstudied organisms, their function remains completely unknown. Humans and other vertebrates have nevertheless undergone duplication events through their evolutionary history, leading to a doubling of the current repertoire of Arf family proteins in extant organisms compared to LECA.

The combination of improvements in genome sequencing, and organism discovery, continues to provide fertile ground for improved evolutionary investigations of protein families. Phylogenetic analyses described here for the Arf family and the best-studied Arf family regulators can now be applied to newly identified GEFs and GAPs, as well as effectors, an exciting area for future exploration. Advances in imaging technologies have made it possible to push past previous limitations in structural biology, and coupled with cell biological and biochemical studies, is providing new insights into the mechanisms of Arf family protein function. Cryo-electron tomography can be used to obtain high resolution structures of large complexes within cells, in their native environments, an approach that has already been used to obtain structures of the Arf1-COPI coat. These approaches promise to revolutionize our understanding of cellular processes at the molecular level, in both wellstudied organisms and in the diversity of less well studied eukaryotes.

Based on a sample of >2,000 manually curated genes from 114 species representing most major eukaryote lineages, the authors defined the Arf family gene complement in the last eukaryotic common ancestor, revealing the existence of previously unknown ancestral Arf family members secondarily missing from the commonly studied models including humans. The study has additionally clarified the genesis of the Arf family in metazoans and pointed to the unexpected diversity of Arf family members in terms of the membrane attachment mechanisms and domain architecture. The authors show that Arl3 activation requires two proteins, Arl13b and BART. As shown previously, Arl13b can stimulate nucleotide release from Arl3, but here the authors show that this reaction is greatly accelerated by addition of BART. Hence both Arl13b and BART are required for activation of Arl3, but do not themselves form a complex, demonstrating a novel mechanism of activation for an Arf family protein. This paper reports that AMPK is a GEF for Arf6 in mammalian cells. AMPK was shown to be a GEF for budding yeast Arf6 (yArf3) [18], hence GEF activity on Arf6 proteins is a conserved function for AMPK, at least in opisthokonts. In both cases, AMPK GEF activity is stimulated in response to glucose depletion. AMPK is one of only two non-Sec7 domain GEFs for Arf family proteins that have been reported to date. This study shows that a mammalian Zn finger Arf GAP, that has been shown to function on Arf1, can also act on Arl1. ArfGAP/Gcs1 was shown previously to act on Arl1 in yeast, so activity of a Zn finger Arf GAP on multiple members of the Arf family appears to be a conserved function, at least in opisthokonts. Along with Su et al. 2020, this paper demonstrates that a complex made up of three proteins, C9orf72, SMCR8 and WDR41, has potent GAP activity on Arf1, Arf5 and Arf6. These studies provide one of the first demonstrations at the molecular level of a cellular function for the C9orf72 protein, one of the major causative agents of the neurodegenerative disease amyotrophic lateral sclerosis (ALS). Interestingly, this complex localizes to lysosomes, which have not been shown to have resident Arf proteins, suggesting that this complex might either act in trans or be sequestered on lysosomal membranes to regulate its activity.

*30. Zhou Y, Amom P, Reeder SH, Lee BH, Helton A, Dobritsa AA: Members of the ELMOD protein family specify formation of distinct aperture domains on the Arabidopsis pollen surface. eLife 2021, 10:e71061.

This paper represents the first functional chracterization of ELMOD proteins in plants. ELMOD proteins in mammalian cells have a highly conserved region with an invariant arginine that is essential for GAP activity on Arf family proteins in vitro. The Arabidopsis ELMOD family proteins investigated in this study (MCR and ELMOD_A) have the same conserved region with the invariant arginine, mutation of which abolished their capacity to complement phenotypes of mutants in Arabidopsis. These results support the conclusion that ELMOD proteins are Arf GAPs in plants. This paper shows that Arl8 promotes the localization of endolysomes towards the cell center in different cell types, and identifies RUFY3 and RUFY4 as effectors of Arl8 that mediate this effect through interaction with the dynein microtubule motor. The authors show that RUFY3 and RUFY4 interact with dynein-dynactin in cells, and using purified proteins, they demonstrate that RUFY3 interacts directly with dynein light intermediate chain 1 (DLIC1). The authors showed that RUFY3 is required for movement of endolysosomes toward the cell center upon cytosol alkalinization. This tree is based on a synthesis of recent phylogenomic literature and shows the consecutive divergence of "side" lineages along the evolutionary paths towards the two focal taxa. Three types of evolutionary events shaping the Arf family are mapped onto the paths: loss of a particular gene; emergence of a "novel" Arf family member, which equals a duplication of one of the pre-existing genes followed by substantial divergence of one of the duplicates (when know, the parental gene is indicated in brackets, with an arrow pointing to the "novel" descendant gene); gene duplication, which corresponds to situations where the fate of the duplicates was more symmetrical (in terms of sequence divergence) than in the previous case. For the duplications, the resulting genes are listed (separated with a slash), with one of the descendants retaining the name of the parental gene (then listed first; eg. the Arf1/Arf4 pair in early Holozoa emerged by duplication of the ancestral Arf1 gene) or with the descendants designated by the name of the parental name extended by a suffix ( Sar1a and Sar1b resulting from duplication of the parental Sar1 gene). The history of the Arf family as presented in the figure is based on results reported by Vargová et al. [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF] and Dewees et al. [53], with substantial updates based on checking the occurrence of the different Arf family members in additional eukaryote lineages that were not previously analysed. Briefly, for Arf family genes previously inferred to have been lost at a particular node of the yeast or human evolutionary lineages, the possible presence of putative orthologs was probed in previously untested taxa descendant to the respective node.

Analogously, for Arf family members previously inferred to be evolutionary novelties of a particular organismal clade, the possible presence of orthologs was checked in the previously unsampled outgroup taxa. As a result, losses or origins of certain Arf family genes were thus pushed to more recent or older nodes, respectively. For instance, SarB, which was previously thought to have been lost already prior to the emergence of opisthokonts [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF], was now newly identified in several opisthokont taxa (Nucleariida, Filasterea, Choanoflagellata), indicating it was lost independently in the early history of the Holomycota and Holozoa lineages. Similar re-evaluations implying a more recent loss concern Arl17 (not previously known to occur in basal holozoan lineages including sponges) and Arl19 (now identified in multiple vertebrate lineages including monotreme mammals).

On the other hand, Arl15 and Arl19 now seem to have emerged already in the stem branch major medically relevant organisms, with the diseases caused given after the hyphen in such cases. The diagram is not to scale. Note that the different groups highlighted are not at equivalent levels, and as in Figure 2, the Holomycota and Holozoa lineages are highlighted (left). Losses, duplications, and convergent gene fusions of GAP and GEF families are mapped, noting that only the losses explicitly stated in the text are mapped on the tree. Symbols, and colouration is as in the inset legend.

  ) [7]. Arf1, Arl1 and Arl5 share the function of recruiting tethers to Golgi membranes: coiled-coil tethers by Arf1 and Arl1, and multisubunit tethers by Arl5 [5,50,51]. Interestingly, Arfrp1 acts upstream of both Arl1 and Arl5 to coordinate recruitment of coiled-coil golgin tethers to the Golgi by Arl1 and multisubunit tethers by Arl5 [51], and has been shown to promote secretion of insulin [52]. Four families of Arf family proteins present in LECA, Arl3, Arl6, Arl13 and Arl16, have primary functions in cilia and flagella. It was only with the extensive phylogenetic analyses of Arf family proteins that the ciliary function of Arl16 was uncovered [53]. Arl16 localizes to cilia in mammalian cells, and its deletion in mouse or human cells causes defects in cilia formation and morphology, at least in part due to a defect in trafficking of certain ciliary proteins from the Golgi to the cilium [53]. Arl3 and Arl13b have well-established functions in mediating localization of lipidated and transmembrane proteins to the cilium [13]. BBSomes are structures that are transported along the axonemal microtubules to the tip of the cilium,

  8. Fansa EK, Wittinghofer A: Sorting of lipidated cargo by the Arl2/Arl3 system. Small GTPases 2016, 7:222-230. **9. ElMaghloob Y, Sot B, McIlwraith MJ, Garcia E, Yelland T, Ismail S: ARL3 activation requires the co-GEF BART and effector-mediated turnover. eLife 2021, 10:e64624.

