Dr Enzo Olivieri

Dr Na Shao

Dr Roselyne Rosas

Jean-Valère Naubron

Dr Adrien Quintard
email: adrien.quintard@univ-grenoble-alpes.fr

J.-V Naubron

Supramolecular Chemistry

Keywords: Catalysis, Conformation, Green Chemistry, Hydrogenation, Molecular Switch

We report here the development of a rotating molecular switch based on metal-catalyzed reversible (de)-hydrogenation. Under an argon atmosphere, acceptorless dehydrogenation induces a switch from an alcohol to a ketone, while reversing to a hydrogen pressure switches back the system to the alcohol. Based on a tolane scaffold, such reversible (de)-hydrogenation enables 180°rotation. The absence of waste accumulation in a switch relying on chemical stimuli is of great significance and could potentially be applied to the design of efficient complex molecular machines.

Nature's biomachinery, able to achieve molecular motion in response to a stimulus or chemical fuel, is essential to processes in living organisms. Given the power of these dynamic biological systems, the development of new synthetic molecular machines might provide new opportunities for applications ranging from physics to biology. [1] But despite the intensive research in this area, a long journey is still ahead before these synthetic systems can efficiently compete with nature and be able to selectively promote useful processes. This is why chemists must continuously propose innovative approaches to trigger efficient molecular switches. Among the potential external stimuli, aside from light, heat, or electrical input, a broad array of chemical fuels have been applied with success. [START_REF] Kariyawasam | For examples of chemically fueled molecular switches where the accumulation of waste is mentioned as the limitation[END_REF] However, as a major drawback, most of these chemical stimuli produce undesired chemical waste whose accumulation in the system can rapidly inhibit the machinery. [START_REF] Kariyawasam | For examples of chemically fueled molecular switches where the accumulation of waste is mentioned as the limitation[END_REF][START_REF] Sorrenti | For example of system with a dialyse apparatus[END_REF] To overcome this limitation, new approaches excluding waste are needed. Recently, emergent strategies were developed to try to solve this challenge, such as dialysis, or the use of self-evacuated or inert waste. [START_REF] Sorrenti | For example of system with a dialyse apparatus[END_REF] However, none of these strategies avoid waste formation and the development of new chemical stimuli is mandatory.

Two-directions redox processes have recently been applied to molecular switches through sequential hydrogenation and oxidation using various chemical reagents. [4] These systems take advantage of aromatization/dearomatization processes through the use of heterogeneous catalysts. Most of these systems are interesting colored switches, but cannot be transposed to the engineering of complex molecular machines. In addition, applying chemical oxidants has the disadvantage of generating waste accumulating in the system that can be detrimental to the good operability of the switch even when oxygen is used which might generate interfering water.

In organic synthesis, waste-free change in the oxidation state can easily be triggered through alcohols acceptorless dehydrogenation and reversible ketones hydrogenation (Figure 1a). [5] Promoted by well-defined metal complexes, these redox reversible processes avoid undesired waste accumulation when switching an organic molecule between two distinct oxidation states. This can be applied to switch unreactive alcohols to reactive carbonyl compounds comparable to an ON/OFF activation pathway. [5] These properties are also central in the field of energy through the storage of hydrogen in various organic molecules such as methanol. [6,7] Consequently, it would be highly desirable to transpose such principles to the field of molecular machines.

In this context, we hypothesized that moving reversibly from an alcohol to a ketone through catalytic acceptorless dehydrogenation and hydrogenation could represent a promising platform to build new rotary switches (Figure 1b).

This could be induced by an easy change in the conditions from a hydrogen pressure promoting system reduction, to an argon atmosphere ejecting hydrogen gas from the machine thus avoiding any potential waste accumulation and enabling to displace the system out of equilibrium. [8] As a result, by embedding the redox function on the southern hemisphere of the tolane switch (rotor), a change in the oxidation state would promote a rapid 180°r otation of the rotor through different interactions with the northern hemisphere (stator).

In order to develop a first model of molecular switch, we choose to take advantage of a rapid rotation around an alkyne in a tolane scaffold, which had been used with success notably by the group of Hamilton in different 180°c onformational switches. [9] For such purpose, finding an appropriate alcohol function able to switch easily and reversibly to the ketone represented an important challenge and would be facilitated using secondary alcohols. [8] Consequently, we designed tolane molecular switches, possessing on one hemisphere a secondary benzylic alcohol. The other hemisphere would be constituted of an amide able to coordinate to the ketone. At first, we focused on the synthesis and application of alkyne 1 ketone possessing only one substituent on the northern hemisphere. However, we discovered that such alkyne lacked of stability during the hydrogenation process. In addition, single crystal X-Ray diffraction revealed that, minimizing steric interactions, both ketone and amide functions were located on the undesired opposite sides (Figure 2). [10] In order to stabilize the structure and bring the conformation of the ketone in interaction with the amide, we designed another model switch bearing an additional electron-rich dimethylamino group on the northern hemisphere (Figure 3a). In addition, insertion of a dimethylamino group could also stabilize the desired conformation at the alcohol level. The desired molecular switch 2 ketone was prepared efficiently in a 7 longest linear steps sequence converging through a final Suzuki coupling (see Figure S1).

In order to promote the desired switch, we used the iridium catalyst cat developed by the group of Yamaguchi, notably able to trigger acceptorless dehydrogenation under mild conditions. [8d] Deuterated benzene is used as solvent since it is compatible with both steps and not entering in competition with the potential interactions between each hemispheres. From 2 ketone , applying 1 atmosphere of hydrogen, a clean conversion to 2 alcohol was observed after 24 hours and the structure in the solid state determined by single crystal X-Ray diffraction (Figure 4). [10] Simply changing the hydrogen atmosphere with an argon one, a clean return to 2 ketone is observed after 24 hours under the otherwise identical conditions. Of interest, only 4 mol % of the iridium catalyst is enough to promote both reactions despite the use of the relatively diluted conditions (0.0225 M) applied in order to avoid potential intermolecular interactions.

1 H NMR enables to follow easily the system through the two states (Figure 3b). Most notably, an important change in the chemical shift of protons 1 ( 0.45 ppm) and 2 ( 0.27 ppm) can be observed when switching from 2 ketone to 2 alcohol . Amide chemical shifts had been extensively used by the group of Hamilton to characterize tolanes switches. [9] Since these protons are not affected by a change in the electronic character of the substituent (vide infra), this is in agreement with an important structural change in the conformation during the switch. In addition, the absence of change in the chemical shift of proton 5, confirm that the amide is locked and that this upfield proton (8.7 ppm) is interacting with the carbonyl of the amide in a rigid 6member ring. Consequently, this indicates that on 2 ketone , the ketone is predominantly interacting with the amide through hydrogen bonding, while on 2 alcohol , a 180°rotation brings the alcohol on the opposite side, far from the amide.

These observations were also confirmed by variable temperature NMR analysis (Figure S9, S10). In order to further determine the exact conformation of 2 ketone and 2 alcohol , a complete conformational analysis was performed corroborating NMR and IR spectroscopy supported by DFT calculations.

First of all, the impact of the 180°rotation around the alkyne over the chemical shift was confirmed through the preparation of para-substituted hemisphere references 3 ketone and 3 alcohol . These two compounds are close in electronic character to 2 ketone and 2 alcohol, but cannot create any hydrogen bond between the lower and upper parts of the switch. This enables to confirm the potential interactions observed in 2 ketone and 2 alcohol (Figure 4). Most notably, at the alcohol oxidation state, a 0.93 ppm shift is observed on the benzylic protons 14 and 16 between 2 alcohol and 3 alcohol . In 2 alcohol the observation of this proton at 6.34 ppm, already observed on other tolanes, [10] is due to a strong anisotropic effect. This effect is corroborated on the calculated DFT major conformations (Figure S16, conformation A1 and A2) where the proton 16 is coplanar with the adjacent aromatic ring and the minor ones where proton 16 is colinear to the alkyne axis (Figure S16, conformation A3 and A4). NOESY experiments on 2 alcohol , gave interactions between the benzylic proton and the NMe 2 (See Figure S4), once again confirming the 180°nature of the switch. At the ketone oxidation state, chemical shift of the amide protons 1 and 2 considerably changed between 2 ketone and 3 ketone . Indeed, the hydrogen bonding interaction between the amide and the ketone lead to an increase of 0.37 ppm in the chemical shift of proton 1 between 2 ketone and 3 ketone . This result is comparable with previous literature increase in chemical shifts observed through such hydrogen bonding (Figure S11).

At last, comparison of the theoretical IR spectra of 2 alcohol and 2 ketone with the calculated one from the Boltzman distribution of the different conformations found in DFT (Figure S14-S22), confirmed the nature of the rotating switch and the major conformers populations (Figure S14-S22). These results confirm that on 2 ketone , stabilization occurs through hydrogen bonding between the ketone and the amide together with a repulsion between the electronrich amine and the ketone. 2 alcohol conformations result from multiple small stabilizations (H•••NMe 2 , hydrogen bonding, π-stacking, van der Waals). The sum of these small interactions favor exclusively the conformers with the alcohol on the side of the dimethylamine with a > 99 : 1 calculated Boltzmann distribution.

Overall, the system can be described as a catalyzed switch evolving between two states. Given the rate of both hydrogenation and dehydrogenation reactions (around 24 hours to go to completion), much higher than the fast rotation around the alkyne (< 1 s, Figure S23), the kinetic of the system exclusively depends on the iridium catalyzed transformation. Considering the thermodynamic, the ketone represents the most favored state and can be formed in 100 % through the use of a large vessel enabling sufficient dilution of the generated H 2 . The thermodynamic displacement from the ketone to the alcohol is favored through the use of an excess of hydrogen, displacing the system out of equilibrium and enabling the exclusive formation of 2 alcohol .

Finally, we checked the possibility to run consecutive (de)-hydrogenation switch cycles. Gratifyingly, starting from 2 ketone and by using only 4 mol % of iridium cat, two consecutive acceptorless dehydrogenation/hydrogenation cycles could be performed (see Figure S2). It is important to notice that these iridium catalyzed processes are performed in one-pot, without any other implication of the operator aside from the change in the gas atmosphere. After these two cycles, the third dehydrogenation takes longer (6 days) to go to almost completion (86 % conv), indicating the partial deactivation of the iridium catalyst with the additional appearance of small amount of an unknown impurity. The catalyst deactivation was confirmed when repeating the cycles and adding additional catalyst when a decrease in dehydrogenation rate is observed. This second catalyst addition restored the catalytic activity providing again full conversion (Figure S3). This indicates the actual limits of the system that should be improved through the potential application of catalysts of improved reactivity and the design of less sensitive switches.

To conclude, we presented herein our success at developing a 180°rotational switch based on catalyzed hydrogenation/acceptorless dehydrogenation. As a result of the reversible catalytic approach used, this switch using a chemical stimuli does not generate any accumulating waste. This represents the first step towards the elaboration of complex molecular machines based on such general principle. In order to improve the reliability of the system over multiple cycles, future directions should focus on the modification of the switch scaffold limiting its degradation and on the implementation of metal catalysts of improved efficiency. In addition, the kinetic and thermodynamic of the switch of the system might also be modulated through the change in the alcohol substitution.

