Karima Ferchichi

Noureddine Amdouni

Yves Chevalier

Souhaira Hbaieb
email: souhaira.hbaieb@fst.utm.tn

Low-cost Posidonia oceanica bio-adsorbent for efficient removal of antibiotic oxytetracycline from water

Keywords: Posidonia biomaterial, Antibiotic removal, Adsorption, Bi-Langmuir isotherm model, Thermodynamic parameters

The presence of antibiotics as micro-contaminants in the water and aqueous environments is a health concern to humans and the ecosystem. Therefore, their elimination by adsorption to available and cheap materials in water treatment plants is a research topic of high relevance. The present paper reports on the adsorption behavior of Oxytetracycline on a bio-adsorbent prepared from Posidonia Oceanica; an abundant Mediterranean biomass.

Characterization of the pretreated Posidonia biomaterial was achieved using several analyses such as Boehm acidbase titration method, pHPZC determination and analysis techniques (FTIR, 13 C CP-MAS NMR, optical microscopy and TGA). The pHPZC occurred around pH 2.11. Posidonia biomaterial showed a fast and high uptake rate throughout the adsorption process, which is a definite advantage for analytical applications such as water decontamination. The experimental kinetic data fitted very rightly the pseudo-second-order kinetic model and the equilibrium uptake can adopt the bi-Langmuir isotherm model for all studied pH values which assumes adsorptions at the two localized sites. Maximum adsorption capacities of 11.8 mg•g -1 and 4.4 mg•g -1 for the two adsorption sites are reached at pH 6. The oxytetracycline adsorption process onto Posidonia bio-adsorbent is spontaneous (ΔadsG 0 < 0), exothermic (ΔadsH 0 < 0), and entropically favorable (ΔadsS 0 > 0). The effect of pH on adsorption behavior and the thermodynamic parameters of adsorption are consistent with a possible origin of adsorption of Oxytetracycline by means of hydrogen bonding interactions between surface hydroxyl and phenolic groups of the biomaterial and Oxytetracycline. The proposed green and environmentally friendly biomaterial offers potential benefits as a bio-adsorbent in the remediation of aquatic environments contaminated by various organic materials.