  10. Barlowe C, Schekman R: SEC12 encodes a guanine-nucleotide-exchange factor essential for transport vesicle budding from the ER. Nature 1993, 365:347-349. 11. Pipaliya SV, Schlacht A, Klinger CM, Kahn RA, Dacks J: Ancient complement and lineagespecific evolution of the Sec7 ARF GEF proteins in eukaryotes. MBoC 2019, 30:1846-1863. 12. Yu C-J, Lee F-JS: Multiple activities of Arl1 GTPase in the trans-Golgi network. Journal of Cell Science 2017, 130:1691-1699. 13. Gotthardt K, Lokaj M, Koerner C, Falk N, Gießl A, Wittinghofer A: A G-protein activation cascade from Arl13B to Arl3 and implications for ciliary targeting of lipidated proteins. eLife 2015, 4:e11859. 14. Hsu J-W, Chen K-J, Lee F-JS: Snf1/AMP-activated protein kinase activates Arf3p to promote invasive yeast growth via a non-canonical GEF domain. Nat Commun 2015, 6:7840. *15. Chen K-J, Hsu J-W, Lee F-JS: AMPK promotes Arf6 activation in a kinaseindependent manner upon glucose starvation. Journal of Cell Science 2022, 135:jcs259609.

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 16 Feng H-P, Cheng H-Y, Hsiao T-F, Lin T-W, Hsu J-W, Huang L-H, Yu C-J: ArfGAP1 acts as a GTPase-activating protein for human ADP-ribosylation factor-like 1 protein. The FASEB Journal 2021, 35:e21337.

  17. Schlacht A, Mowbrey K, Elias M, Kahn RA, Dacks JB: Ancient Complexity, Opisthokont Plasticity, and Discovery of the 11th Subfamily of Arf GAP Proteins. Traffic 2013, 14:636-649. 18. Ivanova AA, East MP, Yi SL, Kahn RA: Characterization of Recombinant ELMOD (Cell Engulfment and Motility Domain) Proteins as GTPase-activating Proteins (GAPs) for ARF Family GTPases. Journal of Biological Chemistry 2014, 289:11111-11121. 19. East MP, Bowzard JB, Dacks JB, Kahn RA: ELMO Domains, Evolutionary and Functional Characterization of a Novel GTPase-activating Protein (GAP) Domain for Arf Protein Family GTPases. Journal of Biological Chemistry 2012, 287:39538-39553. 20. Veltel S, Gasper R, Eisenacher E, Wittinghofer A: The retinitis pigmentosa 2 gene product is a GTPase-activating protein for Arf-like 3. Nat Struct Mol Biol 2008, 15:373-380. 21. Su M-Y, Fromm SA, Zoncu R, Hurley JH: Structure of the C9orf72 ARF GAP complex that is haploinsufficient in ALS and FTD. Nature 2020, 585:251-255. **22. Su M-Y, Fromm SA, Remis J, Toso DB, Hurley JH: Structural basis for the ARF GAP activity and specificity of the C9orf72 complex. Nat Commun 2021, 12:3786.

* 31 .

 31 Billington K, Halliday C, Madden R, Dyer P, Barker AR, Moreira-Leite FF, Carrington M, Vaughan S, Hertz-Fowler C, Dean S, et al.: Genome-wide subcellular protein map for the flagellate parasite Trypanosoma brucei. Nat Microbiol 2023, 8:533-547.This open resource reports the subcellular localization of 89% of the encoded proteome (7766 proteins) of Trypanosoma brucei, one of the best developed molecular cell biological systems outside of animals, plants and fungi. A searchable database allows localization data to be obtained for proteins of interest for comparative cell biology.

FiguresFigure 1 .

 1 Figures

Figure 2 .

 2 Figure 2. The evolutionary trajectory of the Arf family from the last eukaryotic common ancestor (LECA) to budding yeast (S. cerevisiae) and humans. The schematic phylogenetic

Figure 3 .

 3 Figure 3. Evolution of Arf GAPs and GEFs across eukaryotes. This cartoon illustrates a highly simplified depiction of the eukaryotic tree. Some of the major groups of eukaryotes, and their interrelationships are shown, with emphasis on specific examples from the text or on

Acknowledgements

CLJ and JM were supported by grant ANR-20-CE13-0007 from the ANR, France, and the CNRS, France. JBD was supported by NSERC Canada Discovery Grants RES0043758 and RES0046091. The evolutionary studies of GTPases in the lab of ME were supported by the Czech Ministry of Education ERD Funds projects OPVVV 16_013/0001775.

Data availability

Newly identified and analysed Arf family genes that were used to prepare Figure 2 are available at Figshare XXXXXX (URL to be added in revision).

Author contributions CLJ, JM, JBD, ME: Conceptualization, visualisation and writing: MS: conceptualization and visualization

Declarations of interest: none of Holozoa, i.e. earlier than reconstructed previously, owing to their identification in previously untested representatives of the basal holozoan lineages. The assignment of Arf family genes in the newly analysed taxa to specific Arf family members was primarily based on BLAST searches against the curated sequence set reported by Vargová et al. [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF], combined in some cases with the inspection of intron positions (which proved instrumental in defining orthologous relationships in some cases where sequence comparisons or standard phylogenetic analyses did not provide sufficient resolution [START_REF] Vargová | A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family[END_REF]). The newly identified Arf family genes with details on the sequence sources are listed in supplementary Table S1 available XXXXX (URL to be added in revision). The set of gene duplications mapped to early vertebrate evolution (prior to the divergence of Chondrichthyes) presumably results from two WGD rounds, as follows from consulting the OHNOLOGS version 2.0 database (http://ohnologs.curie.fr/; [START_REF] Singh | OHNOLOGS v2: a comprehensive resource for the genes retained from whole genome duplication in vertebrates[END_REF]). The relation of the duplications with respect to the divergence of jawless vertebrates (cyclostomes) remains unclear, as indicated in the figure by the dashed lines connecting cyclostomes to the vertebrate main trunk at two alternative positions.

Declaration of interests

☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:


Hamza Ighnih
email: hamza.ighnih@edu.uiz.ac.ma

Redouane Haounati

Rahime Eshaghi Malekshah

Hassan Ouachtak
email: ouachtakhassan@gmail.com

Yahya Toubi

Fadi Alakhras

Amane Jada
email: amane.jada@uha.fr

Abdelaziz Ait Addi

Rahime Eshaghi Malekshah

Kaol: Experimental and molecular dynamic simulation studies

Keywords: Kaolinite, BiOBr, Co-precipitation, RhB dye, photocatalysis, sunlight, theoretical calculations

Sunlight driven photocatalytic degradation of RhB dye using composite of bismuth oxy-bromide kaolinite

BiOBr@

Introduction

Nowadays, with the rapid increase of the industrial sector, the volume of wastewater generated by this sector is strongly increasing [START_REF] Haounati | Elaboration and properties of a new SDS/CTAB@Montmorillonite organoclay composite as a superb adsorbent for the removal of malachite green from aqueous solutions[END_REF][START_REF] Ighnih | Efficient removal of hazardous dye from aqueous solutions using magnetic kaolinite nanocomposite: Experimental and Monte Carlo simulation studies[END_REF]. Wastewater from sewage plants often contains toxic organic compounds that are difficult to biodegrade [START_REF] Liu | Synthesis of sodium dodecyl sulfate modified BiOBr/magnetic bentonite photocatalyst with Three-dimensional parterre like structure for the enhanced photodegradation of tetracycline and ciprofloxacin[END_REF]. Among these organic compounds, the Rhodamine B dye (RhB) has garnered attention due to its hazardous effects [START_REF] Ouachtak | Experimental and molecular dynamics simulation study on the adsorption of Rhodamine B dye on magnetic montmorillonite composite γ -Fe 2 O 3 @ Mt[END_REF][START_REF] Alakhras | A comparative study of photocatalytic degradation of Rhodamine B using natural-based zeolite composites[END_REF]. RhB is highly toxic, carcinogenic, and possesses a stable molecular structure in aqueous media, which makes it resistant to biodegradation and poses a significant threat to human health and the environment [START_REF] Ahmad | Enhanced photocatalytic degradation of RhB dye from aqueous solution by biogenic catalyst Ag@ZnO[END_REF][START_REF] Ouachtak | Highly efficient and fast batch adsorption of orange G dye from polluted water using superb organo-montmorillonite: Experimental study and molecular dynamics investigation[END_REF].