Figure 2 .

 2 Figure 2. First molecular switch model prepared.

Figure 3 .

 3 Figure 3. a) Operation of the switch 2 through hydrogenation/acceptorless dehydrogenation. b) 1 H NMR spectra of 2 ketone and 2 alcohol in C 6 D 6 (0.045 M).

Figure 4 .

 4 Figure 4. 1 H NMR spectra of 2 alcohol , 3 alcohol , 2 ketone , 3 ketone and single-crystal X-ray structure of 2 alcohol.

Acknowledgements

The project leading to this publication has received funding from the Excellence Initiative of Aix-Marseille University-A*Midex, a French "Investissements d'Avenir" programme" (A-M-AAP-EI-17-06-170223-13.06-QUINTARD-SAT). The Centre National de la Recherche Scientifique (CNRS), Aix-Marseille Université, Université Grenoble-Alpes and Labex Arcane are warmly acknowledged for financial support. This work was supported by the computing facilities of the CRCMM, "Centre Régional de Compétences en Modélisation Moléculaire de Marseille".

Data Availability Statement

The data that support the findings of this study are available in the Supporting Information of this article.

Conflict of Interest

The authors declare no conflict of interest.


Quentin Le Dé

Fourat Orbay

Laure Vendier

Antoine Simonneau
email: antoine.simonneau@lcc-toulouse.fr

Syntheses of N2-bridged heterobimetallic complexes, their structural and qualitative bonding analyses

Keywords: Dinitrogen, Heterobimetallic Complexes, Molecular Orbitals, Molybdenum

A series of N2-bridged (- 1 : 1 -N2) heterobimetallic complexes were prepared by the reaction of the dinitrogen complex [Mo(depe)2(N2)2] (depe = 1,2-bis(diethylphosphino)ethane) with the group IV-VI high valent metal halides [Cp2ZrCl2], NbCl5, TaCl5, MoCl5 and WCl4 via chloride substitution. Compounds [MoCl(depe)2(μ-N2)ZrCp2Cl] (1) and [MoCl(depe)2(μ-N2)M'Cl4(THF)] (2-5, M' = Nb, Ta, Mo or W) were crystallized from the reaction mixtures. In the case of the reaction with WCl4, disproportionation of W(IV) was suspected but not evidenced. Single crystal X-ray diffraction analyses on all compounds allowed a systematic structural study, and the sketching of qualitative molecular orbital diagrams helped discussing the bonding situation and bolster the structural data.

Introduction

Coordination of dinitrogen to a transition metal center is key to render this inert small molecule reactive. This is the way Nature has elected to achieve N2 reduction into ammonia in microorganisms expressing the nitrogenase enzymes. 1 Since the isolation of the first N2 complex [Ru(NH3)5(N2)] 2+ by Allen and Senoff in the 1960s, 2 a plethora of coordination and organometallic compounds featuring a N2 ligand have been described. [START_REF]Transition Metal-Dinitrogen Complexes: Preparation and Reactivity[END_REF] A wealth of coordination modes and reactivity for the dinitrogen ligand is found in those species, depending on the metal, the ligand sphere and the level of reduction of the small molecule, from dinitrogen to diazenide to hydrazide. Reduced N2 complexes such as diazenido or hydrazido ones are often generated through homobimetallic activation, affording N2bridged complexes in either end-on (- 1 : 1 ) or sideon (- 2 : 2 ) coordination mode, and are particularly represented among groups III-VI and the lanthanides. 4 Some of them have allowed the synthesis of hydrazine derivatives by subsequent treatment with electrophiles. 5 Heterobimetallic N2 complexes remain scarce, and consequently their reactivity has not been explored, [START_REF]Some heterobimetallic N2 complexes have been explored in the dinitrogen splitting context[END_REF] even though methods to prepare N2-bridged heterobimetallic complexes have been long known. 7 The group of Hidai has studied the reactivity of group 6 dinitrogen complexes with electrophilic metal halides and have obtained diazenido-bridged heterobimetallic complexes via halide substitution. Depending on the presence of accessible and empty d orbital on the electrophile, bent or linear M-N2-M' array were observed (Scheme 1). 7f,g,j,k Contrastingly, for maingroup or late metal Lewis acid adducts of dinitrogen complexes 7c,f,l-q or those formed from the less electron rich trans-[ReCl(L)4(N2)] complexes (L = phosphine) with high-valent metal halides, as studied by the group of Chatt,[START_REF] Chatt | Chemical Evidence Concerning the Function of Molybdenum in Nitrogenase[END_REF]b,d,e reduction of the N2 unit is usually not observed. Within a research line aimed at exploring the functionalization of dinitrogen within heterobimetallic complexes, we have looked at the reactivity of [Mo(depe)2(N2)2] (depe = 1,2bis(diethylphosphino)ethane) with group IV-VI high valent metal halides. The goal was to verify whether similar reactivity to those reported by the group of Hidai could be achieved when the more electrondonating depe ligand supports the zero-valent metal and when oxidizing metal halides are employed. We document herein on the synthesis and structural characterization of a series of [Mo]-(-N2)-M'Cl4(THF) (M' = Nb, Ta, Mo, W) allowing for the systematic structural comparison of heterobimetallic complexes having identical ligand spheres, plus the isolation of a group IV-VI [Mo]-(-N2)-ZrClCp2 heterobimetallic compound.

Scheme 1. Examples of preparation of heterobimetallic N2 complexes from terminal dinitrogen complexes. 7b,f,j,q (dppe = 1,2bis(diphenylphosphino)ethane). A later report from the same research group also documents on similar chemistry employing a series of W(0) dinitrogen complexes and various analogues of [CpTiCl3], 7k but none of these report mentions a productive reaction between [Mo(depe)2(N2)2] and [Cp2ZrCl2]. At room temperature in toluene, no reaction was observed according to NMR analysis. After 1 h at 60 °C, the color of the solution changed from orange to purple. In the 31 P-NMR spectra recorded on an aliquot, the resonance of the [Mo(depe)2(N2)2] complex (56.0 ppm) had vanished and a new signal appeared at 51.3 ppm. After concentration under vacuum and layering with pentane, purple crystals grew over a night and could be analyzed by single crystal X-Ray diffraction (sc-XRD). Complex [MoCl(depe)2(μ-N2)ZrCp2Cl] (1, Scheme 2), resulting from chloride substitution on [Cp2ZrCl2] by the N2 ligand of [Mo(depe)2(N2)2], crystallizes in the space group P-1 with two molecules per asymmetric unit (Figure 1). When next turned our attention towards group V chloride salts. The group of Hidai also reported chloride substitution at d 0 group V CpMCl4 (M = Nb, Ta) complexes using [W(PMe2Ph) (2) and [MoCl(depe)2(μ-N2)TaCl4(THF)] (3, Scheme 3) were the result of chloride substitution on NbCl5 and TaCl5, respectively. Finally, the reactions between [Mo(depe)2(N2)2] and group 6 metal chlorides, MoCl5 and WCl4, were performed in THF at room temperature. As in the preparation of 2 and 3, N2 evolution was noticed immediately upon mixing solutions of the reactants and after 5 min, 31 P-NMR analysis of an aliquot no longer showed the resonance associated to [Mo(depe)2(N2)2]. As anticipated due to the paramagnetism of MoCl5, no new signal in 31 P NMR could be detected. Intriguingly, the reaction with diamagnetic WCl4 also led to the disappearance of the NMR signals of [Mo(depe)2(N2)2] without giving new ones. The mixtures were concentrated under vacuum and layered with pentane. Under identical crystallization conditions than for 2 and 3, crystals suitable for sc-XRD analysis were obtained. Complex [MoCl(depe)2(μ-N2)MoCl4(THF)] (4, Figure 1) crystallized in the space group P-1. The sc-XRD analysis of the crystalline material obtained from the reaction with WCl4 was unexpected, since the analogous complex [MoCl(depe)2(μ-N2)WCl4(THF)] (5, Figure 1) was obtained.

Results

Our

Scheme 3. Syntheses of the heterobimetallic complexes

[MoCl(depe)2(μ-N2)M'Cl4(THF)] (M' = Nb, Ta, Mo, W) 2-5.

Discussion

Compounds 2-5 have all been obtained in similar conditions, reactions between [Mo(depe)2(N2)2] and the metal halide being immediate at room temperature, as witnessed by N2 evolution right after mixing solutions of the reactants. The high Lewis acidity and unsaturation of the halide salts is likely to explain the quick reactivity with the rather electron rich [Mo(depe)2(N2)2] complex. The situation was different for the preparation of 1 as thermal activation was needed. This may result from Cp-induced steric hindrance in [Cp2ZrCl2] that may lead to a more kinetically demanding ligand interchange. The characterization by sc-XRD of the Mo(II)-W(V) heterobimetallic complex 5 from the reaction with WCl4 is somewhat surprising and points to a possible disproportionation of W(IV) to W(III) and W(V). Indeed, Cummins and co-workers have reported intermetal chlorine atom transfer between W(IV) and Ti(III), allowing for the synthesis of [WCl3(THF)3]. [START_REF] Kim | Synthesis of Mer-Trichlorotris(Tetrahydrofuran) Tungsten(III) by Intermetal Chlorine Atom Transfer[END_REF] It may be possible that under our reaction conditions chlorine is transferred from WCl4 to a transient [Mo(depe)2(μ-N2)WCl4(THF)] adduct to afford 5 and [WCl3(THF)3] or a related species. 9 Unfortunately, we were not able to evidence the presence of a reduced W species by sc-XRD by selecting other crystals of the batch, and NMR analysis on a wide spectral window did not reveal the presence of paramagnetic side-products stabilized with THF. Elemental analyses of the crystalline material were found close to a 5•WCl3•1.7THF formulation. For all complexes, the N-N stretching band of the complexes could not be unambiguously assigned in the IR spectra due to its shifting to the fingerprint region.