Introduction

Oxytetracycline (OTC) is an antibiotic applied for the treatment of bacterial infections in humans and animals [START_REF] Ma | Toxicity of OTC to Ipomoea aquatica Forsk and to microorganisms in a long-term sewage-irrigated farmland soil[END_REF]. Curative and preventive treatments of bacterial infections improve the production of farm animals; this is the reasons why OTC is widely used in animal husbandry such as aquaculture and livestock [START_REF] Lu | A risk-based approach for managing aquaculture used oxytetracycline-induced TetR in surface water across Taiwan regions[END_REF][START_REF] Qin | Carbon dots and Eu 3+ hybrid-based ratiometric fluorescent probe for oxytetracycline detection[END_REF]. The use of OTC in dairy cows is beneficial to farmers, which has improved production performance. However, this antibiotic is a chemical that persists for a long time in the animal tissues and in the environment. It finally accumulates in the environment, especially in water, which can lead to the spread of antibiotic resistance genes and disrupt the functioning of the ecosystem [START_REF] Zhao | Functionalized carbon quantum dots as fluorescent nanoprobe for determination of tetracyclines and cell imaging[END_REF]. The development of resistant species that can be extracted in bovine milk is considered a significant source of toxicological harmful effects to consumers such as allergic reactions, liver damage, tooth yellowing, and gastrointestinal disturbance [START_REF] Liu | Recent advances in sensors for tetracycline antibiotics and their applications[END_REF]. To protect humans from exposure to these drug residues present in water, there is a need for effective and robust methods to separate micro-pollutants from contaminated water. In this respect, very different technologies for antibiotic removal from contaminated water are reported [START_REF] Cheng | Adsorption of emerging contaminants from water and wastewater by modified biochar: A review[END_REF][START_REF] Leon-Condes | A coupled ozonationelectrooxidation treatment for removal of bisphenol A, nonylphenol and triclosan from wastewater sludge[END_REF][START_REF] Fanourakis | Nano-based adsorbent and photocatalyst use for pharmaceutical contaminant removal during indirect potable water reuse[END_REF][START_REF] Ribeiro | Cephalosporin antibiotics in the aquatic environment: A critical review of occurrence, fate, ecotoxicity and removal technologies[END_REF] including electrochemical oxidation (Dos [START_REF] Santos | Recent advances in electrochemical water technologies for the treatment of antibiotics: A short review[END_REF][START_REF] Rahmani | A combined advanced oxidation process: electrooxidation-ozonation for antibiotic ciprofloxacin removal from aqueous solution[END_REF], photocatalytic degradation [START_REF] Chenguang | Sequential combination of photocatalysis and microalgae technology for promoting the degradation and detoxification of typical antibiotics[END_REF], ultrafiltration [START_REF] Hembach | Dissemination prevention of antibiotic resistant and facultative pathogenic bacteria by ultrafiltration and ozone treatment at an urban wastewater treatment plant[END_REF] and chemical precipitation [START_REF] Saleh | Water treatment technologies in removing heavy metal ions from wastewater: A review[END_REF]. However, such techniques have several limitations pertaining to their cost, efficiency, design and durability. The most widely used method relies on adsorption, which is of high efficiency and low operating costs [START_REF] Banhishikha | The effective adsorption of tetracycline onto zirconia nanoparticles synthesized by novel microbial green technology[END_REF][START_REF] Dutta | Removal of antibiotic from the water environment by the adsorption technologies: A review[END_REF][START_REF] Geetha | A review on tetracycline removal from aqueous systems by advanced treatment techniques[END_REF]). The conventional adsorbent made of modified silica [START_REF] Ayadi | Molecularly imprinted polyaniline on silica support for the selective adsorption of benzophenone-4 from aqueous media[END_REF][START_REF] Zeidman | Removal of antibiotics in aqueous phase using silica-based immobilized nanomaterials: A review[END_REF]) is a rather expensive material [START_REF] Ayadi | Molecular imprints frozen by strong intermolecular interactions in place of cross-linking[END_REF][START_REF] Han | Modification of naturally abundant resources for remediation of potentially toxic elements: A review[END_REF]. Alternative low-cost adsorbents derived from natural materials, industrial and agricultural solid wastes have been proposed in recent investigations [START_REF] Gupta | Application and efficacy of low-cost adsorbents for metal removal from contaminated water[END_REF]. Indeed, adsorption using biomass materials has been demonstrated to be one of the easiest and most efficient ways to uptake and retain various contaminants from contaminated matrices [START_REF] De Gisi | Characteristics and adsorption capacities of low-cost sorbents for wastewater treatment[END_REF]. For example, a few studies aiming at fixing such issues, put forward the use of biochar as a low-cost adsorbent material [START_REF] Wang | Recent advances in engineered biochar productions and applications[END_REF]. As instances, virgin softwood biochar was used as an adsorbent medium to remove dissolved arsenic from contaminated groundwater [START_REF] Boni | Experimental and numerical study of biochar fixed bed column for the adsorption of arsenic from aqueous solutions[END_REF]; and rambutan peel waste hydrochar was applied as an adsorbent to remove Fe(II) contaminants from aqueous media [START_REF] Normah | Hydrothermal carbonization of rambutan peel (Nephelium lappaceum L.) as a green and low-cost adsorbent for Fe(II) removal from aqueous solutions[END_REF]. Several research studies have also indicated that certain methods can be used to remove recalcitrant contaminants such as carbamazepine from water by adsorption onto granular activated carbon and biological activated carbon [START_REF] Décima | A Review on the removal of carbamazepine from aqueous solution by using activated carbon and biochar[END_REF]. Additionally, technologies incorporating the modification of biochar have been reported to improve their sorption capacity for various chemical contaminants. For instance, modified coal fly has much higher sorption ability to acid and reactive dyes than carbon black or chitosan [START_REF] Hussain | Modification of coal fly ash and its use as low-cost adsorbent for the removal of directive, acid and reactive dyes[END_REF]. The present study aims at investigating the feasibility and potential benefits of introducing marine seagrass balls as a bio-adsorbent. Posidonia Oceanica (L.) Delile, from the Posidoniaceae family and commonly known as Neptune grass or Mediterranean tapeweed, a native biomass abundant on the coasts of Tunisia, has demonstrated its ability to remove both organic and inorganic molecules [START_REF] Douissa | Spectrophotometric investigation of the interactions between cationic (C.I. Basic Blue 9) and anionic (C.I. Acid Blue 25) dyes in adsorption onto extracted cellulose from Posidonia oceanic in single and binary system[END_REF][START_REF] Boubakri | Nanoscale zero-valent iron functionalized Posidonia Oceanica marine biomass for heavy metal removal from water[END_REF][START_REF] Elmorsi | Adsorption of methylene blue and Pb 2+ by using acid-activated Posidonia Oceanica waste[END_REF]. The main constituents of Posidonia Oceanica balls are cellulosic substances (cellulose and hemicellulose, 62%) together with a relatively high content of lignin (27%) [START_REF] Maisano | Syngas production by BFB gasification: Experimental comparison of different biomasses[END_REF]. Herein, we have developed efficient bio-adsorbent materials using Posidonia Oceanica balls to extract OTC antibiotics from water. This topic has previously been addressed in an investigation of the adsorption of tetracycline antibiotic onto Posidonia bio-adsorbent focusing on the relationships between the processing parameters and the adsorption behavior using a neural network approach [START_REF] Donut | Artificial neural network modeling of tetracycline biosorption by pre-treated Posidonia Oceanica[END_REF]. The present work addresses the characterization of the Posidonia bio-adsorbent and physicochemical mechanisms of OTC adsorption through a thermodynamic study. The kinetics of adsorption was assessed as it is of high relevance with regards to water treatment process.