The use of reliable and sustainable treatment methods for the industrial wastewater should be necessary to achieve depollution and facilitate the reuse of purified water [START_REF] Ouachtak | 3,4dihydroxybenzoic acid removal from water by goethite modified natural sand column fixed-bed: Experimental study and mathematical modeling[END_REF][START_REF] Ouachtak | Combined molecular dynamics simulations and experimental studies of the removal of cationic dyes on the ecofriendly adsorbent of activated carbon decorated montmorillonite Mt@AC[END_REF][START_REF] Largo | Design of organically modified sepiolite and its use as adsorbent for hazardous Malachite Green dye removal from water[END_REF]. Various techniques, such as adsorption [START_REF] Imgharn | Synthesis and characterization of polyanilinebased biocomposites and their application for effective removal of Orange G dye using adsorption in dynamic regime[END_REF], coagulation-flocculation [START_REF] Zhao | Application of coagulation/flocculation in oily wastewater treatment: A review[END_REF], and membrane technology [START_REF] Yusaf | Micellar-enhanced ultrafiltration (MEUF) for removal of rhodamine B (RhB) from aqueous system[END_REF], have been employed to remove toxic organic compounds. However, these methods primarily concentrate the pollutants on a substrate without breaking down the organic molecules. In contrast, advanced oxidation processes (AOPs) have gained significant attention from researchers worldwide due to their cost-effectiveness, practical applicability, ease of use, and high efficiency in water mineralization [START_REF] Miklos | Evaluation of advanced oxidation processes for water and wastewater treatment -A critical review[END_REF][START_REF] Kanakaraju | Advanced oxidation process-mediated removal of pharmaceuticals from water: A review[END_REF][START_REF] Ma | Critical review of advanced oxidation processes in organic wastewater treatment[END_REF]. Heterogeneous photocatalysis has emerged as one of the most effective advanced oxidation processes (AOPs) for wastewater treatment and complete degradation of organic pollutants, particularly dyes [START_REF] Haounati | Synthesized of Zeolite@Ag2O Nanocomposite as Superb Stability Photocatalysis Toward Hazardous Rhodamine B Dye from Water[END_REF]. This technology is based on the principle of exciting a semiconductor material using an artificial or natural radiation source [START_REF] López | Photocatalytic diphenhydramine degradation under different radiation sources: Kinetic studies and energetic comparison[END_REF]. Upon excitation, the semiconductor generates electron-hole pairs (e-and h+), which in turn generate reactive species such as hydroxyl radicals ( • HO) and superoxide radicals ( • O2 -) [START_REF] Méndez-Arriaga | Photocatalytic degradation of nonsteroidal anti-inflammatory drugs with TiO2 and simulated solar irradiation[END_REF]. These radicals play a crucial role in the photodegradation of pollutants, converting them into harmless products such as water (H2O) and carbon dioxide (CO2).

Recently, various semiconductors (photocatalysts) have been utilized in the photodegradation process for removing toxic organic compounds, including g-C3N4 [START_REF] Zhao | A critical review on graphitic carbon nitride ( g-C 3 N 4 ) -based composites for environmental remediation[END_REF], Ag/AgBr [START_REF] Tun | Facile preparation of visible-lightresponsive kaolin-supported Ag @ AgBr composites and their enhanced photocatalytic properties[END_REF], Ag2O [START_REF] Haounati | Synthesized of Zeolite@Ag2O Nanocomposite as Superb Stability Photocatalysis Toward Hazardous Rhodamine B Dye from Water[END_REF], ZnO [START_REF] Oyewo | Sawdust-Based Cellulose Nanocrystals Incorporated with ZnO Nanoparticles as E ffi cient Adsorption Media in the Removal of Methylene Blue Dye[END_REF], TiO2 [START_REF] Cavalcante | Photocatalytic mechanism of metoprolol oxidation by photocatalysts TiO2 and TiO2 doped with 5% B: Primary active species and intermediates[END_REF]. Hence, these photocatalysts have several drawbacks that limit their application, such as, high cost, electron-hole recombination, lower efficiency, and difficulties in regeneration [START_REF] Zhao | Synthesis of bismuth oxyiodide/kaolinite composite with enhanced photocatalytic activity[END_REF]. Bismuth-based semiconductors [START_REF] Tan | Preparation and photocatalytic activity of BiOBr/TiO2 heterojunction nanocomposites[END_REF] such as BiPO4 [START_REF] Kumar | Recent progress in emerging BiPO4based photocatalysts: Synthesis, properties, modification strategies, and photocatalytic applications[END_REF], BiVO4, Bi2WO6, Bi2MoO6 [START_REF] Liu | BiVO4, Bi2WO6 and Bi2MoO6 photocatalysis: A brief review[END_REF], BiFeO3 [START_REF] Irfan | Critical review: Bismuth ferrite as an emerging visible light active nanostructured photocatalyst[END_REF], Bi4Ti3O12 [START_REF] Chen | Chromium-modified Bi4Ti3O12 photocatalyst: Application for hydrogen evolution and pollutant degradation[END_REF], as well as BiOBr have been synthesized and utilized in photocatalytic applications. Among them, BiOBr semiconductor has gained significant attention due to its stability, non-toxicity, corrosion resistance, superior electrical conductivity, unique structure (Fig. 1-a), good photocatalytic performance, and suitable band gap for various applications [START_REF] Zhao | Modulation of BiOBr-based photocatalysts for energy and environmental application: A critical review[END_REF][START_REF] Imam | The photocatalytic potential of BiOBr for wastewater treatment: A mini-review[END_REF][START_REF] Chang | Photodegradation of Rhodamine B over unexcited semiconductor compounds of BiOCl and BiOBr[END_REF][START_REF] Meng | Recent advances in BiOBr-based photocatalysts for environmental remediation[END_REF]. However, pure BiOBr photocatalyst suffers from issues such as agglomeration in solution, low photo-generated charge separation, lengthy treatment time, and limited photocatalytic power under sunlight, which have hindered its practical applications [START_REF] Liu | Synthesis of sodium dodecyl sulfate modified BiOBr/magnetic bentonite photocatalyst with Three-dimensional parterre like structure for the enhanced photodegradation of tetracycline and ciprofloxacin[END_REF]. To address these challenges, several studies have made significant efforts to enhance the performance of pure BiOBr by forming heterojunctions with other photocatalytic semiconductors, such as BiOBr/TiO2 [START_REF] Tan | Preparation and photocatalytic activity of BiOBr/TiO2 heterojunction nanocomposites[END_REF], ZnO/BiOBr [START_REF] Yang | Ultrasonic-microwave synthesis of ZnO/BiOBr functionalized cotton fabrics with antibacterial and photocatalytic properties[END_REF], BiOBr/g-C3N4 [START_REF] Tian | Facile assembly and excellent elimination behavior of porous BiOBr-g-C3N4 heterojunctions for organic pollutants[END_REF]. However, these solutions are cost-intensive and not applicable under sunlight. A potential solution to improve the photocatalytic performance is the utilization of pure BiOBr catalysts under solar light irradiation with the aid of natural clay minerals [START_REF] Haounati | Z-Scheme g-C3N4/Fe3O4/Ag3PO4@Sep magnetic nanocomposites as heterojunction photocatalysts for green malachite degradation and Dynamic molecular studies[END_REF], including montmorillonite [START_REF] Xu | Efficient adsorption and photocatalytic degradation of Rhodamine B under visible light irradiation over BiOBr/montmorillonite composites[END_REF], sepiolite [START_REF] Wang | Photocatalytic degradation of rhodamin B and diclofenac sodium on hollow hierarchical microspheres of BiOBr modified with sepiolite and polyvinyl pyrrolidone (PVP)[END_REF], have been employed to address issues such as easy agglomeration and electronhole pair recombination in BiOBr semiconductors. However, the use of kaolinite clay as a carrier for BiOBr semiconductor shows the enhancement photocatalytic performance under sunlight irradiation due to the higher surface area allows for increased adsorption, the interface promotes efficient charge transfer and separation of photogenerated electron-hole pairs, the stability and reusability of the photocatalyst [START_REF] Cao | Recent advances in kaolinite-based material for photocatalysts[END_REF][START_REF] Ighnih | Photocatalytic degradation of RhB dye using hybrid nanocomposite BiOCl@Kaol under sunlight irradiation[END_REF].