Pertinent bond lengths and angles for compounds 1-5 are compiled in Table 1. The five (hetero)bimetallic complexes show a molybdenum atom supported by two depe ligands within a pseudooctahedral geometry (Figure 1). A chloride and the bridging N2 ligand are occupying the apical positions. The structural features of their coordination spheres are almost identical in all complexes. In 1, the Zr center is found in a distorted tetrahedron. In 2-5, the high-valent metal lies in a pseudo-octahedral environment with four chlorides in the equatorial plane and one THF molecule facing the bridging N2 ligand. The ClMoNNM'(O) array slightly distorts from linearity, except in the case of 3: all 6 atoms were found on a mirror of the C2/c space group with half occupation in the unit cell and were fixed on that mirror plane for refinement, resulting in perfect linearity. The bridging dinitrogen of the complexes have N-N bond lengths between 1.208(7) and 1.262(4) Å. These numbers are pointing to a bond order of two, although in 1, the recorded N-N bond length is smaller than those found in representative diazene compounds (1.23-1.25 Å). [START_REF] Wells | Structural Inorganic Chemistry[END_REF] The N2 unit would act as a doubly reduced dinitrogen moiety, or diazene-diide (N2 2-), with each nitrogen acting as an LX-type ligand for each metal. [START_REF] Pyykkö | Molecular Double-Bond Covalent Radii for Elements Li-E112[END_REF] This would result in formal oxidation states of +II for the phosphinesupported molybdenum center and +IV for Zr in 1 and +V for M' in 2-5. The (depe)2Mo-N bond lengths all approach 1.80 Å, the shortest being found in 3 (1.778(3) Å) and the longest in 1 (1.820(6) Å). The Zr-N bond in 1 is 2.009(4) Å and is comparable to the one of [WI(PMe2Ph)3(py)(-N2)ZrCp2Cl] 7g (1.98(1) Å, py = pyridine). The M'-N bonds in 2 and 3 are 1.834(4) and 1.822(3) Å, respectively. For comparison, these bond lengths are longer that what is typically found in group V [M(+V)Cl3(ether)n(NR)] imido complexes (average of M-N bond lengths from a 13 hits list is 1.758 Å). 12 The same trend is observed for compounds 4 and 5 that show close M'-N distances of 1.786(5) and 1.784(3) Å, respectively. An average M-N distance calculated for a series of 11 group VI trans-[M(+VI)Cl4(THF)(NR)] imido complexes is 1.722 Å. 13 These discrepancies may arise from the nature of the N-based ligand (X2 vs. LX), the not strictly comparable ligand sphere for the group V halides, and the difference in oxidation states considered for the group VI halides. Overall, the bond lengths of the Mo-N-N-M' array all agree with double bonding between the four atoms. 11 The difference between complexes 2-5 is the number of d electrons of the metal opposing the Mo(II) center: the group V-group VI bimetallic complexes 2 and 3 incorporate a MCl4 moiety that carries no d electrons, while in the group VI-group VI ones (4 and 5), the MCl4 center has a d 1 electronic configuration. Since the N-N bond lengths are comparable in these four complexes, the single electron in 4 should be located on a non-bonding orbital centered on the more oxidized metal and not involved in antibonding orbitals of the N2 unit or of the M-N linkage.

To shed light on the bonding situation, a qualitative Molecular Orbital (MO) diagram focusing on the  system of the MoNNM' core was drawn from the perturbation of a hypothetical, negatively charged C4v [MoCl(L)4(N2)] -complex by a [M'Cl4(THF)] + cation of the same symmetry (Scheme 4, right side). 14 The former carries 8  electrons stemming from the filled {dxz, dyz} set and the two  bonds of N2, while the latter has either 0 (M' = Nb, Ta) or 1 (M' = Mo, W) d electron in a 1e orbital. In the cationic species, the dxy, dxz and dyz orbital were given high energy levels due to the destabilizing effects of the chlorides, that are more pronounced for the b2 (dxy) orbital. Interaction of the frontier orbitals of the two fragments gives a new set of MOs within a heterobimetallic complex of C4v symmetry, in which the single electron of the d 1 cation resides, as suggested by comparison of the crystal structures of 2-5, in a non-bonding, M'centered d orbital. A set of two degenerate MOs that are antibonding regarding the N-N linkage are further stabilized than in [MoCl(L)4(N2)] - , giving it more N2 character. Since they are populated, a high level of activation of N2 (i. e., N-N bond elongation) results. Based on the metrical data issued from sc-XRD analyses and by comparison with computed covalent radii, [START_REF] Pyykkö | Molecular Double-Bond Covalent Radii for Elements Li-E112[END_REF] an Mo=N=N=M' depiction for complexes 2-5 makes sense, as mentioned above. However, the drawing of accurate Lewis structures for N2-bridged bimetallic complexes has recently been discussed by Hasanayn,Holland,Goldman and Miller,[START_REF] Hasanayn | Lewis Structures and the Bonding Classification of End-on Bridging Dinitrogen Transition Metal Complexes[END_REF] arguing that comparison of N-N bond lengths with either N2, diazene or hydrazine is not always valid. According to their model, compounds 2-5 would better correspond to a Mo + (IV)≡N-N≡M' -(V) depiction, with a positive charge on Mo and a negative one on M' and the N2 unit acting as a two-fold LX2 ligand. The former would have 18 valence electrons (VE) and the latter, depending whether it is a group V or VI metal, 16 or 17 VE, respectively, to be compared with 18 VE for Mo and 14 or 15 VE for M' in a Mo(II)=N=N=M'(V) bonding situation (Chart 1). The former depiction better distributes valence electron to the metals and takes into account the electron-withdrawing nature of the M'Cl4(THF) fragment. Complex 1 has a N-N bond length shorter than the four other complexes (1.207 (6) or 1.230(7) Å vs 1.254-1.262 Å). N-N bond lengths are 1.207( 6) and 1.230(7) Å, slightly shorter than a N-N double bond (1.25 Å). Zr-N bond lengths are 2.009(4) and 1.991(5) Å long and Mo-N bonds measure 1.821(5) and 1.806(4) Å. Mo-N-N and N-N-Zr angles are 173.96 and 173.35°, respectively. The solid state structure of 1 is very similar to the one of the N2bridged heterobimetallic complex

[WI(PMe2Ph)3(py)(μ-N2)ZrCp2Cl], reported by Hidai and co-workers 7g (N-N and Zr-N bond lengths: 1.24(2) and 1.98(1) Å, respectively). In 1, the zirconium center has a formal oxidation state of +IV and, like the Ta and Nb ions in complexes 2 and 3, has a d 0 electronic configuration. We drew the MO diagram of 1 by the perturbation of the d 6 complex [MoCl(L)4(N2)] -with the [Cp2ZrCl] + cation of Cs symmetry to see whether it could provide an explanation for a shorter N-N bond (Scheme 4, left side). The frontier MOs of the latter have been calculated by Lauher and Hoffmann, and we considered here, to match with the orientation of [MoCl(L)4(N2)] -, that the Zr-Cl bond is along the y axis. [START_REF] Lauher | Structure and Chemistry of Bis(Cyclopentadienyl)-MLn Complexes[END_REF] Only the 2a' MO of [Cp2ZrCl] + can interact with the  system of [MoCl(L)4(N2)] - , resulting in the stabilization of only the half of the MOs that are antibonding with respect to the N-N bond. This may explain why the level of activation in 1 is inferior to those in 2-5. The MO diagram for 1 would support, according to the model of Miller and colleagues, [START_REF] Hasanayn | Lewis Structures and the Bonding Classification of End-on Bridging Dinitrogen Transition Metal Complexes[END_REF] a Mo(IV)=N=N=Zr(IV) depiction. A Mo + (IV)≡N-N≡Zr -(IV) bonding situation similar to the one encountered in 2-5, where the electron-withdrawing nature of the chloride ligands is helping the stabilization of the negative charge on M', would be counter-intuitive in the case of 1, the valence electron count for Zr being 20 (Chart 1). The fact that the negative charge would be carried by the more electropositive metal, the scarcity of 20-electron zirconocene complexes [START_REF] Jaroschik | Characterization and Reactivity of Formal 20 Electron Zirconocene-Pentafulvene Complexes[END_REF] as well as the relatively short N-N bond are additional arguments that rule out a hydrazine tetraide (N2 4-) ligand in 1.

Chart 1. Comparison of bonding situations for the Mo-N-N-M' core of the heterobimetallic complexes in terms of oxidation states and valence electron count (VEC).

Conclusion

We have prepared new N2-bridged heterobimetallic complexes, obtained by the reaction of [Mo(depe)2(N2)2] with various group IV-VI halide complexes.

Compound [MoCl(depe)2(μ-N2)ZrCp2Cl] (1) and a series of analogous [MoCl(depe)2(μ-N2)M'Cl4(THF)] (2-5, M' = Nb, Ta, Mo, W) complexes could be structurally characterized. Sketching of the qualitative molecular orbital diagrams helped understand the bonding situation as well as structural similarities or differences. In light of a recent discussion on qualitative analysis of the bonding in bimetallic N2 complexes by Miller and colleagues, [START_REF] Hasanayn | Lewis Structures and the Bonding Classification of End-on Bridging Dinitrogen Transition Metal Complexes[END_REF] we have applied their model on the compounds reported herein: if a hydrazine tetraide (N2 4-) ligand can be supported for the 2-5 family, a Mo=N=N=Zr depiction (with a diazene-diide ligand) seems more appropriate for 1.

Materials and methods

General information

All reactions were performed in oven-dried glassware with rigorous exclusion of air and moisture, using a nitrogen filled Jacomex glove box (O2 < 2 ppm, H2O < 1 ppm) equipped with a vacuum line. Solvent used were pre-dried (toluene, tetrahydrofuran and pentane by passing through a Puresolv MD 7 solvent purification machine) degassed by freeze-pump-thaw cycles, dried over molecular sieves and stored in the glove box. THF-d8 (purchased from Eurisotop) was degassed by freeze-pump-thaw cycles, dried over molecular sieves and stored in the glove box. MoCl5, NbCl5, TaCl5 and [Cp2ZrCl2] have been purchased from Strem, the latter one was recrystallized from dichloromethane. WCl4 has been purchased from Sigma-Aldrich. trans-[Mo(depe)2(N2)2] has been prepared from MoCl5. 18 1 H, 13 C and 31 P NMR spectra were recorded in THF-d8 by using NMR tubes equipped with J. Young valves on a Bruker Avance III 400 spectrometer. Chemical shifts are in parts per million (ppm) downfield from tetramethylsilane and are referenced to the residual solvent resonances as the internal standard (C4HD7O: δ reported = 3.58 and 1.72 ppm for 1 H NMR). 13 C and 31 P NMR spectra were calibrated according to the IUPAC recommendation using a unified chemical shift scale based on the proton resonance of tetramethylsilane as primary reference. 19 Data are reported as follows: chemical shift, multiplicity (s = singlet, t = triplet, q = quartet, quint. = quintet, m = multiplet) and integration. Infrared (IR) spectra were recorded in a nitrogen filled Jacomex glove box (O2 < 2 ppm, H2O < 1 ppm) on an Agilent Cary 630 FT-IR spectrophotometer equipped with ATR and are reported in wavenumbers (cm -1 ). Elemental analyses were performed on samples sealed in tin capsules under N2 by Analytical Service of the Laboratoire de Chimie de Coordination; results are the average of two independent measurements.

Characterization

Synthesis of [MoCl(depe)2(μ-N2)ZrCp2Cl] (1)

[Mo(depe)2(N2)2] (20.0 mg, 35.4 µmol, 1 equiv.) was dissolved in 2 mL of toluene. A toluene solution (2 mL) of [Cp2ZrCl2] (10.2 mg, 35.4 µmol, 1 equiv.) was added to the first solution. The mixture was then stirred and warmed to 60 °C during 1 h, time during which the solution became purple. The mixture was concentrated under vacuum to ca. 2 mL and pentane (4 mL) was added. After a night at -40 °C, crystals of (1) were separated from the supernatant and washed with pentane. After drying under vacuum, complex 1 was obtained as purple crystals (25.2 mg, 30.4 µmol, 86%).