Materials and Methods

Reagents and chemicals

Oxytetracycline (OTC) was supplied by Sigma-Aldrich. All chemicals and solvents used were of analytical grade.

All solutions were made with Milli-Q water of 18 M•cm resistivity.

Characterization methods

IR spectra were recorded with a Bruker IFS 55 Equinox FTIR spectrometer in ATR mode. CP MAS 13 C NMR spectra of Posidonia biomaterials were run on a Bruker Avance III 500 ultra-shield PLUS spectrometer. The thermal stability of all the prepared Posidonia biomaterials was studied by thermogravimetric analyses (TGA) carried out on a TG209F1 Netzsch instrument. The analysis was performed in the temperature range of 25-1000 °C at a rate of 10°C•min -1 under a dynamic atmosphere of nitrogen. Zeta potentials were measured by electrophoresis with Malvern Zetasizer Nano ZS, with 0.05 wt% aqueous suspensions at different pH values. The  potential was calculated from the electrophoretic mobility under the Smoluchowski approximation. The ultraviolet-visible (UVvis) spectrophotometer (Varian Cary 50 type) was employed for the measurement of absorbance of OTC solutions.

Optical microscopy pictures of Posidonia biomaterials dispersions were taken with a Leica DMLM microscope.

A drop of the aqueous dispersion was observed in transmission mode between glass slide and cover slip at magnifications of the objective ranging from ×10 to ×100.

Preparation of Posidonia biomaterials

Posidonia Oceanica balls were collected from the Cheba-Mahdia beach at the east coast of Tunisia. The fibers of biomass balls have been manually separated, extensively washed with large volumes of distilled water to remove sand and salt coming from sea water, and then dried in the open air. The obtained Posidonia fibers were washed in a Soxhlet extractor with ethanol during 24 h and dried in an oven at 50 °C for 48 h, until the mass of the fibers stayed constant. The dry biomass materials were crushed, sieved in order to recover particles of homogeneous size (100, 75 and 50 μm), washed several times with distilled water, and oven dried for 24 h at 50-60 °C. After that, the fibers and crushed Posidonia were stored in a desiccator for further use. The prepared fiber and powder materials and the corresponding abbreviations as used throughout the paper are listed in Table 1.

Table 1. List of the studied materials with their abbreviations.

Bio-materials Abbreviations

Posidonia fiber POS-fiber Posidonia powder (medium width 100 μm) POS-100 Posidonia powder (medium width 75 μm) POS-75 Posidonia powder (medium width 50 μm) POS-50

Characterization of raw materials

The elemental and moisture content analysis of dry Posidonia Oceanica fibers were determined. Elemental content of carbon, sulfur, nitrogen and hydrogen were determined using a Perkin Elmer type series II analyzer 2400.

Posidonia Oceanica raw material has contents of C = 43.65%, S = 2.73%, N = 1.19% and H = 6.12%, which are similar to those previously reported in case of other Posidonia raw materials (Zaafouria et al. 2016). The percentage moisture content was calculated by the difference between wet mass and dry mass of 2 g of Posidonia fibers using a muffle oven at 105 °C until the mass of dried matter became constant. The moisture content was 9.53%.

Surface characterization of Posidonia functional groups

Acidic functions of POS-50 were characterized by acid-base titrations using the Boehm method [START_REF] Boehm | Surface oxides on carbon and their analysis: a critical assessment[END_REF].

First, aqueous solutions of NaHCO3 (0.02 mol•L -1 ), Na2CO3 (0.02 mol•L -1 ) and NaOH (0.02 mol•L -1 ) were freshly prepared. Then, 0.3 g of POS-50 was added to 20 mL of each base prepared solution. The samples were stirred for 24 h (400 rpm, room temperature), centrifuged and the base excess was titrated with 0.02 M HCl. The amount of acidic groups on the POS-50 surface particle was calculated on the assumptions that: NaOH neutralizes carboxylic, lactonic, and phenolic groups, Na2CO3 neutralizes carboxylic and lactonic groups and NaHCO3 neutralizes only carboxylic groups. The number of surface basic sites was calculated from the amount of HCl that reacted with the deprotonated functional surface of POS-50. The titrations were repeated three times.