In this study, BiOBr@Kaolinite nanocomposite photocatalysts were successfully synthesized using a facile co-precipitation method in an acidic medium. The synthesized nanocomposites were characterized using various techniques. X-ray diffraction (XRD) was employed to study the structures, Fourier-transform infrared spectroscopy (FT-IR) was performed to determine the crystal phase, Scanning Electron Microscopy (SEM) was used to observe the topography, Transmission Electron Microscopy (TEM) was utilized to visualize the morphologies and nanostructures, X-ray photoelectron spectroscopy (XPS) was used to identify chemical species at the surface, UV-vis Diffuse Reflectance Spectroscopy (DRS) to study the optical properties and bang gape energy. The characterized samples were then tested for their ability to degrade the hazardous RhB dye in an aqueous solution under sunlight irradiation.

Additionally, molecular dynamics (MD) and Density Functional Theory with dispersion correction (DFT-D) simulations, as well as adsorption calculations based on Monte Carlo, were applied in this study.

Material and methods

Photocatalysts preparation

Materials and reagents

The natural kaolinite clay, the bismuth nitrate pentahydrate extra-pure, the glacial acetic acid (CH₃CO2H ≥ 99.95%) and rhodamine B (RhB) used in this study were purchased from Sigma-Aldrich, while sodium bromide (NaBr ≥ 99.5%) was obtained from Scharlau. All these chemical reagents were applied without any further purification.

Preparation of BiOBr and BiOBr@Kaol

The BiOBr@Kaol was prepared using the co-precipitation method in an acidic medium. Firstly, 3.3 mmol of bismuth nitrate pentahydrate extra-pure was dissolved completely in 40 mL of glacial acetic acid/ deionized water (1:1) solution at 25 °C for 1 h to obtain a transparency liquid. After that, 1 g of kaolinite clay was added to the solution and stirred for 1 hour (Solution A). Another solution of sodium bromide was prepared by dissolving of 3.3 mmol of NaBr in 30 mL of deionized water under vigorous stirring for 30 min (solution B).

Then, solution B was slowly added to solution A under vigorous stirring for 5 h. Finally, the precipitate was filtered, washed three times with distilled water and ethanol, and dried at 70 ºC for 12 h and signed BiOBr@1.0Kaol. According to this procedure, BiOBr@Kaol composites with a different mass of kaolinite (0.2, 0.4, 0.6, and 0.8 g) were synthesized and named as BiOBr@0.2Kaol, BiOBr@0.4Kaol, BiOBr@0.6Kaol, and BiOBr@0.8Kaol, respectively. The same way was applied for the synthesis of a pure BiOBr without adding kaolinite.

Samples characterization

The phase and crystallinity of the kaolinite and the prepared photocatalysts were investigated using X-ray diffraction (Bruker D8 Twin) with monochromatic λ(KαCu) = 1.5418 Å radiation at a step size of 0.05° and a scan rate of 1 s/step. The functional groups were analyzed in the wavenumber region from 400 to 4000 cm -1 using Fourier Transform Infrared Spectroscopy (Shimadzu spectrometer equipped with a Jasco ATR PRO ONE). The morphology and microstructure were analyzed by scanning electron microscopy (Supra 40 VP Gemini Zeiss Column, with a maximum voltage of 20 kV), and the elemental compositions of the nanocomposite were determined by recording their Energy Dispersive X-ray (EDX) spectra.

The high resolution of the catalysts was analyzed by transmission electron microscopy (TEM). The chemical compositions and electronic states were characterized using X-ray photoelectron spectroscopy (XPS). The band gap of the as-synthesized catalysts was measured using UV-Vis diffuse reflectance spectra with a Lambda de PerkinElmer instrument.

Photocatalysis processes

The photocatalytic degradation of RhB dye in aqueous solution over as-prepared nanocomposites was investigated under sunlight irradiation that performed in the month of April 2022 between 11:40 A.M. and 12:40 P.M. 100 mL of RhB dye (10 mg/L) solutions were mixed in a reactor with 100 mg of the photocatalyst. Prior to sunlight irradiation, the reactor was maintained in the dark for one hour until an adsorption-desorption equilibrium was established between RhB dye and the photocatalyst. Under the sunlight irradiation, 4 mL of the solution was collected each 5 min, centrifuged, and the concentration of residual RhB dye was measured using a UV spectrometer (UV-1800, SHIMADZU), at the wavelength of 554 nm. The degradation efficiency (%) and the rate constants K (min -1 ) are calculated using Equations 1 and 2, respectively:

(1) (2)
Herein, C0 and Ct are the concentrations of the RhB dye at the initial and any time during photodegradation, respectively. K (min -1 ) is the constant of the first-order reaction.

Calculation methods

Model Construction

Computational method

The electronic structures of typical Kaol, BiOBr and RhB were simulated using DFT-D method implementing DMol 3 in Materials Studio 2017. The electron exchange-correlation energy of compunds was carried out by the generalized gradient approximation (GGA) developed by Perdew-Burke-Ernzerhof (PBE) in addition to the DFT-D correction. After optimization, to obtain the optimal adsorption sites and directions of BiOBr on Kaol (0 0 1) and RhB on BiOBr@Kaol surfaces, Monte Carlo simulations were performed with universal force field that the number of cycles and the van der Waals interactions were calculated under 10 cycles and the Group-based option at a cutoff of 12.5 Å. The hydroxyl groups of Alterminated for the (0 0 1) surface and oxygen and silicon atoms for the (0 01) surface of Kaolinite were free [START_REF] Salahshoori | Elevated performance of the neat , hybrid and composite membranes by the addition of nanoparticles ( ZIF-67 ): A molecular dynamics study[END_REF].

Results and discussion

X-ray diffraction (XRD)

Figure 4 displays the X-ray diffraction of the synthesized materials pure "BiOBr, BiOBr@xKaol (x= 0.2, 0.4, 0.6, 0.8 and 1) and raw kaolinite". The XRD patterns of the raw kaolinite are represented in black, it can be observed that the diffraction peaks located at 2θ = 12.35°, 20.35°, 24.85°, 26.6°, 37.7°, and 62.25° were assigned to the planes (001), ( 110), (002), (003), and (031) according to the card (JCPDS No. 96-900-9235). XRD patterns of the pure BiOBr showed the principal diffraction peaks situated at 2θ=10.9°, 21.92°, [START_REF] Tan | Preparation and photocatalytic activity of BiOBr/TiO2 heterojunction nanocomposites[END_REF] 002), ( 101), ( 102), ( 110), ( 112), ( 004), ( 200), ( 113), ( 201), ( 104), ( 211), ( 114), ( 212), ( 105), (204), and (220) lattice planes, respectively. This is indexed to the Tetragonal structure according to the (JCPDS card no. 01-078-0348). However, it can be seen from the plots of all the mass ratio of photocatalytic nanocomposites that as the mass of kaolinite increases, the peak intensity of the plans (001), ( 002), ( 101), (102), of the BiOBr phase, and (001), (002), of the kaolinite also increases. This increment can be explained by the increased crystalline due to the increasing amount of kaolinite [START_REF] Ighnih | Photocatalytic degradation of RhB dye using hybrid nanocomposite BiOCl@Kaol under sunlight irradiation[END_REF][START_REF] Dlamini | Photocatalytic abatement of phenol on amorphous TiO2-BiOBr-bentonite heterostructures under visible light irradiation[END_REF]. In addition, the intensity of BiOBr peaks was always higher than those of kaolinite peaks, and some peaks of kaolinite were missing in all nanocomposites, indicating that the kaolinite surface was recovered by the BiOBr nanosheets, owing to the adsorption capacity of the layered aluminosilicate of kaolinite [START_REF] Chuaicham | Efficient photocatalytic degradation of emerging ciprofloxacin under visible light irradiation using BiOBr/carbon quantum dot/saponite composite[END_REF]. The results indicate that the nanocomposites were successfully synthesized.