1 H-NMR (400 MHz, THF-d8) δ 6.01 (s, 10H, Cp), 2.01 (m, 8H), 1.92 (m, 8H), 1.79 (m, 8H), 1.23 (t, 12H), 1.14 (t, 12H). 13 C-NMR (100.6 MHz, THF-d8) δ 110.8 (s), 21.7 (quint.), 18.5 (quint.), 17.9 (quint.), 8.1 (s), 7.5 (s). 31 P-NMR (162 MHz, THF-d8) δ 51.3 (s).

Elem. Anal. Calcd. for C30H58Cl2MoN2P4Zr: C 43.48; H 7.05; N 3.38. Found: C 42.77; H 6.76; N 2.65. 2931, 2896, 2875, 1543, 1457, 1407, 1305, 1232, 1182, 1118, 981, 863, 786, 730.

IR (ATR) ν =

Synthesis of [MoCl(depe)2(μ-N2)NbCl4(THF)] (2)

[Mo(depe)2(N2)2] (30.0 mg, 53.2 µmol, 1 equiv.) was dissolved in 3 mL of THF. A THF solution (3 mL) of NbCl5 (14.4 mg, 53.2 µmol, 1 equiv.) was added to the first solution, and bubbling was immediatly observed. The mixture was stirred for 5 min at room temperature, then concentrated under vacuum to ca. 3 mL. The resulting THF solution was then layered with 4 mL of pentane. After a night at room temperature, crystals of (2) were separated from the supernatant and washed with pentane. After drying under vacuum, complex 2 was obtained as orange crystals (41 mg, 46.7 µmol, 88 %).

1 H-NMR (400 MHz, THF-d8) δ 2.20 (m, 8H), 2.01 (m, 16H), 1.31 (t, 12H), 1.22 (t, 12H). 13 C-NMR (100.6 MHz, THF-d8) δ 21.7 (quint.), 20.5 (quint.), 18.1 (quint.), 8.5 (s), 7.4 (s). 2935, 2874, 1456, 1410, 1352, 1243, 1111, 1031, 869, 837, 817, 759, 734, 673.

Synthesis of [MoCl(depe)2(μ-N2)TaCl4(THF)] (3)

[Mo(depe)2(N2)2] (30.0 mg, 53.2 µmol, 1 equiv.) was dissolved in 3 mL of THF. A THF solution (3 mL) of TaCl5 (19.1 mg, 53.2 µmol, 1 equiv.) was added to the first solution, and bubbling was immediatly observed. The mixture was stirred for 5 min at room temperature, then concentrated under vacuum to ca. 3 mL. The resulting THF solution was then layered with 4 mL of pentane. After a night at room temperature, crystals of (3) were separated from the supernatant and washed with pentane. After drying under vacuum, complex 3 was obtained as orange crystals (30.8 mg, 31.9 µmol, 60 %).

1 H-NMR (400 MHz, THF-d8) δ 2.16 (q, 8H), 1.94 (m, 16H), 1.29 (t, 12H), 1.21 (t, 12H). 13 C-NMR (100.6 MHz, THF-d8) δ 21.1 (quint.), 20.0 (quint.), 17.7 (quint.), 8.1 (s), 7.0 (s). 31 P-NMR (162 MHz, THF-d8) δ 43.6 (s).

Elem. Anal. Calcd. for C24H55Cl5MoN2OP4Ta: C 29.85; H 5.74; N 2.90. Found: C 30.07; H 5.66; N 2.40. 2969, 2937, 2907, 1879, 1602, 1577, 1495, 1480, 1454, 1409, 1379, 1252, 1129, 1082, 1029, 1003, 982, 946, 896, 867, 842, 813, 785, 729, 695.

IR (ATR) ν =

Synthesis of [MoCl(depe)2(μ-N2)MoCl4(THF)] (4)

[Mo(depe)2(N2)2] (30.0 mg, 53.2 µmol, 1 equiv.) was dissolved in 3 mL of THF. A THF solution (3 mL) of MoCl5 (14.5 mg, 53.2 µmol, 1 equiv.) was added to the first solution, and bubbling was immediatly observed. The mixture was stirred for 5 min at room temperature, then concentrated under vacuum to ca. 3 mL. The resulting THF solution was then layered with 4 mL of pentane. After a night at room temperature, crystals of (4) were separated from the supernatant and washed with pentane. After drying under vacuum, complex 4 was obtained as orange crystals (34.2 mg, 38.8 µmol, 73 %).

Elem. Anal. Calcd. for C24H55Cl5Mo2N2OP4: C 32.73; H 6.29; N 3.18. Found C 33.12; H 5.96; N 2.92 IR (ATR) ν = 2935, 1875, 1456, 1411, 1376, 1306, 1233, 1183, 1119, 1030, 980, 917, 867, 829, 815, 739.

Synthesis of [MoCl(depe)2(μ-N2)WCl4(THF)] (5)

[Mo(depe)2(N2)2] (30.0 mg, 53.2 µmol, 1 equiv.) was dissolved in 3 mL of THF. A THF solution (3 mL) of WCl4 (17.3 mg, 53.2 µmol, 1 equiv.) was added to the first solution, and bubbling was immediatly observed. The mixture was stirred for 5 min at room temperature, then concentrated under vacuum to ca. 3 mL. The resulting THF solution was then layered with 4 mL of pentane. After a night at room temperature, orange crystals were separated from the supernatant and washed with pentane. After drying under vacuum, the crystalline solid weighed 34.2 mg. sc-XRD analysis revealed a W(+V) complex that could not be obtained quantitatively with the applied stoichiometry.

Elem.

Anal.

Calcd. for C24H55Cl5MoN2OP4W•WCl3•1.7(C4H8O): C 26.76; H 5.03; N 2.03. Found C 26.82; H 4.33; N 1.28. 2960, 2933, 2905, 2876, 1894, 1757, 1649, 1454, 1409, 1378, 1308, 1230, 1182, 1121, 1027, 980, 863, 813, 786, 746, 718.

IR (ATR) ν =

  depe)2(N2)2] with the group IV metal complex [Cp2ZrCl2]. It was employed by the group of Hidai for the synthesis of heterobimetallic dinitrogenbridged complexes by halide substitution with trans-[W(PMe2Ph)4(N2)2] 7g or [W(dppe)2(NCS)(N2)][NBu4] 7j

Scheme 2 .

 2 Scheme 2. Synthesis of the Mo-Zr heterobimetallic N2 complex 1.

Figure 1 .

 1 Figure 1. Solid-state molecular structure of compounds 1-5 determined by sc-XRD with ellipsoids drawn at the 30% probability level. Hydrogen atoms were omitted and hydrocarbon rings and chains are depicted as wireframes for clarity.

Scheme 4 .

 4 Scheme 4. Qualitative MO diagrams for compounds 1, 4 and 5 obtained by perturbation of [MoCl(L)4(N2)] -with group IV-VI cations.

Table 1 .

 1 Selected bond lengths and angles for compounds 1-5. n. a. = not applicable.

	Bond (Å) or angle (°)	1	2	3	4	5
	Mo-N	1.820(6)	1.803(4)	1.778(3)	1.816(4)	1.801(3)
	Mo-Cl	2.550(2)	2.478(1)	2.4779(9)	2.4517(12)	2.4708(8)
	N-N	1.208(7)	1.254(5)	1.258(4)	1.257(6)	1.262(4)
	M'-N	2.009(4)	1.834(4)	1.822(3)	1.786(5)	1.784(3)
	M'-O	n. a.	2.307(3)	2.254(3)	2.230(4)	2.243(2)
	Cl-Mo-N	174.7(2)	173.7(1)	180.0	173.77(12)	173.63(8)
	Mo-N-N	173.9(5)	172.8(3)	180.0	173.0(3)	172.4(2)
	N-N-M'	176.8(4)	176.6(3)	180.0	177.0(4)	177.4(2)
	N-M'-O	n. a.	178.0(1)	180.0	177.91(17)	178.1(1)

Acknowledgements

A.S. and Q. L. D. acknowledges the European Research Council (ERC) for funding (Grant Agreement 757501). All authors are indebted to the French National Center for Scientific Research (CNRS) for financial support.

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.

Graphical Abstract

Synopsis

Syntheses of new N2-bridged heterobimetallic complexes are reported, with their systematic structural analysis. Similarities or discrepancies are explained with qualitative molecular orbital diagrams.


Sofie Vranken
email: sofie.vranken@ugent.com

Marine Robuchon

Stefanie Dekeyzer

Ignacio Bárbara

Inka Bartsch

Aurélie Blanfuné

Charles-François Boudouresque

Wim Decock

Christophe Destombe

Bruno De Reviers

Pilar Díaz-Tapia

Anne Herbst

Romain Julliard

Rolf Karez

Priit Kersen

Stacy A Krueger-Hadfield

Ralph Kuhlenkamp

Akira F Peters

Viviana Peña

Cristina Piñeiro-Corbeira

Fabio Rindi

Florence Rousseau

Jan Rueness

Hendrik Schubert

Kjersti Sjøtun

Marta Sansón

Dan Smale

Thierry Thibaut

Myriam Valero

Leen Vandepitte

Bart Vanhoorne

Alba Vergés

Marc Verlaque

Christophe Vieira

Line Le Gall

Frederik Leliaert

Olivier De Clerck
email: olivier.declerck@ugent.be

AlgaeTraits: a trait database for (European) seaweeds

Keywords: Trait-based ecology, Functional groups, Macroalgae, Morphology, Life history traits

The analysis of biological and ecological traits has a long history in evolutionary and ecological research. However, trait data are often scattered and standardised terminology that transcends taxonomic and biogeographical context are generally missing. As part of the development of a global trait database of marine species, we collated trait information for European seaweeds and structured the data within the standardised framework of the World Register of Marine Species (WoRMS). We collected 45,175 records for 21 biologically and ecologically relevant traits of seaweeds. This resulted in a trait database for 1,745 European seaweed species of which more than half (56%) of the records were documented at the species level, while the remaining 44% was documented at a higher taxonomic level and subsequently inherited at lower levels. The trait database for European seaweeds will serve as a foundation for future research on diversity and evolution of seaweeds, and their responses to global changes. The data will contribute to developing detailed trait-based ecosystem models, and will be an important tool to inform marine conservation policies. The data is publicly accessible through the

Introduction

Trait-based approaches, focusing on diversity of organismal characteristics rather than species diversity, are an effective data source to answer important biological questions [START_REF] Costello | Biological and ecological traits of marine species[END_REF][START_REF] Beauchard | The use of multiple biological traits in marine community ecology and its potential in ecological indicator development[END_REF][START_REF] Degen | Trait-based approaches in rapidly changing ecosystems: A roadmap to the future polar oceans[END_REF]. Traditionally, traits have been and still are of significant value for taxonomic research (Voultsiadou et al., 2017). Moreover, as they enable the description and investigation of complex ecosystems in relatively simple ways without having to laboriously study each individual component species, they are also integral to the study of the ecological and evolutionary dynamics of populations, species, communities, and ecosystems [START_REF] Violle | Let the concept of trait be functional![END_REF][START_REF] Kattge | A generic structure for plant trait databases[END_REF][START_REF] Degen | Trait-based approaches in rapidly changing ecosystems: A roadmap to the future polar oceans[END_REF][START_REF] Schleuning | Trait-based assessments of climate-change impacts on interacting species[END_REF]. For example, the analysis of trait data can assist in estimating responses to multiple stressors, including anthropogenic and climate change impacts [START_REF] Degen | Trait-based approaches in rapidly changing ecosystems: A roadmap to the future polar oceans[END_REF][START_REF] Schleuning | Trait-based assessments of climate-change impacts on interacting species[END_REF], and may provide crucial information needed to develop effective management strategies to counter negative consequences of climate change [START_REF] Bremner | Species' traits and ecological functioning in marine conservation and management[END_REF].