Binding experiments

Calibration curve of UV-vis absorbance

The concentrations of OTC standard solutions were prepared by appropriate dilution in water of the mother solution at 10 -4 mol•L -1 stored at 4 °C. The concentrations of the solutions ranged between 175 and 20 µmol•L -1 .

Their absorbance at 352 nm wavelength was linear with respect to the concentration.

Effect of adsorbent mass

The tests were conducted by stirring 10 mL of 80 mg L -1 OTC solutions, with different masses of Posidonia biomaterials (POS-50, POS-75, POS-100 and POS-fiber) at 25 °C and pH 6.0. The mixture of each sample was centrifuged and the residual concentration of OTC in the supernatant was determined by absorbance measurements at the appropriate wavelength (λmax = 352 nm).

Adsorption experiments

All adsorption measurements were performed by the depletion method in water since real environmental samples were essentially aqueous media. For equilibrium adsorption, the biomaterial (80 mg) was immersed in 10 mL of water containing OTC with various concentrations ranging from 20 to 175 μmol•L -1 and shaken at 380 rpm constant shaking rate at constant temperature in thermostatic water bath. The initial pH of both OTC solutions and Posidonia materials was maintained at a fixed value 2, 4.5, 6 or 8 using 1 M HCl or 0.1 M NaOH solutions. The mixtures were stirred for different contact times t, and then centrifuged at 5000 rpm for 10 min. The residual concentration of OTC (Ce, mol•L -1 ) in the supernatant was determined by UV-vis absorbance analysis (λmax = 352 nm).

The dynamic adsorption capacities (Qe, mol•g -1 ) and adsorption percentage (%A, %) of OTC were calculated according to the following equations.

𝑄𝑒 = 𝑉 𝑚 (𝐶 0 -𝐶𝑒) (Eq 1) %𝐴 = (𝐶 0 -𝐶𝑒) 100 𝐶 0 (Eq 2)
where C0 and Ce respectively are the initial and the residual concentrations of OTC, V is the volume of the OTC solution, m is the mass of Posidonia biomaterials. The experiments were performed at 298 K unless otherwise indicated.

Results and discussion

Physicochemical characterization of Posidonia

The contents of carbon, hydrogen, nitrogen and sulfur, the surface functional characterization and point of zero charge of POS-50 are given in Table 2. According to such analyses, the major elements of POS-50 were carbon and hydrogen, which are the basic elements of cellulose, hemicellulose and lignin [START_REF] Meseguer | Biosorption of cadmium(II) from aqueous solutions by natural and modified non-living leaves of Posidonia Oceanica[END_REF]. The percentage of carbon and hydrogen were similar to those previously observed in the case of other cellulosic materials such as, cherry stones [START_REF] Nowicki | Comparison of physicochemical and sorption properties of activated carbons prepared by physical and chemical activation of cherry stones[END_REF], olive seed [START_REF] Stavropoulos | Production and characterization of activated carbons from olive-seed waste residue[END_REF] and vetiver roots [START_REF] Gaspard | Activated carbon from vetiver roots: gas and liquid adsorption studies[END_REF]), which have elemental contents of C = 46-49% and H = 5.7-6.0%. The Boehm titration method was applied to identify and quantify the surface functions of POS-50. They are split into three types: acidic, basic, or neutral. The main acidic groups on Posidonia surface are carboxylic, lactonic and phenolic groups [START_REF] Pennesi | Removal of vanadium(III) and molybdenum(V) from wastewater using Posidonia Oceanica (Tracheophyta) biomass[END_REF][START_REF] Astudillo-Pascual | New phenolic compounds in Posidonia Oceanica seagrass: A comprehensive array using high resolution mass spectrometry[END_REF]. The heterogeneous POS-50 has a wide variety of functional surface groups that may act as adsorption sites for OTC adsorption. Table 2 summarizes the experimental surface functions determined by Boehm titration of POS-50. The surface composition of Posidonia mostly included carboxylic acidic functional groups, followed by phenolic and then lactonic groups that are the main acidic functions of lignin and hemicelluloses contained in Posidonia [START_REF] Douissa | Macroscopic and microscopic studies of methylene blue sorption onto extracted celluloses from Posidonia Oceanica[END_REF]). Infrared spectra of POS-50, POS-75, POS-100 and POS-fiber were collected in the wavenumber range 400-4000 cm -1 (Fig. 1). All biomaterials presented similar spectra. The functional groups present on the bio-adsorbent surface are essential for understanding the adsorption mechanism. The main absorption bands observed in the IR spectrum of POS-50 were those of cellulose, hemicellulose and lignin, which are characterized by the presence of carbonyl, hydroxyl and methoxy functional groups. The broad band in the range 3700-3000 cm -1 (with maximum absorption at 3334 cm -1 ) showed the existence of -OH and -NH vibrations [START_REF] Tarchoun | Microcrystalline cellulose from Posidonia Oceanica brown algae: Extraction and characterization[END_REF]. The two small bands located at 2971 and 2886 cm -1 are due to asymmetric and symmetrical C-H stretching vibrations attributed to alkyl groups respectively. The band at 1617 cm -1 was assigned to amide C(O)NH2 bond and the one at of POS-50 is 41%. In the crystalline phase, the cellulose fibers are ordered by inter-and intramolecular hydrogen bonds, on the other hand in the non-crystalline phase, the network does not have an organized structure [START_REF] Wohlert | Cellulose and the role of hydrogen bonds: not in charge of everything[END_REF]. The only signal that could be assigned to lignin was that belonging to the methoxy group of the aromatic moieties at 56 ppm. In addition, the region between 106 and 180 ppm was specific for the aromatic carbons of lignin. The adsorption of OTC was studied by the depletion method. Ionization behaviors have a significant influence on the adsorption of OTC on bio-adsorbents. Indeed, the OTC is a complex organic compound having particular chemical characteristics and behaviors with several ionizable functional groups. Oxytetracycline has three pKa and hence can exist as cationic, zwitterionic or anionic species, under acidic, neutral and alkaline conditions, they respectively [START_REF] Prarat | Amino-functionalized mesoporous silica-magnetic graphene oxide nanocomposites as water-dispersible adsorbents for the removal of the oxytetracycline antibiotic from aqueous solutions: adsorption performance, effects of coexisting ions, and natural organic matter[END_REF], as show in Fig. 4. OTC adsorption to Posidonia biomaterial and other sorbents is expected to be considerably influenced by its ionization behavior [START_REF] Aghababaei | Optimized removal of Oxytetracycline and cadmium from contaminated waters using chemically-activated and pyrolyzed biochars from forest and wood-processing residues[END_REF]. Aqueous speciation of OTC was also considered following the reactions below:

OTCT  OTCH 3 + + OTCH 2 0 + OTCH -+ OTC 2- (Eq 3) OTCH 3 +  OTCH 2 0 + H + (Eq 4) OTCH 2 0  OTCH -+ H + (Eq 5) OTCH - OTC 2-+ H + (Eq 6)
The OTCT in the reactions represents all possible solutions species for OTC. The pKa values (Fig. 4) were taken from the literature [START_REF] Punamiya | Effectiveness of aluminum-based drinking water treatment residuals as a novel sorbent to remove tetracyclines from aqueous medium[END_REF]. The pH is a very important parameter in the adsorption process because it strongly influences the surface charge of the adsorbent and the ionic form of the adsorbates (Fig. 5), which both affect the adsorption behavior. To elucidate the role of surface charge of the adsorbent in the adsorption of OTC molecules, the point of zero charge (pHPZC) of Posidonia was determined. This corresponds to the pH value of the medium for which the positive and negative charges are balanced, so that the overall surface charge is zero. The pHPZC is important in adsorption phenomena, especially when electrostatic interactions are involved, which presently is the case. It was determined by zeta potential measurements in aqueous suspension of POS-50 of variable pH values between 2 and 10 set by the addition of 0.1 M NaOH or HCl solution. The suspensions must be kept under constant agitation at ambient temperature for 4 h to equilibrate the final pH. The pHPZC of POS-50 was close to pH 2 (Fig. 5). Therefore, the overall surface charge was negative above pH 2. This result was expected since the POS-50 material mostly contains polar functions such as phenolic and carboxylic groups whose ionization yields negatively charged groups. Upon increasing the pH, the zeta-potential decreased from -2 mV to -18 mV at pH 10.

Performance for adsorption of oxytetracycline

Effect of adsorbent type and mass

The influence of adsorbent mass has been studied in the range 0.020-0.100 g. The histogram in Fig. 7 shows that POS-50 was more efficient at adsorbing OTC and that maximum adsorption of 86% was reached for the masses of POS-50 of 0.08 g and above. The efficiency of POS-50 was significantly higher than other samples that could uptake a maximum of OTC antibiotics in the range 45-75%. This optimum mass of POS-50 corresponds to the specific conditions of this series of experiments with a fixed OTC concentration of 80 mg L -1 and a volume of aqueous solution of mL. The amount of adsorbent dispersed in the solution is to be set with regards to the amount of OTC molecules to be uptaken so as to ensure an equivalent number of adsorption sites. Beyond a certain mass of bio-adsorbent, the adsorption rate slightly decreased, indicating that supplementary phenomena detrimental to adsorption were operating. A possible origin of this phenomenon is the poor dispersion of POS-50 at too high concentrations. Indeed, aggregation of Posidonia fibers lowers the accessibility to the fibers surface and prevents OTC from reaching adsorption sites. Therefore, there is an optimum concentration of bio-adsorbent, which avoids such an ineffective overdose. In the further study aiming at determining the adsorption capacities by saturating all sites, adsorbent masses of 0.08 g of POS-50 were chosen.