• • • • • • • • • • • • • • Kaolinite BiOBr Kaolinite BiOBr • BiOBr@0.2Kaol
BiOBr@0.4Kaol BiOBr@0.6Kaol BiOBr@0.8Kaol BiOBr@1.0Kaol

Figure 4: XRD of raw kaolinite and as-prepared photocatalysts.

Fourier transform infrared

Fourier transform infrared spectroscopy (FTIR) of raw kaolinite, pure BiOBr and assynthesized BiOBr@Kaol are investigated in the range of 400-4000 cm -1 (Figure 5). The spectra of raw kaolinite (Figure 5a), showed the characteristics band at 3618.45 cm -1 and 3697.54 cm -1 which is attributed to the stretching vibration mode of Aluminum hydroxide (Al-OH) and silicon hydroxide (Si-OH) group, respectively [START_REF] Zhao | Synthesis of bismuth oxyiodide/kaolinite composite with enhanced photocatalytic activity[END_REF]. The characteristics peaks at 1116 cm -1 and 1007 cm -1 are allocated to the stretching vibration mode of Si-O group. The bands at 536 cm -1 and 785 cm -1 are assigned to Al-O-Si deformation [START_REF] Sun | Enhanced visible-light photocatalytic activity of kaolinite / g-C 3 N 4 composite synthesized via mechanochemical treatment[END_REF]. Furthermore, the characteristics bands located at 468.70 cm -1 and 1029 cm -1 are associated by the deformation modes of Si-O-Si group [START_REF] Abukhadra | Enhancing the removal of organic and inorganic selenium ions using an exfoliated kaolinite / cellulose fibres nanocomposite[END_REF]. The FT-IR spectra of pure BiOBr presented the characteristic peaks located at 421.37 cm -1 is attributed to vibration of Bi-Br. The detection of Bi-O functional group is confirmed by the characteristic band at 518 cm -1 [START_REF] Liu | Synthesis of sodium dodecyl sulfate modified BiOBr/magnetic bentonite photocatalyst with Three-dimensional parterre like structure for the enhanced photodegradation of tetracycline and ciprofloxacin[END_REF]. The FT-IR spectrum of BiOBr@Kaol nanocomposites contains the functional groups of raw kaolinite and BiOBr confirmed the successful elaboration.

4000

Wavenumber (cm -1 )

Figure 5: FT-IR spectra of raw kaolinite (a), BiOBr@0.2Kaol (b), BiOBr@0.4Kaol (c), BiOBr@0.6Kaol (d), BiOBr@0.8Kaol (e), BiOBr@1.0Kaol (f), and pure BiOBr (g).

Scanning electron microscopy & high resolution TEM

Figure 6 shows the surface image and elementary compositions of raw kaolinite and assynthesized photocatalyst, as investigated by scanning electron microscopy and energydispersive X-ray spectroscopy (EDX). The SEM image and EDX spectrum of kaolinite clay mineral exhibits a stacking of many micro-sized layered structures of alumina octahedron and siloxane tetrahedron, the elementary composition of raw kaolinite is Al, Si, and O, which are well dispersed (as can be seen in Figure 5(a,b,c). Moreover, the SEM image of pure BiOBr displayed in Figure 6d and6e, showed the assembled of many with a morphology similar to that of a lotus flower, with diameter size about 3-6.2 µm. In addition, the EDX spectrum and mapping micrographic of pure BiOBr (Figure 6f)), indicated that the proportion of element Bi, O, and Br are equal and evenly dispersed. The SEM image of nanocomposite BiOBr@0.4Kaol, (Figure 6g and6h) showed that the BiOBr catalysis was supported on kaolinite surface. Additionally, EDX analysis and mapping image in Figure 6-i, revealed that the nanocomposite surface is homogenous due to the best distribution of all elements of pure BiOBr and raw kaolinite.

The micrograph in Figure 6j shows a 2D nanolayer of raw kaolinite in a pseudohexagonal form with a smooth and homogeneous surface. The diameter of these layers' ranges is between 400-900 nm. The TEM image in Figure 6k shows BiOBr holey nanosheets with a diameter size between 100 nm to 500 nm stacked together. Moreover, the TEM image in c), pure BiOBr (d, e, f) Kaol@BiOBr (g, h, i). HRTEM of kaolinite (j), BiOBr (k) and BiOBr@Kaol (l).

Chemical state and surface structure analysis

The chemical compositions and chemical states of raw kaolinite, pure BiOBr and BiOBr@Kaol were analyzed using X-ray photoelectron spectroscopy (XPS) in the range of 0-1000 eV. Figure 7 shows XPS spectra of BiOBr@Kaol, indicating the presence of Al, Si, O, Bi, Br and C elements. The high-resolution XPS spectra of Bi 4f exhibit two powerful peaks located at 157.1 eV and 162.4 eV corresponding to Bi 3+ 4f7/2 and Bi 3+ 4f5/2 orbitals of BiOBr in the BiOBr@Kaol composite, respectively (Figure 7b) [START_REF] Wang | One-pot preparation of novel Bi/BiOBr/Bi2O2CO3 heterojunction for pollutant degradation under visible light: Catalyst generation insights, reaction mechanism, degradation pathways, and toxicological effects[END_REF]. The high-resolution XPS spectrum of Br 3d (Figure 7c), shows two peaks at binding energies of 65.5 eV and 66.5 eV, assigned to Br -1 3d5/2 and Br -1 3d3/2, respectively [START_REF] Zhao | 3D BiOBr/BiOCl heterostructure microspheres with enhanced photocatalytic activity[END_REF]. In Figure 7d, the high-resolution XPS spectrum of O 1s, exhibits two peaks at 528.6 eV and 530.5 eV, corresponding to the B-O and Bi-OH bands, respectively [START_REF] Zhao | Synthesis of bismuth oxyiodide/kaolinite composite with enhanced photocatalytic activity[END_REF][START_REF] Wang | Synergistic enhancement of the visible-light photocatalytic activity of hierarchical 3D BiOClxBr1-x/graphene oxide heterojunctions for formaldehyde degradation at room temperature[END_REF]. The high-resolution XPS spectrum of Al 2p (Figure 7e), shows two peaks at 735 eV and 74.3 eV ascribed the Al 2p1/2 an Al 2p3/2 orbitals sates.

Figure 7f

, presents the high-resolution XPS spectrum of Si 2p, where the observed peaks at binding energies 100.8 eV are depicted the Si-O-Si band [START_REF] Zhang | Synthesis of BiOCl/TiO2-zeolite composite with enhanced visible light photoactivity[END_REF].

Comparing the XPS spectra of pure BiOBr and BiOBr@Kaol (Figure 7b and 7d), it is evident that the peaks corresponding to electronic states Bi 3+ 4f7/2, Bi 3+ 4f5/2 and O 1s (B-O band) exhibit a positive shift from 156.4 eV, 161.6 eV, and 527.1 eV, in pure BiOBr to 157.1 eV, 162.4 eV and 528.6 eV in BiOBr@Kaol, respectively. This shift can be attributed to the strong interfacial interaction between BiOBr and kaolinite [START_REF] Yang | Ternary hetero-structured BiOBr/Bi2MoO6@MXene composite membrane: Construction and enhanced removal of antibiotics and dyes from water[END_REF][START_REF] Lin | Self-cleaning photocatalytic MXene composite membrane for synergistically enhanced water treatment: Oil/water separation and dyes removal[END_REF]. The interaction between the two materials leads to hybridization of electronic states and charge transfer phenomena at the interface, resulting in changes in electron density and binding energies of the elements involved. Moreover, the shift of the, O 1s peak from 528.3 eV to 530.5 eV and the increased intensity of the Bi-OH band in confirm the a strong interaction between pure BiOBr and hydroxide groups in the kaolinite surface, indicating the successful synthesis of the BiOBr@Kaolinite composite.