Although the importance of trait-based approaches is widely recognised, there remains a general lack of accessible, standardised, and harmonised trait data for aquatic organisms [START_REF] Costello | Biological and ecological traits of marine species[END_REF][START_REF] Beauchard | The use of multiple biological traits in marine community ecology and its potential in ecological indicator development[END_REF][START_REF] Degen | Trait-based approaches in rapidly changing ecosystems: A roadmap to the future polar oceans[END_REF][START_REF] Martini | Functional trait-based approaches as a common framework for aquatic ecologists[END_REF]. Recent initiatives have intended to resolve this gap and made significant progress for some marine animals, including fishes, polychaetes, copepods, and macroinvertebrates (reviewed in [START_REF] Martini | Functional trait-based approaches as a common framework for aquatic ecologists[END_REF], but aquatic photoautotrophs, including marine macroalgae (or seaweeds), remain underrepresented.

Seaweed traits and functional forms have been used for at least one century as a tool to answer various ecological and evolutionary questions. Since the early 1900s, traits have been explored to formulate life-form classification schemes for algae which intended to reflect habitat requirements and responses to environmental fluctuations [START_REF] Chapman | Life forms in the algae[END_REF][START_REF] Feldmann | Les types biologiques d'algues marines benthiques[END_REF], or describe different reproductive strategies (Clayton, 1988;De wreede and Kinger, 1988;[START_REF] Bell | Lectures on mathematics in life sciences: The evolution of haplo-diploid life cycles[END_REF]) used to explain various evolutionary questions [START_REF] Heesch | Evolution of life cycles and reproductive traits: insights from the brown algae[END_REF]. In the 1980s, [START_REF] Littler | The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of functional form model[END_REF]1983) used the adaptive value of morphological traits to categorise algal species into morpho-functional groups, which cluster species with similar ecological functioning. As the concept of morpho-functional groups is relatively easy to apply and can limit processing time and associated costs, it has been frequently applied in seaweed ecology (Veiga et al., 2013;Vélez-Rubio et al., 2021). As a result, multiple variations of the original six morpho-functional groups have been developed and applied in a wide range of contexts. For example, they have been applied to understand the distribution of communities along spatial [START_REF] Steneck | A functional group approach to the structure of algal-dominated communities[END_REF][START_REF] Wieters | Biogeographical boundaries, functional group structure and diversity of rocky shore communities along the Argentinean coast[END_REF][START_REF] Gaspar | Intertidal zonation and latitudinal gradients on macroalgal assemblages: Species, functional groups and thallus morphology approaches[END_REF] or environmental scales [START_REF] Balata | Increase of sedimentation in a subtidal system: effects on the structure and diversity of macroalgal assemblages[END_REF][START_REF] Gaspar | Intertidal zonation and latitudinal gradients on macroalgal assemblages: Species, functional groups and thallus morphology approaches[END_REF][START_REF] Gómez | Bio-optical and physiological patterns in Antarctic seaweeds: a functional trait based approach to characterize vertical zonation[END_REF][START_REF] Gómez | Form and Function in Antarctic Seaweeds: Photobiological Adaptations, Zonation Patterns, and Ecosystem Feedbacks[END_REF], the potential of communities to resist invasion [START_REF] Arenas | The invasibility of marine algal assemblages: role of functional diversity and identity[END_REF], and to evaluate the ecological status of coastal waters [START_REF] Orfanidis | Ecological Evaluation Index continuous formula (EEI-c) application: a step forward for functional groups, the formula and reference condition values[END_REF]). Yet, other recent research indicates that current morpho-functional groups may not capture enough variation to describe ecological functioning (Mauffrey et al., 2020;[START_REF] Ryznar | When form does not predict function: Empirical evidence violates functional form hypotheses for marine macroalgae[END_REF] and call for further development towards a broader trait-based approach that includes non-morphological and other traits (Mauffrey et al., 2020).

Seaweed trait information remains largely scattered, not widely available, and not semantically standardised, which has hampered the development and application of phycological trait-based approaches over broad taxonomic, spatial, or temporal scales. To overcome such drawbacks and enhance the development of a common ontology favouring the use and comparability of trait-based approaches on seaweeds, we present AlgaeTraits, a seaweed trait database for 1,745 species occurring along the Atlantic and Mediterranean coasts of Europe. We expand the spectrum of commonly used functional traits (i.e., measurable or quantifiable properties of individuals; https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License. [START_REF] Mcgill | Rebuilding community ecology from functional traits[END_REF] to include data on habitat, seasonality, morphology, life cycle, life history, and biogeographical range (Fig. 1, Table A1). In total, we describe 21 traits linked to taxonomic information, covering nine of the 10 previously prioritised traits in [START_REF] Costello | Biological and ecological traits of marine species[END_REF]. These data are available on the AlgaeTraits data portal algaetraits.org, doi: https://doi.org/10.14284/574 (AlgaeTraits, 2022), which is a subregister of the World Register of Marine species (WoRMS, 2022;Marine Species Traits, 2022). Here we introduce AlgaeTraits by (i) presenting the methodologies used to collect data, (ii) highlighting trait coverage for the current and first version of the database and (iii) exploring trait variability for a selected subset of traits.

Data

Trait collection

Trait data collection started with an extensive literature review in 2013, supported by the Biology project of the European Marine Observation and Data Network (EMODnet). In 2015, the data were further refined with expert opinions. In total, more than 200 references were used and 33 experts (all co-authors on this article) contributed by filling out a survey. For specific traits where interspecific variation is known to be minimal, trait information was documented in the World Register of Marine Species (WoRMS, 2022) at the genus level. The database behind WoRMS (Aphia, see further) is built in such a way that the information at the genus level is then automatically inherited to all species within this genus, if no information at the species level was provided or available. Traits that may have substantial interspecific variation, such as Blooming, Seasonality, Wave exposure, Zonation, and Body Size (Table A1), were not inherited from the genus to species level, and were only documented at the species level. Contributions were quality-checked to verify if they conformed to the survey and the database format.

Trait data

We included 21 traits for marine seaweeds, of which eight ecological traits, four morphological traits, six life cycle traits, and three life history related traits (Fig. 1, Table A1). Ecological traits relate to the habitat of the seaweed with respect to 'Environment' (Marine, Freshwater, Brackish), tidal 'Zonation', various degrees of 'Wave exposure', 'Environmental position' (substrate), 'Tolerance to organic pollutants', 'Vertical space use', and 'Seasonality'. In the few instances where seaweed species are known for their potential to form blooms this has been indicated as well (Fig. 1, Table A1). Morphological traits describe the thallus based on 'Body Shape', 'Body Size', 'Calcification', and 'Cytomorphology' (Fig. 1, Table A1). 'Body size' is the only quantitative trait included in AlgaeTraits and can be documented as a mean, maximum, or minimum value to describe the thallus length or diameter. Life history related traits describe patterns that influence demography and population dynamics, while life cycle traits relate to the various stages an organism undergoes from one stage in its development (e.g. fertilsation) to the same stage in the next generation [START_REF] Albecker | Does a complex life cycle affect adaptation to environmental change? Genome-informed insights for characterizing selection across complex life cycle[END_REF]) (Fig. 1, Table A1).

In addition to these 21 traits, species distributions were documented as ecoregions defined by Spalding et al. (2007) and can be used to subset the database according to geographic region. Moreover, WoRMS also displays species' occurrences of the Ocean Biodiversity Information System (OBIS; www.obis.org) (Fig. 1). Contrary to the other traits, 'Environment' and 'Distribution' were not uploaded as traits (i.e., attributes) in the database system (Aphia, see further) but as environment flags and distributions. This implies that 'Environment' and 'Distribution' are slightly different visualised on the AlgaeTraits data portal (www.AlgaeTraits.org).

https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

Taxonomy

The total number of described seaweeds is estimated at 9,250 species on a global scale [START_REF] Appeltans | The magnitude of global marine species diversity[END_REF][START_REF] Guiry | How many species of algae are there?[END_REF], of which at least 1,800 species occur in Europe [START_REF] Costello | European Register of Marine Species[END_REF]. The taxonomic classification of these species is not always straightforward and is continuously updated. To provide the best possible taxonomic accuracy, the trait data were implemented in WoRMS. WoRMS aims to provide a complete taxonomic authoritative list of all currently published names of marine species and is synchronised with AlgaeBase, the most complete database on global algal taxonomic information (Guiry and Guiry, 2022).

Meta-data

Every trait value is linked to a source (expert or literature) and a note field that can be used to include relevant meta-data related to specific trait-values. As values for the traits 'Asexual reproduction', 'Macroalgal Blooming', 'Body Size', and 'Seasonality' may display considerable geographic variation we assigned a specific locality to these trait values. Localities are defined as georegions obtained from the Marine Regions platform, which provides a hierarchical, standardised list of georeferenced marine regions and areas (www.MarineRegions.org) As mentioned above, life cycles of seaweeds can be complex and often consist of different life stages with radically different morphological, physiological, and ecological characteristics (Fig. 2). When relevant, trait values are documented for the specific life cycle stage they apply to (i.e., sporophyte, gametophyte, microthallus, macrothallus).

Database structure and management

The AlgaeTraits database is a thematic subregister of WoRMS, part of the Aphia platform [START_REF] Vandepitte | How Aphia -the platform behind several online and taxonomically oriented databases -can serve both the taxonomic community and the field of biodiversity informatics[END_REF]2018). The Aphia platform is an MS SQL (Microsoft Structured Query Language) database specifically built to include taxonomic data and related information such as biological traits. In total, Aphia contains more than 400 data fields, which are maintained by more than 500 experts under guidance of the WoRMS steering committee, which takes the lead on setting priorities and future directions, and coordination of the experts [START_REF] Vandepitte | How Aphia -the platform behind several online and taxonomically oriented databases -can serve both the taxonomic community and the field of biodiversity informatics[END_REF]2018). Both editors and database users are supported by a data management team that includes technical and scientific staff hosted at the Flanders Marine Institute (VLIZ) and can be contacted through info@marinespecies.org. This data management team is committed to safeguarding the integrity and online access of the database.