Effect of pH on oxytetracycline adsorption

Adsorption isotherms represent the thermodynamic equilibrium between adsorbed and free molecules. They 1918). The Langmuir theory describes monolayer adsorption of adsorbate molecules on a homogeneous surface having a well-defined density of active sites, all sites being identical and independent [START_REF] Liu | Application of nanotechnology in the removal of heavy metal from water[END_REF]). The bi-Langmuir isotherm model considers the presence of two types of adsorption sites (site 1 and site 2) with different densities and affinities for adsorbing molecules [START_REF] Fornstedt | Modeling of preparative liquid chromatography[END_REF]. This model also assumes, as in the case of the Langmuir model, that adsorptions events are localized at the two well-defined specific sites. The bi-Langmuir model is written as the sum of two Langmuir isotherms for the two types of surface sites:

𝑄 𝑒 = 𝑄 e1 + 𝑄 e2 = 𝑄 𝑚𝑎𝑥,1 𝐾 𝑎1 𝐶 𝑒 1+𝐾 𝑎1 𝐶 𝑒 + 𝑄 𝑚𝑎𝑥,2 𝐾 𝑎2 𝐶 𝑒 1+𝐾 𝑎2 𝐶 𝑒 (Eq 7)
where Qe1 and Qe2 are the adsorbed quantities at equilibrium on the two types of adsorption sites, Qmax,1 and Qmax,2 are the densities of sites 1 and 2, and Ka1 and Ka2 are the binding constants of adsorption on site 1 and 2. The density of sites Qmax,1 and Qmax,2 are also their maximum adsorption capacity. The units of concentration are mg•L -1 , which means that the standard state is an ideal solution of concentration 1 mg•L -1 . The variations of thermodynamic parameters with respect to pH are presented in Fig. 8. It can be seen from Fig. 8 that bi-Langmuir model is suitable for describing the adsorption process of OTC onto POS-50 bio-adsorbent. This result is based by minimizing the average relative error (ARE, Eq 8, Table 4) by non-linear regression to experimental data, allowing the determination of the binding constants Ka1 and Ka2 and adsorbed amounts at full coverage Qmax,1 and Qmax,2 for the two localized sites of adsorption. Kai values for sites 1 and 2 helps at ascribing the nature of these sites. Sites 1 contain the most acidic functions revealed by the Boehm titration method, namely carboxylic acids. Conversely, sites 2 contain weaker acidic phenolic groups. On this basis, sites 1 are belonging to cellulose and hemicellulose whereas sites 2 are belonging to lignin. The predominant non-electrostatic interactions are presumed of two types: hydrogen bonds between the hydroxyls of cellulosic materials and carbonyl groups of OTC for sites 1, and - stacking interactions between the aromatic rings of lignin and OTC for sites 2. Such assignment of sites 1 to cellulose and sites 2 to lignin is in agreement with the values of the densities of adsorption sites with Q1,max > Q2,max. Indeed, Posidonia is richer in cellulosic materials than in lignin.

Enthalpic and entropic contributions to the standard free energy of adsorption

The thermodynamic study reflects the feasibility and spontaneous nature of the adsorption process. The thermodynamic parameters of adsorption at pH 6.0 and different temperatures (298 K, 303 K, 313 K and 323 K) such as standard Gibbs free energy ΔadsG 0 , standard enthalpy ΔadsH 0 and standard entropy ΔadsS 0 were estimated from Qi,max and Kai parameters from the Gibbs and van't Hoff equations for both binding sites (i = 1 or 2):

∆ ads 𝐺 𝑖 0 = -𝑅𝑇 ln(𝐾 𝑎𝑖 ) (Eq 9)

∆ ads 𝐺 𝑖 0 = ∆ ads 𝐻 𝑖 0 -𝑇∆ ads 𝑆 𝑖 0 (Eq 10)

where R (8.314 J•mol -1 •K -1 ) is the gas constant, T is the absolute temperature, and Kai is the binding constant for either two sites adsorption.