As shown in figure 7b, two low intensity peaks located at the binding energies of 154 eV and 159.4 eV are corresponded to the Bi 4f7/2 and Bi 4f5/2 states of the bismuth element. However, in the case of BiOBr@Kaolinite, it is noted that the Bi 4f7/2 and Bi 4f5/2 feature peaks are not clearly observed. This could be attributed to several factors, including the modification of the kaolinite surface, interaction between the bismuth species and kaolinite, or changes in the oxidation state of bismuth in the composite material. Further investigation and analysis are required to fully understand and explain the absence or alterations of these characteristic peaks in BiOBr@Kaolinite compared to pure BiOBr.

Optical properties and band gap energy

The band structure and band gap energy of semi-conductor are important indicators to evaluate the photocatalysis mechanism. Figure 8 displays the UV-vis diffuse reflectance spectra (DRS) of as-synthesized photocatalyst. It can be seen from the Figure 8a, that the raw kaolinite, pure BiOBr, BiOBr@0.2Kaol, BiOBr@0.4Kaol, BiOBr@0.6Kaol, BiOBr@0.8Kaol and BiOBr@1.0Kaol exhibited an absorption edge at about 420, 475, 460, 450, 453, 455, 470 nm, respectively. This indicates that, all samples have a great absorption in the visible and UV regions. In addition, BiOBr@0.4Kaol has a best absorption boundary when compared with other samples. The data provided by UV-vis DRS were used to determinate the band gap energy of samples, using the following equation 3.

(

Si 2p

Intensity (a.u.)

Binding energy (eV) Where α, hν, β and Eg are the absorption coefficient, the photon energy, the band tailing parameter and the band gap energy, respectively. For the value of n, it depends on the property of the semiconductor (n=1 or 4 for direct band gap or indirect band gap separately).

For a semiconductor with indirect band gap, BiOBr, the value of n is 4. The results were plotted in Figure 8b, the band gap energy (Eg) value of raw kaolinite, pure BiOBr, BiOBr@0.2Kaol, BiOBr@0.4Kaol, BiOBr@0.6aol, BiOBr@0.8Kaol, BiOBr@1.0Kaol, were (αhυ)^1/2 (eV^0.5)

hυ (eV)

Kaolinite BiOBr BiOBr@0.2Kaol BiOBr@0.4Kaol BiOBr@0.6Kaol BiOBr@0.8Kaol" BiOBr@1.0Kaol

Figure 8: UV-vis diffuse reflectance spectra of raw kaolinite, pure BiOBr, BiOBr@0.2Kaol, BiOBr@0.4Kaol, BiOBr@0.6Kaol, BiOBr@0.8Kaol, BiOBr@1.0Kaol and (b) plot of (αhν) 2 versus hν of as prepared sample.

Photocatalytic degradation study

The compared photocatalytic performance of as-prepared photocatalysts: pure BiOBr, BiOBr@1.0Kaol, BiOBr@0.8Kaol, BiOBr@0.6Kaol, BiOBr@0.4Kaol, and BiOBr@0.2Kaol, were investigated by employing 100 mL of RhB dye (10 ppm) with 100 mg of photocatalysts under sunlight irradiation. Figure 9, Shows the photolysis test, the adsorption-desorption equilibrium test, and photocatalytic degradation study. The degradation of RhB dye in aqueous solution was tested under sunlight irradiation. Before each photodegradation test, an adsorption-desorption equilibrium is applied for 60 min in dark condition (Figure 9a). The adsorption study of RhB dye into as-prepared BiOBr@0.4Kaol composite material demonstrated that the maximum removal efficiency did not exceed 29% after 60 min. After that, the rest solutions were exposed for further 30 min under sunlight irradiation using the as-prepared nanocomposites, the degradation efficiency for pure BiOBr, BiOBr@1.0Kaol, BiOBr@0.8Kaol, BiOBr@0.6Kaol, BiOBr@0.4Kaol, BiOBr@0.2Kaol, and raw kaolinite, are 65.45%, 67.39%, 71.48%, 82.98%, 99.81%, 90.76%, and 6.28%, respectively (Figure 9b). It can be seen that the BiOBr@0.4Kaol nanocomposite has the best degradation efficiency (99.81%), this can be explained by the high separation performance of electron-hole pairs due to assembled of pure BiOBr and kaolinite clay. This suggested that electron-hole recombination is strongly decreased, which leads to strong photocatalytic performance. The experimental data also demonstrated that all BiOBr@Kaol nanocomposites

time (min)

BiOBr@1.0Kaol BiOBr@0.8Kaol BiOBr@0.6Kaol BiOBr@0.4Kaol BiOBr@0.2Kaol BiOBr Kaol Blank

Modelling by Monte Carlo adsorption locator simulation

After the optimization of compounds by quantum calculations, the lowest energy absorption of 5 BiOBr (001) species on Kaol (001) was investigated to make the BiOBr@Kaol heterojunction interface by adsorption locator module and force field; universal in Materials Studio 2017 software [START_REF] Pelalak | Molecular dynamics simulation of novel diamino-functionalized hollow mesosilica spheres for adsorption of dyes from synthetic wastewater[END_REF]. The electrostatic and van der Waals was calculated using the Group summation method.

The BiOBr (001) surfaces with Bi-, O-and Br-terminated can be adsorbed on Kaol surface.

The adsorption energy (Ead) of 5 molecules of BiOBr on Kaol was evaluated about -982.282 kcal/mol. In addition, BiOBr can be adsorbed approximately more on HO-Al surface (0 0 1) as compared with SiO-terminated surfaces (0 01). The equilibrium configurations can be displayed in Figure 12. In other words, in the view of the configurations on kaolinite (0 0 1) surface was located easier to coat on HO-Al surfaces than (0 01) surface. The results showed that, Bi atoms of BiOBr were contributed to interact on HO-Al and SiO-terminated surfaces of kaolinite. This work gives deep theoretical insights into the migration of RhB on the BiOBr(001)@Kaol(001) surface and provides new perspective for understanding the structure-performance relationship rule. Based on the preferential adsorption models of adsorbates (RhB) on BiOBr@Kaol heterojunction surface by Monte Carlo calculation, the total adsorption energies of 5 molecules and 3 molecules of the RhB for BiOBr@Kaol were obtained about -310.813 and -233.816 kcal/mol, respectively (Figure 13), demonstrating the exothermic and stability of the adsorption system owing to its high negative interaction energy [START_REF] Chen | Mechanism research on surface hydration of kaolinite, insights from DFT and MD simulations[END_REF][START_REF] Salahshoori | A deep insight of solubility behavior, mechanical quantum, thermodynamic, and mechanical properties of Pebax-1657 polymer blends with various types of vinyl polymers: A mechanical quantum and molecular dynamics simulation study[END_REF]. On the basis of the above analyses, the negative values mean that the adsorbates can be adsorbed on the (0 0 1) surface. It also could be concluded that van der Waals attractions were responsible between the RhB molecules and BiOBr@Kaol surface.

The negative adsorption energy Eads value of 5 molecules of the RhB on BiOBr@Kaol surface was larger than the 3 molecules of the RhB on BiOBr@Kaol surface, suggesting more adsorption of pollutants. In addition, by RhB adsorption on BiOBr@Kaol surface, bismuth oxybromide (BiOBr) as a typical layered visible light photocatalyst can be affected on the degradation of RhB. surface. Meanwhile, the BiOBr adsorption on (0 01) surface was relatively strong. In addition, the adsorption of RhB species on the BiOBr@Kaol surface should be more stable due to the high negative interaction energy.