Results

Twenty-one traits were documented resulting in 45,195 entries for 2,830 accepted taxa according to AlgaeBase, among which 681 were at the genus level and 1,742 at the species level. Fifty-six percent of the trait entries for species were inherited from the genus level. 'Environment' and 'Cytomorphology' were the traits most documented for species, while the least information was provided for the traits that show substantial variation within genera and that were not inherited from genus to species level (Fig. 3).

https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

Morphology-related traits

Body shape

Seaweeds are known for their wide variation in body shapes, as illustrated in Fig. 4. For example, seaweeds can exist as filaments (filamentous) or be leaf-(foliose) or cushion-like (saccate). They can trail closely along the surface (prostrate) or be upright (erect), or take many other shapes (Table A1, Fig. 4). 'Body shape' had a high data coverage of 96% (1,678 species) at the species level (Fig. 3, Fig. 567).

Body size

Seaweed 'Body size' was described in several dimensions (thallus length, diameter, width, thickness, height) and varied from a few micrometres in thickness or width (e.g., filamentous, turf forming species such as Hapalospongidion macrocarpum) to several metres long (e.g., kelp such as Saccharina latissima). Compared to other traits, 'Body size' had a relatively low data coverage of 28% (490 species) for European accepted seaweed species (Fig. 3, Fig. 567).

Calcification

Several species in different taxonomic groups have calcified thalli (Fig. 8-10). In the green seaweed orders Dasycladales and Bryopsidales, calcification can occur as intra-or extracellular aragonite deposition, and both orders contain calcified articulated and calcified non-articulated species (Fig. 8). In European brown seaweeds, calcification is restricted to Padina (Dictyotales), where the surface of several species is covered with aragonite crystals [START_REF] Benita | Padina pavonica: morphology and calcification functions and mechanism[END_REF]) (Fig. 4A, Fig. 9). Calcification in various forms is present in four European orders of red seaweeds; in the Corallinales and Sporoplithales as calcite in the cell walls (Fig. 4D, Fig. 10), whereas the Peyssonneliales and Nemaliales deposit aragonite (Pentecost 1980). 'Calcification' had a high data coverage of 96% (1,670 species) on a European level (Fig. 3, Fig. 567).

Cytomorphology

'Cytomorphology' was the trait best documented on a European level and reached a data coverage of 99% (1,726 species) (Fig. 4, Fig. 567). Although the trait which distinguishes uni-from multicellular organisms and therefore might be perceived as trivial, in a seaweed context, it does set apart macroscopic multicellular thalli from a series of exotic cytomorphologies, including coenocytic and siphonal growth forms. Especially in green seaweeds (e.g., Bryopsidales and Dasycladales), the morphology of the thallus is decoupled from the formation of cells, which may result in thalli tens of centimetres tall and differentiated in blade-like structures, stolons and rhizoids, while still being essentially unicellular.

Ecology-related traits

Environmental position

'Environmental position' was well documented on the European level with 94% (1,636 species) (Fig. 3, Fig. 567). Most seaweeds grow attached to rock (epilithic) or other macrophytes (epiphytic), while some other species grow on animals (epizoic) or within rocks (endolithic), macrophytes (endophytic) or animals (endozoic) (Table A1). Many seaweeds are not very specific with respect to the substrate onto which they are attached. The same https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License. species may grow epilithically or epiphytically, but some species show high substrate specificity. Several diminutive algal species (e.g., Acrochaete, Acrochaetium, Laminariocolax and Myrionema) grow exclusively epiphytically, endophytically or even endozoically on a variety of hosts. At least for some species (e.g., Vertebrata lanosa being associated with Ascophyllum nodosum), high substrate specificity has been demonstrated (Garbary 2017).

Macroalgal blooming

'Macroalgal blooming' indicates the demonstrated capacity of a species to produce blooms. This trait had relatively low data coverage of 13% (233 species) on a European level (Fig. 3, Fig. 567). Notorious examples of blooming species include Ulva prolifera, Cladophora glomerata, Caulerpa cylindracea, holopelagic Sargassum and Rugulopteryx okamurae, and events have been often linked to eutrophication [START_REF] Charlier | How Brittany and Florida coasts cope with green tides[END_REF]Smetacek and Zingone 2013). The trait, however, shows considerable variation with geographic location. This is exemplified by several non-native species, which bloom in the invaded region while showing non such behaviour in their regions of origin. This variation was incorporated in the database by linking entries for 'Macroalgal blooming' to geographic localities.

Seasonality

'Seasonality' had a relatively low data coverage of 14% on a European level (249 species) (Fig. 3, Fig. 567).

Seaweeds with large geographical ranges adapt to local seasonal conditions by adjusting their phenology [START_REF] Lüning | Seaweeds: their environment, biogeography, and ecophysiology[END_REF]. It is therefore possible for a species to be present in one season in one part of its range while being absent elsewhere.

Vertical space

All types of 'Vertical space' (encrusting, turf, sub-canopy, canopy; Table A1) occur and vary among and within orders of the green (Fig. 8), brown (Fig. 9) and red seaweeds (Fig. 10). 'Vertical space' had a moderate coverage of 46% on European level (808 species) (Fig. 3, Fig. 567).

Tolerance to organic pollutants

Some seaweeds have a lower tolerance to turbidity or nutrient concentrations than others (Table A1). For example, Choristocarpus tenellus is mainly observed in waters with low nutrient levels and high visibility (oligotrophic, clear water; Table A1), while Ulva spp. are mainly observed from waters with mid to high nutrient concentration (meso-, eutrophic; Table A1). 'Tolerance to organic pollutants' was covered for 39% of European accepted seaweeds (678 species) (Fig. 3, Fig. 567).

Wave exposure

Some seaweed species are solely known from habitats with low energy wave forces (sheltered; Table A1) such as Chaetomorpha adrianii or from habitats with solely high energy wave forces (exposed; Table A1) such as Valonia utricularis. Other seaweeds can occur in a variety of wave exposures including sheltered semi-exposed and exposed such as the non-native Sargassum muticum. 'Wave exposure' had a relatively low coverage of 18% on the European level (315 species) (Fig. 3, Fig. 567).

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Zonation

Many species are physiologically adapted to endure the stress of tidal differences and daily changes between desiccation and submersion (e.g. Pelvetia canaliculata). Other species will only occur below the low water mark and do not endure such high variation in desiccation, salinity, temperature or other stressors under normal conditions (e.g. Alaria esculenta). 'Zonation' had a relatively low data coverage of 18% on a European level (316 species) (Fig. 3, Fig. 567).

Life cycle related traits

Life cycle

Information on 'Life cycle' was available for 95% of European seaweed species (1,660 species) (Fig. 3, Fig. 567). Many seaweeds have a biphasic or haplodiplontic life cycle in which a diploid sporophytic and a haploid gametophytic life phases alternate. These can have a similar (isomorphic; e.g., Chondrus crispus) or distinct (heteromorphic) body shape (e.g., Laminariales) (Fig. 2). Haplodiplontic life cycles are the dominant type of life cycle in the brown (Fig. 9) and red (Fig. 10) seaweeds. Other seaweeds have a monophasic life cycle that is either diploid (diplontic) or haploid (haplontic) (Fig. 2). Variation in the life cycle has been documented in several species either in the lab (e.g., in reds, [START_REF] Maggs | Intraspecific life history variability in the Florideophycidae (Rhodophyta)[END_REF]in Ectocarpus, Coelho et al., 2012) or in the field (e.g., in Gracilaria, [START_REF] Destombe | What controls haploid-diploid ratio in the red alga, Gracilaria verrucosa?[END_REF]. However, the knowledge about the processes driving this variation (e.g. epigenetic (plastic) or genetic bases) is not known.

Asexual reproduction

In many seaweeds, sexual reproduction occurs alongside asexual reproduction (i.e., partial clonality) that does not involve fusion of gametes or meiosis and usually results in progeny with an identical genetic constitution to the parent and to each other (Table A1). Asexual reproduction is widely spread in green, brown, and red seaweeds (Fig. 8-10) and can happen through fragmentation, direct development of spores, parthenogenesis, or other mechanisms. 'Asexual reproduction' had a high data coverage of 95% on a European level (1,649 species) (Fig. 3, Fig. 567).

Dispersion mode

Seaweed dispersal is heavily influenced by ocean currents and water motion (but in red seaweeds, animal mediated transport of male gametes could be important, [START_REF] Lavaut | Pollinators of the sea: A discovery of animal-mediated fertilization in seaweed[END_REF] and is in most cases limited in spatial scale.

But dispersal over longer distances is also possible when the species can for example drift, or the dispersal is mediated by vectors such as boat hulls (Table 1A). 'Dispersion mode' has a moderate data coverage of 80% on the European level (1,401 species) (Fig. 3, Fig. 567).

Gamete type

'Gamete type' varies among and within orders of green and brown seaweeds (Fig. 8, Fig. 9). In red seaweeds, 'Gamete type' is more conserved: male gamete is unflagellated (spermatia) and fertilisation takes place in the female organ called the carpogonium. This type of reproduction is considered oogamous when information is available. This trait was documented for 95% of the European seaweeds (1,661 species) (Fig. 3, Fig. 567).

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Gametophyte arrangements

In seaweeds, the male and female gametes can be formed on the same or separate thalli (mono-vs. di-), sex determination can happen in both the haploid and diploid life phase depending on the taxon (-oicous vs. -oecious) (Fig. 3, Table A1). For example, in fucoids, sex determination occurs in the diploid-dominant stage, whereas, in all red seaweeds, sex determination occurs in the haploid stage. 'Gametophyte arrangement' was documented for 93% of the European seaweed species (1626 species) (Fig. 3, Fig. 567).

Spawning

For the majority of the brown and green seaweeds, fertilisation occurs in the water column, but in red seaweeds, male gametes are not flagellated and fertilisation occurs on the female gametophyte and gives rise to the 'third phase' of the life cycle called the carposporophyte. 'Spawning' has been documented for 95% of European species (1,658 species) (Fig. 3, Fig. 567).

Life history-related traits

Generation time

Of all traits, least information was collected for the trait 'Generation time' (Fig. 4B). In seaweeds, generation time can vary from just a few weeks in Ulva [START_REF] Wichard | The green seaweed Ulva: a model system to study morphogenesis[END_REF] to multiple decades such as in Gracilaria [START_REF] Engel | Population dynamics and stage structure in a haploid-diploid red seaweed, Gracilaria gracilis[END_REF] or Ascophyllum (Åberg 1992). Generation time was documented for only 7% of the European seaweed (117 species) (Fig. 3, Fig. 567).