Combination of the two equations gives the van't Hoff equation The van't Hoff plots of ln(Kai) against 1/T (Fig. 9a) for the two types of sites were linear with slope ΔadsH 0 /R and y-intercept ΔadsS 0 /R. Linear behavior was showing that the values of ΔadsH 0 and ΔadsS 0 did not significantly vary in the studied temperature range (Table 5). Table 5. Standard adsorption enthalpy and entropy, ΔadsH 0 and ΔadsS 0 , for the two-sites adsorption of OTC to POS-50 at pH 6.0 and ΔadsG 0 at 298 K.

ΔadsH 0 (kJ•mol -1 ) ΔadsS 0 (J•mol -1 •K -1 ) ΔadsG 0 at 298 K (kJ•mol -1 ) Site 1 Site 2 26.5 126.9

337.8 0.50 127.2 127.0

The standard enthalpy of adsorption onto POS-50 was strongly negative for both adsorption sites. The enthalpic contribution to the standard Gibbs free energy mainly comes from hydrogen bonding between hydroxy and carboxy functional surface groups of POS-50 and OTC molecules. Upon adsorption, these hydrogen bonds formed induce at the same time the broken of hydrogen bonds between water and both OTC. ΔadsH 0 is the balance of all these processes. The exothermic balance for adsorption to POS-50 reveals that hydrogen bonds between OTC and surface hydroxyl are stronger. This is the result of POS-50 hydroxyl groups interacting more favorably with OTC.

ΔadsS 0 is positive for both the two sites adsorption processes. Thus, ΔadsH 0 = -26.5 kJ•mol -1 and ΔadsS 0 = 337.8 J•mol -1 •K -1 for the adsorption site onto POS-50; and ΔadsH 0 = -126.8 kJ•mol -1 and ΔadsS 0 = 0.5 J•mol -1 •K -1 for the site adsorption off the biomaterial. For both sites, the entropic contribution (-T ΔadsS 0 ) to the standard Gibbs free energy is lower than the enthalpic contribution, so that ΔadsG 0 assumes a negative value.

The standard enthalpy of site 2 adsorption off phenolic sites was strongly negative. Such an exothermic adsorption process suggests the formation of strong hydrogen bonds between OTC and phenolic groups. The site 1 adsorption onto POS-50 material is much less exothermic. The hydrogen bonds between OTC and the primary hydroxyl groups of monosaccharides are expected to be weaker in the adsorption process at Site 1. In addition, this decrease in the exothermic process results from compensation of the exo-and endothermic processes, to know the adsorption of one OTC molecule results in the release of many water molecules, so that the net balance is an increase of the number of free molecules. However, although the OTC molecules adsorbed off the adsorption sites are non-located and mobile, the adsorption to biomass material is localized. As a result, the entropy for adsorption off POS-50 is higher.

Kinetics of adsorption

In applications to analysis such as liquid chromatographic separations and sample pre-concentration in solid phase extraction devices (SPME), the kinetics of adsorption is extremely important. Fast adsorption provides for a high flow rate and a fast analysis time. Pre-concentration using SPME necessitates that almost all of the analyte be absorbed during the residence time in the SPME cartridge. The influence of contact time on OTC adsorption onto POS-50, POS-75, POS-100 and POS-fiber at different concentrations of OTC (from 5 10 -5 to 10 -4 mol•L -1 ) was studied using the depletion method (Fig. 10). The adsorption of OTC onto POS-50 material was much larger than onto others tested materials during the adsorption equilibration time. At all tested OTC concentrations, binding to Posidonia biomaterials were quite fast processes. Adsorption equilibrium was reached within the first few minutes.

90 % uptake of OTC onto POS-50 occurred within 10 min. A typical time scale taken from the scarce experimental data is about 15 min using activated in alkaline medium and functionalized Posidonia materials [START_REF] Boubakri | Nanoscale zero-valent iron functionalized Posidonia Oceanica marine biomass for heavy metal removal from water[END_REF]. Theoretical studies were established to explain the nature of adsorption.

The nonlinear forms of the pseudo-first order model and pseudo-second order:

𝑄 𝑡 = 𝑄 𝑒 -𝑄 𝑒 𝑒 -𝑘 1 𝑡 (Eq 12) 𝑄 𝑡 = 𝑘 2 𝑄 𝑒 2 𝑡 1+𝑘 2 𝑄 𝑒 𝑡 (Eq 13)
where k1 (min -1 ) et k2 (mg•g -1 •min -1 ) are the pseudo-first order and pseudo-second order kinetic constants, respectively. Qe and Qt are the quantities of OTC (mg•g -1 ) adsorbed at equilibrium and at time t.