Possible Photocatalytic mechanism

The photocatalytic mechanism for the RhB degradation by BiOBr@Kaol nanocomposite under sunlight irradiation was investigated. The photocatalytic reaction was trapping using the actives species named scavengers; these scavengers play a crucial role to determine the radical species responsible for RhB oxidation in the photocatalytic reaction. Acid ascorbic (ASC), isopropanol alcohol (IPR), and ethylene diamine tetraacetic acid (EDTA), are the most commonly scavengers using to trapping radicals (•O2 -), (HO•), and (h + ), respectively. In the typical process, 4 mmol of each scavenger was added in 50 mL RhB dye solution (10 ppm), with 50 mg of BiOBr@0. In addition, the BC and BV edge potentials of BiOBr@Kaol semiconductor are calculated using the following equations [START_REF] Haounati | Z-Scheme g-C3N4/Fe3O4/Ag3PO4@Sep magnetic nanocomposites as heterojunction photocatalysts for green malachite degradation and Dynamic molecular studies[END_REF]. Table 2 summarized the calculated χ of BiOBr@Kaol, EVB, ECB, edge potential and Eg of BiOBr@Kaol. The photocatalytic mechanism of RhB dye degradation over the BiOBr@Kaol nanocomposite under sunlight irradiation is depicted in Figure 15. When the semiconductor is excited by solar radiation, an electron (e-) from the valence band edge (ECV) transfers to the conduction band edge (ECB), generating a hole (h+) in the valence band (VB) and forming an electronhole pair (Equation 7). The (e -and h + ) pairs oxidize water molecules to hydroxyl radicals (OH • ) using hole (h + ), (Equation 8) and reduce the oxygen to the superoxide radicals (•O2 -) through electron (e -), (Equation 9). These generated radicals are responsible for degrading the RhB molecules to H2O and CO2 as shown in (Equation 10). Additionally, the strong adsorptive properties and negatively charged surface of kaolinite clay play a crucial role to improve the photocatalytic performance. The electrostatic attraction between the photogenerated holes at the EVB edge and the negatively charged kaolinite surface effectively prevents recombination of the electron-hole pairs. Therefore, the free holes in the EVB are occupied by the negative charge of the kaolinite, further enhancing the separation of photogenerated electrons and holes. This process significantly improves the photodegradation efficiency of RhB dye over the BiOBr@Kaol photocatalyst. The potential mechanism of the RhB photodegradation reaction by BiOBr@Kaol is illustrated in Figure 15.

Stability and reusability of the photocatalyst

The evaluation of the durability of photocatalyst is very important index for their practical applications in large-scale. In typical protocol, the BiOBr@Kaol and pure BiOBr were used in first application to degrade RhB dye, after the first demineralization, the powder BiOBr@Kaol and pure BiOBr were collected using centrifuge, washed several times by deionized water and acetone, dried in the oven at 75 °C for 12 hours and used for the next application. The regeneration of BiOBr@Kaol was realized in five cycles. As can be seen in Figure 16-a, the degradation efficiency of RhB dye by BiOBr@Kaol is slightly decreased from 100% to 97.99% after five cycles compared with pure BiOBr, which has a degradation efficiency strongly decreased from 81.96% to 20.45%. In addition, the SEM image of the BiOBr@0.4Kaol nanocomposite after five cycles of reuse (Figure 16,b) clearly shows that the material remains stable and its morphology unchanged. Furthermore, the EDX spectrum and mapping micrograph of BiOBr@0.4Kaol after five cycles of reuse (Figure 16,c

Comparison study

To confirm the reliability of the synthesized nanocomposites, the degradation efficiency of RhB dye by BiOBr@Kaol was compared with other highly efficient photocatalysts reported in the literature (Table 3). When the pure BiOBr catalyst was modified with Kaolinite clay, the photodegradation performance of RhB dye was remarkably enhanced and reached 100% compared with Metal doped BiOBr or heterojunction with another semiconductor. These results can be applied by utilizing kaolinite clay for synthesis of other nanocomposites with different semiconductor photocatalysts in order to achieve higher photocatalytic performance.

Conclusion

It summarizes the findings of the study and draws conclusions based on the results. It states that the BiOBr@Kaol nanocomposite with a mass ratio of 0.4 kaolinite exhibited the highest photocatalytic efficiency for RhB degradation, achieving 100% dye decomposition within 30 minutes under sunlight irradiation. It also mentions that the degradation rate of BiOBr@0.4Kaol was 4.17 times higher than that of pure BiOBr, indicating improved separation of photogenerated electron-hole pairs. Furthermore, to investigate the adsorption mechanisms of BiOBr on kaolinite particles and RhB molecules on BiOBr@Kaol, DFT-D and MD simulations were employed. The MD simulations and Monte Carlo calculations revealed that the BiOBr molecules aligned approximately parallel to the surfaces of kaolinite particles that contained -OH groups. Specifically, one of the (001) kaolinite surfaces, which carried OH groups, formed hydrogen bonds with the BiOBr-O atoms. Additionally, the results indicated that the interactions between RhB molecules and BiOBr@Kaol were of the Van der Waals type. Importantly, the adsorption energies of BiOBr on kaolinite particles and RhB molecules on BiOBr@Kaol were determined to be negative, indicating a stable and exothermic system. The facile synthesis of the photocatalyst holds promising potential for large-scale water remediation applications.

Figure 1 :

 1 Figure 1: The side view of BiOBr crystals unit cells, and (b and c) views of kaolinite clay unit cells.

Figure. 2

 2 shows a brief summary of the steps involved in the preparation of the BiOBr@Kaol nanocomposite.

Figure 2 :

 2 Figure 2: Strategies of the synthesis of the BiOBr@Kaol photocatalysts.

  Kaolinite (Kaol) as layered clay mineral containing of tetrahedral SiO4 and octahedral AlO6 periodically is shown in Figure 3a and 3b. Al₂Si₂H₄O₉ (code; mp-695878) with Space Group; P1, a =5.21, b =7.48, c = 9.05 Å, α=91.79, β =89.73 γ = 104.97 ° and Volume= 340.74 Å 3 was downloaded from https://materialsproject.org/materials/mp-695878. Then, the crystal structure of Kaol (0 0 1) was designed on (0 0 1) surface and characterizations including thickness of 2.06 Å, set u v; 2 1, vacuum thickness (0.000) and slab position (1.00) Figure 3 (c, d). Figures (3-e and 3-f) are showed designed Kaolinite surface without unit cell to optimize and adsorb BiOBr and pollutants which the structure of Kaolinite are included both two sides; Al-bterminated and Si-terminated surfaces [41]. BiOBr including (code; mp-23072) with Space Group; P4/nmm, Lattice System; Tetragonal a = b =3.93, c = 8.39 Å, α= β = γ = 90.000° and Volume= 129.51 ų Figures 3g and 3h, was downloaded from https://materialsproject.org/materials/mp-23072. BiOBr along the (001) facet was first studied [42]. In order to adsorb BiBr adsorption on Kaolinite, the crystal model was prepared from download primitive BiOBr cell with the structure of Bi-, O-and Br-terminated. So, this model was constructed in the (U V; 2 × 2) supercells (illustrated in Figures (3-g and 3-h). at last, the optimized lattice parameters were obtained a = 8.394, b = 5.554, c = 5.554 Å, α= β = γ = 90.000°. BiOBr without cell box was applied for adsorption as observed in Figures (

3 :

 3 Snapshots of the proposed structures (a and b); Al₂Si₂H₄O9 (Kaol)₉ (side), (c and d); side view of Kaol unit cell (0 0 1, U V; 2 1), (e and f); side view of Kaol without unit cell (001) (g and h); BiOBr unit cell, (g and h); BiOBr unit cell ((0 0 1), and thickness; 2.50), (k); BiOBr without unit cell (0 0 1). (The Si, Al, Br, Bi, and O, atoms are represented by the yellow, light purple, brown, black purple and red balls, respectively.

Figure 6 l

 6 Figure 6 l clearly demonstrates that BiOBr nanosheets have been successfully dispersed on the surface of kaolinite.

Figure 6 :

 6 Figure6: SEM image and EDX spectrum of raw kaolinite (a, b, c), pure BiOBr (d, e, f) Kaol@BiOBr (g, h, i). HRTEM of kaolinite (j), BiOBr (k) and BiOBr@Kaol (l).