Life span

'Life span' varies within and among European green, brown, and red seaweeds (Fig. 8-10). Perennial macroalgae can live up to multiple years such as for several years, such as many kelp species (Laminariales), or Gracilaria gracilis that can live for more than 50 years [START_REF] Engel | Population dynamics and stage structure in a haploid-diploid red seaweed, Gracilaria gracilis[END_REF], or Ascophyllum nodosum, which can live for more than 120 years (Åberg 1992) . In contrast, annuals live only a few months, such as several small filamentous species (e.g. Chaetomorpha). At the European level, data coverage was high for 'Life span', 95% (1,652 species) (Fig. 3, Fig. 567).

Reproductive frequency

Data coverage was limited for 'Reproductive frequency', with data available for only 25% for the European species (427 species) (Fig. 3, Fig. 567).

Discussion

AlgaeTraits includes 21 traits, 1,742 European seaweed species, and is structured within a general framework and ontology aiming to describe all marine species [START_REF] Costello | Biological and ecological traits of marine species[END_REF]. With a mean coverage of ~60% per trait, this database will be a solid tool for a variety of biological research and related fields, including marine conservation, nature-based solutions, and aquaculture. For example, traits can be used to monitor community and ecosystem changes [START_REF] Mcgill | Rebuilding community ecology from functional traits[END_REF]Vélez-Rubio et al., 2021) or to identify conservation priorities (Albouy et al., 2017;[START_REF] Cardeccia | Assessing biological invasions in European Seas: Biological traits of the most widespread nonindigenous species[END_REF]Esmaeili et al., 2022). In addition, they can be incorporated into predictive modelling to assess eco-evolutionary consequences of climate change [START_REF] Schleuning | Trait-based assessments of climate-change impacts on interacting species[END_REF], can contribute to predicting the invasiveness of species (Nyberg and Wallentinus, 2005;[START_REF] Quell | Biological trait profiles discriminate between native and non-indigenous marine invertebrates[END_REF]), be used in research aiming to better understand the driving forces of evolutionary trait history [START_REF] Heesch | Evolution of life cycles and reproductive traits: insights from the brown algae[END_REF], or the mechanisms of community assembly [START_REF] Weiss | Unifying functional trait approaches to understand the assemblage of ecological communities: synthesizing taxonomic divides[END_REF], and can even help to assess ecosystem services vulnerability (Díaz et al., 2013;Stevenson, 2014).

The AlgaeTraits database complements recent efforts to collect and publicly provide well-structured and organised seaweed trait data. Just as MarLIN (2006) and SeaTraIn (2022) we focussed on biologically important traits. But contrary to these other initiatives, AlgaeTraits includes all European seaweed species, and presents a different, yet overlapping, set of traits. MarLIN (2006) covers over 40 traits, of which 12 overlap with AlgaeTraits, but is limited to only 30 seaweed species. SeaTrain (2022) covers around 10 traits, of which two traits overlap with AlgaeTraits, and includes 96 seaweed species. As to taxonomic coverage (1,742 species) and inclusion of functional important traits as prioritised by [START_REF] Costello | Biological and ecological traits of marine species[END_REF], AlgaeTraits is the most extensive seaweed trait database published so far.

In this first version of AlgaeTraits, not all traits are available for all species yet, and the current list of traits is not yet complete. For example, other key eco-evolutionary traits that might be considered to be included in the database are 'Tolerance to light', 'Tolerance to temperature', 'Tolerance to grazing', 'Tolerance to sedimentation' or 'Tolerance to epiphytism'. There is currently no possibility to describe parasitic algal life forms in the database, ignoring a relatively diverse group of red algae. Completion and further refining and expanding the database will be an ongoing effort of the AlgaeTraits editor community. AlgaeTraits currently has five thematic editors, who actively update the trait information on a voluntary basis. During an upcoming workshop (December 2022), more experts will be trained to contribute to AlgaeTraits through the online editing interface, and expansion of this European database to a global level will be initiated. The AlgaeTraits editorial community will also need to report to the WoRMS steering committee. As the database expands, adding new traits or trait values can be considered under thorough consideration and discussion with the WoRMS steering committee and data management team.

For now, traits are included at the species level in AlgaeTraits. However, multiple traits can exhibit substantial intraspecific variation [START_REF] Kattge | A generic structure for plant trait databases[END_REF]. For example, morphological seaweed traits can differ among populations depending on underlying genetic patterns [START_REF] Serisawa | Growth and survival rates of large-type sporophytes of Ecklonia cava transplanted to a growth environment with small-type sporophytes[END_REF], or depending on environmental conditions such as wave exposure with rather smaller and more slender individuals in exposed than sheltered localities (Ruuskanen et al., 1999;Fowler-walker et al., 2006;[START_REF] Kim | Geographic differentiation of morphological characteristics in the brown seaweed Sargassum thunbergii along the Korean coast: A Response to Local Environmental Conditions[END_REF]. But also, habitat preference, lifehistory [START_REF] Araújo | Phenotypic differentiation at southern limit borders: the case study of two fucoid macroalgal species with different life-history traits[END_REF] or life-cycle traits can vary intraspecifically. Some seaweeds reproduce sexually under normal conditions but change to asexual reproduction under specific environmental conditions [START_REF] Demes | Abiotic regulation of investment in sexual versus vegetative reproduction in the clonal kelp Laminaria Sinclairii (laminariales, Phaeophyceae)[END_REF]Murúa et al., 2017) or at the limits of their distribution (e.i. geographic parthenogenesis [START_REF] Oppliger | Alteration of sexual reproduction and genetic diversity in the kelp species Laminaria digitata at the southern limit of its range[END_REF]Hoshino et al., 2021). Intraspecific trait variation is thus caused by both genetic variation and phenotypic plasticity and can be a response to improve performance under specific environmental biotic or abiotic conditions [START_REF] Kattge | A generic structure for plant trait databases[END_REF]. At the moment, we considered intraspecific variation by assigning localities (or life stages) to the trait values when possible, or specifying detailed information in the note field. However, complementary approaches measuring trait information at specimen level (e.g., Mauffrey et al., 2020;Cappelatti et al., 2019) are useful, especially for quantitative traits, to fully capture intraspecific trait variability and allow more in-depth analysis.

https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

Data Availability

The data can be accessed from the AlgaeTraits portal, algaetraits.org, doi: https://doi.org/10.14284/574 (AlgaeTraits, 2022).

Conclusion

We provided a consolidated database of important traits of European seaweeds that is distinct in its completeness and taxonomic coverage. Because the database is standardised and fits within the broader framework of WoRMS that aims to include all taxa described, it serves not only as a significant resource for phycological research focusing on trait-based ecology or evolution, but also for general macro-ecological and macroevolutionary research in general. The database can help to explore ecological questions about relations among traits or help to unravel taxonomic and evolutionary patterns of traits in seaweeds. Because some trait values vary geographically and some traits values were documented at the genus level, the database may not always provide the highest variation at the species level. However, an active thematic editorial community is currently committed to further updating and improving the quality of this European database and expanding it to a global level to facilitate thorough and broad scale trait-based analysis.

Littoral zone

The part of the shore covering the intertidal and the splash zone, with the upper limit marked by the top of the lichen zone and Crustose / Forming a thin crust on the substratum, appl. certain lichens, sponges, algae [START_REF] Lawrence | Henderson's dictionary of Biology[END_REF].

Cushion-like / Approximating the shape of a cushion [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Discoid / (1) Flat and circular;

(2) Disc-shaped [START_REF] Lawrence | Henderson's dictionary of Biology[END_REF].

Erect / Upright.
Filamentous / Existing out of a branched or unbranched row of cells joined end to end [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Filiform / resembling a filament.

Flabellate / Fan-shaped, thallus usually expanding upward from a narrow base.

Foliose / Leaf-like [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Mucilaginous / consisting of a slippery and slimy texture [START_REF] Maggs | Seaweeds of the British Isles Volume 1 Rhodophyta Part 3A Ceramiales, The Natural History Museum[END_REF] https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

Trait group Trait Trait value Trait child value Definition

Pinnate / With laterals or branches arranged along each side of an axis or branch [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Prostrate / Trailing on the ground or lying closely along a surface [START_REF] Lawrence | Henderson's dictionary of Biology[END_REF].

Saccate / Inflated, or sac-like [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Siphonous / An algal growth form that is filamentous, tubular, multinucleate and with a few cross-walls, if any [START_REF] Brodie | Green Seaweeds of Britain and Ireland[END_REF].

Spheric / Approximating the shape of a sphere [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Stoloniferous / forming a prostrate axis, lying on or in the substrate, from which erect branches arise [START_REF] Womersley | The marine benthic flora of southern Australia. Part I: Chlorophyta[END_REF].

Tubular / In the form of a tube, having tubes, consisting of tubes [START_REF] Lawrence | Henderson's dictionary of Biology[END_REF]. Unicellular siphonous An algal growth form that is filamentous, tubular, multinucleate and with a few cross-walls, if any [START_REF] Brodie | Green Seaweeds of Britain and Ireland[END_REF].

Unreported

Non-unicellular

Having more than one cell or consisting of more than one cell (adapted from [START_REF] Lawrence | Henderson's dictionary of Biology[END_REF].

Non-unicellular coenocytic

With cells being multinucleate. [START_REF] Lincoln | Dictionary of ecology, evolution and systematics[END_REF].

Life

Isogamous / Having gametes that are similar in size, shape and behaviour; having gametes (isogametes) not differentiated into male and female [START_REF] Lincoln | Dictionary of ecology, evolution and systematics[END_REF].

Oogamous / Having a reproduction involving a large, non-motile female gamete (egg cell) and a small, motile male gamete (sperm cell or equivalent), except for red algae in which the male gamete is also non-motile [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF]. [START_REF] Lincoln | Dictionary of ecology, evolution and systematics[END_REF].

Haplodiplontic / Having a life cycle with alternating freeliving gametophyte and sporophyte phases [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Haplodiplontic Heteromorph ic

Organisms with the gametophyte and sporophyte of different morphology and size [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Haplodiplontic Isomorphic

Organisms with the gametophyte and sporophyte of similar morphology and size [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Haplodiplontic Not applicable

It is not applicable whether this taxon is heteromorphic or isomorphic.

Haplodiplontic Unknown

According to literature it is unknown whether this organism is heteromorphic or isomorphic.

Haplodiplontic Unreported So far it has not been reported in literature whether this taxon is heteromorphic or isomorphic.

Haplontic / Having a life cycle in which meiosis occurs in the zygote to produce the haploid phase;

only the zygote is diploid [START_REF] Lincoln | Dictionary of ecology, evolution and systematics[END_REF]. plant that completes its life cycle in a year. [START_REF] Lawrence | Henderson's dictionary of Biology[END_REF]. Thallus which survives only one growing season (less than 1 year) [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF]. (3) completing life cycle within a brief period; (4) n. a short-lived plant or animal species [START_REF] Lawrence | Henderson's dictionary of Biology[END_REF]. Thallus which survives for only a few weeks (less than 1 month) [START_REF] Womersley | A re-classification of the Acrochaetiales based on molecular and morphological data, and establishment of the Colaconematales ord. nov. (Florideophyceae, Rhodophyta)[END_REF].

Unknown

Perennial / Plant which persists for several years [START_REF] Lawrence | Henderson's dictionary of Biology[END_REF].

  https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

  https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

  photosynthesis is still possible.Unreported/ unreported

  https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

  individual of the same ploidy (exospore, endospore, monospore,

  not reproduce asexually, which is reproduction which does not involve formation and fusion of gametes and results in progeny with an identical genetic constitution to the parent and to each other. Reproduction may occur by binary fission, budding, asexual spore formation or vegetative propagation. In asexual division in eukaryotic organisms, all cell divisions are by mitosis. the thallus can be lost and drift. https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

  https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

Figure 1 .

 1 Figure 1. A) Relation of AlgaeTraits to other databases. AlgaeTraits is a subregister of the World Register of Marine Species (WoRMS), which aims to provide an comprehensive authoritative list of all published names of marine organisms and other biological information including traits. AlgaeBase, the most complete list on global algal taxonomy, is used as the main source for algal taxonomy in WoRMS. WoRMS and AlgaeTraits display OBIS occurrence data. All traits included in WoRMS and AlgaeTraits were collected under the EMODnet project. B) All 21 traits currently included in AlgaeTraits can be categorised under 'Morphology', 'Life History', 'Life Cycle' and 'Ecology'.

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	Trait group Trait	Trait value	Trait child	Definition
			value
				the gametes are haploid
		Not applicable	/	The attribute "gamete type" is not
				applicable for this taxon.
		Unknown	/	According to literature it is unknown
				which gamete type this organism has.
		Unreported	/	So far it has not been reported in literature
				what the gamete type is for this taxon.

https

  ://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License. Source literature Van der Strate, H. J.; Van de Zande, L.; Stam, W. T.; Olsen, J. L. (2002). The contribution of haploids, diploids and clones to fine-scale population structure in the seaweed Cladophoropsis membranacea (Chlorophyta). Mol. Ecol. 11, 329-345. literature Leliaert, F.; Coppejans, E.; De Clerck, O. (1998). The Siphonocladales sensu Egerod (Chlorophyta) from Papua New Guinea and Indonesia (Snellius-II Expedition). Belgian Journal of Botany. 130, 177-197. literature Kawai, H.; Tokuyama, M. (1995). Laminarionema elsbetiae gen. et sp. nov.(Ectocarpales, Phaeophyceae), a new endophyte in Laminaria sporophytes. Phycol Res. 43, 185-190. literature Maggs, C. A.; Douglas, S. E.; Fenety, J.; Bird, C. J. (1992). A molecular and morphological analysis of the Gymnogongrus devoniensis (Rhodophyta) complex in the North Atlantic. Journal of Phycology. 28(2): 214-232. literature Bressan, G.; Babbini, L. (2003). Biodiversità marina delle coste Italiane: Corallinales del Mar Mediterraneo: guida all deteminazione. 10, 1-237. literature Norris, R. E. (1991). The structure, reproduction and taxonomy of Vidalia and Osmundaria (Rhodophyta, Rhodomelaceae). Botanical Journal of the Linnean Society. 106(1): 1-40. expert Verlaque, Marc. Institut Méditerranéen d'Océanologie. marc.verlaque@mio.osupytheas.fr literature Cochrane, et al. (2010). Marine Strategy Framework Directive Task Group 1 Report. Biological Diversity. JRC Scientific and Technical Reports; OSPAR 2010 Background Document for Maërl beds. OSPAR Commission Biodiversity Series. Publication Number: 491/2010. ISBN 978-1-907390-32-6. literature Cortel-Breeman, M. C.-B.; Van Den Hoek, C. (1970). Life-history studies on Rhodophyceae I. Acrosymphyton purpuriferum. J. Ag.) Kyl. Acta Bot. Neerl. 19, 265-284. literature Clayden, S. L.; Saunders, G. W. (2010). Recognition of Rubrointrusa membranacea gen. et comb. nov., Rhodonematella subimmersa gen. et comb. nov. (with a reinterpretation of the life history) and the Meiodiscaceae fam. nov. within the Palmariales (Rhodophyta). Phycologia. 49(3), 283-300. literature Loiseaux-de-Goër, S.; Noailles, M. -C. (2008). Algues de Roscoff. Editions de la Station Biologique de Roscoff. p. 215. literature Schneider, C. W.; Chengsupanimit, T.; Saunders, G. W. (2011). A new genus and species from the North Atlantic, Archestenogramma profundum (Phyllophoraceae, Rhodophyta), with taxonomic resolution of the orphaned Leptofauchea brasiliensis. Eur. J. Phycol. 46, 442-452.

	Type Type	Source
	literature	Womersley, H. B. S. (1996). The marine benthic flora of southern Australia -Rhodophyta -Part
		III B. In: Flora of Australia, supplementary series, number 5. Australian biological resources study
		Canberra, p. 392 pp.
	literature	Barcelo Marti, M.; Gallardo Garcia, T.; Gomez Garreta, A.; Perez Ruzafa, I.; Ribera Siguan, M.;
		Rull Luch, J. (2001). Flora Phycologica Iberica, vol 1: Fucales. Universidad de Murcia.
	literature	Taylor, W. R. (1985). Marine algae of the eastern tropical and subtropical coasts of the Americas.
		The University of Michigan press, Michigan.
	literature	Abbott, I. A. (1999). Marine red algae of the Hawaiian Islands. Bishop Museum Press, Hawaii,
		Honolulu.
	literature	Perennial Burrows, E.M. (1991). Seaweeds of the British Islands, vol. 2 Chlorophyta. Natural History Long Thallus or part thereof with a lifespan
		perennial Museum Publications London, p. 238 pp.	exceeding 3 years (more than 3 years)
			Perennial		Short	Thallus or part thereof with a lifespan
					perennial	exceeding 1 year but under 3 years.
			Unreported	/	So far it has not been reported in literature
					which life span this organism has.
		Reproductive	Throughout the	/	Fertile individuals observed throughout the
		frequency	year		year.
			One long period	/	A unique fertility period lasting more than
			a year		1 month.
			One	short	/	A unique fertility period lasting less than 1
			period a year	month.
			Several	long	/	Several distinct fertility periods lasting
			periods a year	more than 1 month each.
		Several short Woolman, Government Printer, South Australia, Adelaide. / Several distinct fertility periods lasting less
			periods a year	than 1 month each.
	literature	Spawning Womersley, H.B.S. (1998). The marine benthic flora of Southern Australia. Rhodophyta. Part III Fertilization in / Fertilization with gametes released in the
		the C: Rhodophyceae, Ceramiaceae, Dasyaceae. State Herbarium, South Australia. water water column.
	literature	column Schnetter, R.; Brück, B.; Gerke, K.; Seibold, G. (1990). Notes on heterokaryotic life cycle phases
		Fertilization on in some Dasycladales and Bryopsidales (Chlorophyta). In: Cell Walls and Surfaces, Reproduction, / Female gamete retained on the female
		the Photosynthesis. Springer, pp. 124-133. female	gametophyte (e.g. Rhodophyta).
	literature	gametophyte Díaz-Tapia, P.; Bárbara, I. (2013). Seaweeds from sand-covered rocks of the Atlantic Iberian
		Not applicable Peninsula. Part 1. The Rhodomelaceae. (Ceramiales, Rhodophyta). Cryptogamie Algologie. 34(4): / The attribute "spawning" is not applicable
		325-422.			for this taxon.
			Unknown		/	According to literature it is unknown
					which spawning mechanism this organism
					has.
			Unreported	/	So far it has not been reported in literature
					whether there is spawning for this taxon.

https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License. literature Womersley, H. B. S. (2003). The marine benthic flora of southern Australia -Rhodophyta -Part III D (Ceramiales, Delesseriaceae, Sarcomeniaceae, Rhodomelaceae). In: Flora of Australia, supplementary series, number 18. Australian biological resources study and the State Herbarium of South Australia Canberra, pp. 533 pp., ill. literature Stegenga, H.; Anderson, R. J.; Bolton, J. J. (2000). Notes on Ceramiaceae (Rhodophyta) from the eastern Cape Province, South Africa. III. New records from the Tsitsikamma coastal park, with the description of Scageliopsis tsitsikammae. Blumea. 45, 485-494. literature Wang, W. J.; Zhu, H. Y.; Xu, P.; Xu, J. R.; Lin, X. Z.; Huang, C. K. (2008). Characterization of the life history of Bangia fuscopurpurea (Bangiaceae, Rhodophyta) in connection with its cultivation in China. Aquaculture. 278, 101-109. literature Womersley, H.B.S. (1984). The marine benthic flora of southern Australia. Part I: Chlorophyta. literature Van Reine, W. P. (1982). A taxonomic revision of the European Sphacelariaceae:(Sphacelariales, Phaeophyceae). Brill Archive. literature Coppejans, E. (1995). Flore algologique des côtes du Nord de la France et de la Belgique. In: Scripta botanica Belgica, p. 454. httpsliterature Hasle, G. R.; Syvertsen, E. E. (1997). Marine Diatoms. pp. 5-385. In: C.R. Tomas (ed.) (1997). Identifying Marine Phytoplankton. Academic Press: San Diego, CA [etc.] (USA). ISBN 0-12-693018-X. XV, 858 pp.

Acknowledgements

Authors Stefanie Dekeyzer, Wim Decock and Leen Vandepitte have been supported through the EMODnet Biology project (MARE/2012/10/SI2.657705). This work makes use of data and/or infrastructure provided by VLIZ and funded by Research Foundation -Flanders (FWO) as part of the Belgian contribution to LifeWatch. This work used resources and facilities provided by UGent as part of the Belgian contribution to EMBRC-ERIC (FWO GOH3817N and I001621N) https://doi.org/10.5194/essd-2022-329 Preprint. Discussion started: 14 October 2022 c Author(s) 2022. CC BY 4.0 License.

Author contribution:

SV, MR, IBD, IB, AB, C-FB, CD, BDR, PD-T, AH, RJ, RK. PK, SAKH, RK, AFP, VP, CP-C, FB, FR, JR, HS, IKS, MS, DS, TT, MVa, AV, MVe, CV, LL, FL and ODC contributed data. SV and MR collated the data and performed quality control. SD, WD, BV, LV supported data curation. SV performed analysis and wrote the original draft with help from MR, LV, LL, FL, ODC. All authors approved and contributed to the final draft for submission.

Competing interests

The authors declare that they have no conflict of interest.

Appendix A 593

Table A1 Trait definitions as applied in AlgaeTraits. When no reference is provided, definitions are created by the Growing within a rock or other hard inorganic or organic substratum [START_REF] Lincoln | Dictionary of ecology, evolution and systematics[END_REF].

Endophytic / Living within a plant tissue or macroalgal thallus and not deriving nourishment from it.

Endozoic / Living within or passing through the body of an animal and not deriving nourishment from it.

Epilithic / Growing on rocks or other hard inorganic or organic substrata [START_REF] Lincoln | Dictionary of ecology, evolution and systematics[END_REF].

Appendix B 599

Table B1. Sources used in the database, ordered from most to least used.