Figure 7 :

 7 Figure 7: the XPS survery spectrum of raw kaolinite, BiOBr and BiOBr@Kaol (a), the high-resolution XPS of Bi 4f (b), Br 3d (c), O 1s (d), Al 2p (e), and Si 2p (f).

  have excellent degradation performance compared with pure BiOBr Figure9a. It emphasizes that the interface between kaolinite and BiOBr plays a crucial role in facilitating efficient charge transfer and separation of photogenerated electron-hole pairs. This, in turn, reduces the recombination rate of the electron-hole pairs, leading to an enhancement in the photocatalytic activity of BiOBr. The findings highlight the significance of kaolinite modification as a key factor in improving the overall performance of BiOBr as a photocatalyst.

Figure 9 :Figure 10 : 3 . 7 .CFigure 11 :

 9103711 Figure 9: (a) adsorption and photocatalytic degradation of RhB dye under sunlight, (b) Degradation efficiency of RhB dye

Figure 12 :

 12 Figure 12: The lowest energy absorption of 5 BiOBr (001) species on Kaol (001) by adsorption locator module and forcefield; universal in Materials Studio 2017 software.

13 .

 13 (a and b); The lowest adsorption energy of 5 RhB on Kaol (001) and (c and d); the lowest adsorption energy of 3 RhB on Kaol (001) by adsorption locator module and forcefield; universal in Materials Studio 2017 software. DFT-D and MD were used to investigate the optimization of structures, BiOBr absorption on the kaolinite (0 0 1) surface and RhB adsorption on BiOBr@Kaol. The results indicated that the BiOBr adsorption was parallel on HO-Al surface of kaolinite (0 0 1) surface and (0 01)

  4Kaol and agitated under sunlight irradiation for 20 min. The solution was then collected and separated by centrifuge; the remaining dye concentration was determined using UV spectrophotometer. The experimental results of the scavenger's tests are presented in Figure 14. Whereas, the degradation efficiency of RhB dye is 95.3 %, 80.50 %, and 26% for as scavengers (EDTA), (ASC), and (IPR), respectively, demonstrating that the superoxide radicals (•O2 -) is the active species responsible of the degradation of RhB dye and the h + hole has a relatively minor effect on the direct photodegradation of RhB molecules.

Figure 14 .

 14 Figure 14. The actives species trapping experiments for degradation efficiency of RhB dye by BiOBr@Kaol

  Where χ(eV) is the absolute electronegativity of the semiconductor BiOBr, and a, b, and c are the number of atoms in a chemical formula AaBbCc. EVB (eV), ECB, and Eg (eV) are the VB edge potential, CB edge potential, and the band gap energy of the semi-conductors respectively. E0 (eV) is the energy of free electrons on the hydrogen scale (E0 ≈ 4.5 eV/NHE).

Figure 15 :

 15 Figure 15: Proposal mechanisms of degradation of RhB dye by BiOBr@Kaol nanocomposite under sunlight.

  ) indicate that the nanocomposite surface is homogeneous and that all elements of pure BiOBr and raw kaolinite are evenly dispersed. It also mentions the absence of impurity peaks, providing important insights into the nanocomposite structural integrity. This indicates that the agglomeration issue of the BiOBr semiconductor has been successfully solved. Thus, the results are very promising for large-scale application.

Figure 16 :

 16 Figure 16: Cyclic rune experiment of BiOBr@0.4Kaol nanocomposite and pure BiOBr for RhB degradation (a), SEM and EDS mapping images of BiOBr@0.4Kaol nanocomposite after five reuse cycles (b and c).

  .19°, 31.71°, 32.24°, 39.32°, 44.66°, 46.17°, 46.90°, 47.64°, 50.66°, 53.34°, 56.10°, 57.18°, 61.85°, 66.28°, and 67.48°, which were assigned to (001), (

3600 3200 2800 2400 2000 1600 1200 800 400

		O-H		Bi-Br 517,8 421,37 Bi-O
				785
	3697.54	3618.45	1116	914
			1029	1007	536	468.7

  )

	(a)											(b)					(c)
	Bi 5d	Br 2p	Al 2p Si 2p Bi 4f5/2	Bi 4f7/2	C 1s	Bi 4d5/2	Bi 4d3/2	O 1s	Bi 4p3/2	BiOBr@Kaol BiOBr Kaolinite	BiOBr@Kaol Bi 4f	157.12 eV			162.4 eV	Br 3d	Br 3d 5/2 (65.5 eV)
	Intensity (a.u.)											Intensity (a.u.)	156.4 eV	161.7 eV			Intensity (a.u.)	Br 3d 3/2 (66.5 eV)
													154 eV	159.4 eV
																	BiOBr
	0			200		400 Binding energird (eV) 600	800	1000	152	154	156 Binding energy (eV) 158 160	162	164	166	62	64	66 Binding energy (eV)	68	70
	(d)											(e)					(f)
	524 Intensity (a.u.) O 1s Bi-O (527.1 eV) 526 BiOBr BiOBr@Kaol		528 Binding energy (eV) 530 -OH adsorbed (528.3 eV) Bi-O (528.6 eV)	532 Bi-OH (530.5 eV)	534	Intensity (a.u.)	72 Al 2p 3/2 73.5 eV	74 Binding energy (eV) Al 2p 1/2 74.3 eV	76	Al 2p	78	96	98	100 Si-O-Si (100.8 eV) 102	104	106

Table 1 .

 1 The geometric parameters of all compounds obtained by DMol 3 based on DFT-D.

		Kaolinite	BiOBr	RhB
	Sum of atomic energies	-27686.708	-372.585	-1868.168
	Kinetic	-126.215	-0.729	-18.431
	Electrostatic	39.296	-2.237	-2.017
	Exchange-correlation	20.682	0.348	4.536
	Spin polarization	12.481	0.516	3.394
	DFT-D correction	-	-0.002	-0.079
	Total Energy	-27740.463	-374.690	-1880.764

Table 2 :

 2 Calculation results of the ECB and EVB potentials of BiOBr semiconductor.

	Semiconductors	χ(eV)	Eg	ECB	ECV
	BiOBr	6.45	2.79	0.5	3.29

Table . 3

 . : Comparison between BiOBr@Kaol and other composites materials for RhB dye photodegradation.

	Photocatalysts	Condition	Light source	Degradation	Time	Reference
				Efficiency (%)	(min)
	2.0% gC3N4/	60.0 mg, 60.0 mL	visible	98%	150	[57]
	BiOBr	* 10.0 mg L -1	light
	Y-doped BiOBr	10 mg, 100 mL	Visible light	98%	60	[58]
		* 10 mg L -1
		50 mg, 100 mL	Visible light	89.7%	90	[59]
	Bi-BiOBr/BiPO4	* 10 mg L -1
		100 mg, 100 mL	UV-light	95%	70	[60]
	Mt/ZnO	* 10 mg L -1
		120 mg, 250 mL	UV light	98%	120	[61]
	Bentonite /Nb2O5	* 30 mg L -1
		100 mg, 100 mL	UV light	98.3%	25	[62]
	BiOBr/ZnWO4	* 1.0×10 -5 mol L -1
		50 mg, 50 mL	Sunlight	100%	50	[63]
	BiOBr-Au-CdS	* 20 mg/L
		100 mg, 100 mL	Sunlight	100%	30	This work
	BiOBr@Kaol	* 10 mg/L
		100 mg, 100 mL	Sunlight	81.96%	40	This work
	Pure BiOBr	* 10 mg/L

Acknowledgements:

This work results from a collaborative effort between involving scientific members of Faculté des Sciences d'Agadir, Faculté des Sciences Appliquées d'Ait Melloul, Université Ibn Zohr, Agadir Morocco, and Institut de Sciences des Matériaux de Mulhouse (IS2M-UMR 7361 CNRS), Université de Haute Alsace (UHA), Mulhouse-France. We thank VIDAL Loïc (IS2M-MulhouseFrance), VAULOT Cyril (IS2M-Mulhouse-France), GREE Simon (IS2M-Mulhouse-France) and FIOUX Philippe (IS2M-Mulhouse-France), for the Transmission electron microscopy (TEM), the Ultraviolet-Visible Diffuse Reflectance Spectroscopy (UV-Vis DRS), the Fourier-transform infrared spectroscopy (FT-IR), and the X-Ray photoelectron spectrometry analyzes, respectively.