In order to determine the model of the adsorption kinetics, it is required to compare the value of Qe calculated by the theoretical equation with that of the experimental value [START_REF] Lin | Comparison between linear and non-linear forms of pseudo-first-order and pseudo-secondorder adsorption kinetic models for the removal of methylene blue by activated carbon[END_REF].

Comparative study

The adsorption capacities and the equilibrium time of Posidonia biomaterial with respect to OTC have been compared to some recently reported sorbents. The adsorption capacity of Posidonia is comparable to that of the majority of these adsorbents, which are therefore suitable for the removal of OTC from wastewater [START_REF] Harja | Studies on adsorption of oxytetracycline from aqueous solutions onto hydroxyapatite[END_REF][START_REF] Minale | Enhanced removal of oxytetracycline antibiotics from water using manganese dioxide impregnated hydrogel composite: Adsorption behavior and oxidative degradation pathways[END_REF][START_REF] Pham | Adsorption characteristics of molecular oxytetracycline onto alumina particles: The role of surface modification with an anionic surfactant[END_REF][START_REF] Wu | Performance of bimetallic nanoscale zero-valent iron particles for removal of oxytetracycline[END_REF]. Considering the difference in physical properties of adsorbents and experimental conditions, an accurate evaluation using adsorption capacity and contact time data is quite difficult to make, although our data still provide useful information at least on the order of magnitude. Finally, due to the relatively low raw material cost and fast adsorption time, Posidonia particles have the potential to be cost effective adsorbents for the removal of OTC from aqueous solutions and a good candidate towards the environment.

Conclusion

Results highlighted that the Posidonia biomaterial exhibit a good ability and efficient uptake of oxytetracycline antibiotics from aqueous solutions, due to the fact that Posidonia has more than 80% organic compounds and functional surface which could be uptake sites. Different adsorption process, such as solution pH, contact time, initial OTC concentration, and temperature have been studied and optimized. The optimal removal occurred at pH 6.0. A correct thermodynamic approach taking into account the presence of two types of adsorption sites has been applied using the bi-Langmuir adsorption isotherm better than the simpler Langmuir isotherm that considers a localized adsorption on one single type of site. The thermodynamic study under variation of the temperature shows that interactions are of entropic nature, which is expected for a cation exchange phenomenon driven by electrostatic interactions. The kinetic equilibrium was rapidly established in about 10 min. The quite fast kinetics of adsorption makes the POS-50 a sorbent material able to extract a high capacity of OTC from aqueous media in the framework of an application to SPME. The experimental data were closely fitted to the pseudo-second-order model, suggesting that chemisorption is predominant. These promising results show the successful use of native Posidonia as an adsorbent medium to remove organic micro-contaminants from wastewater. It is inexpensive and can also contribute to a circular economy as it is made of pellets washed up on sea beaches. The results could be useful to implement the large-scale use of Posidonia as material adsorbing organic pollutants in the treatment of contaminated water.

Statements and Declarations -Ethical Approval:

Not applicable -Consent to Participate: Not applicable -Consent to Publish:

Not applicable -Funding: The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

-Competing Interests: All the authors (Karima Ferchichi, Noureddine Amdouni, Yves Chevalier and Souhaira Hbaieb) declare that they have no known competing financial or no financial interests or personal relationships which have or could be perceived to have influenced the work reported in this article.

-Author contributions: All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Karima Ferchichi, Noureddine Amdouni, Yves Chevalier and Souhaira Hbaieb. The first draft of the manuscript was written by [Karima Ferchichi] and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

-Availability of data and materials: All authors declare that all data and materials of their published claims comply with field standards.

  1425 cm -1 corresponded to the deformation vibration of -C-OH with contribution from the symmetrical stretching vibration O-C-O of the carboxylate group[START_REF] Radhakrishnan | Fabrication of 3D printed antimicrobial polycaprolactone scaffolds for tissue engineering applications[END_REF]). Particularly, this band at 1425 cm -1 is also known as the crystalline band. The band located at 1254 cm -1 was attributed to the O-C-O segment of the ester group. Finally, the band at 1019 cm -1 was assigned to alcoholic groups[START_REF] El Achaby | New highly hydrated cellulose microfibrils with a tendril helical morphology extracted from agro-waste material: application to removal of dyes from waste water[END_REF]).

Figure 1 .

 1 Figure 1. FTIR spectra of POS-50, POS-75, POS-100 and POS-fiber biomaterials.

Figure 2 .

 2 Figure 2. 13 C CP MAS NMR spectrum of POS-50.The investigation of the thermal properties of Posidonia biomaterials is essential for its applications. The TGA curves of POS-fiber, POS-100, POS-75 and POS-50 are shown in Fig.3. Table3reports the results of thermal analyses. The degradation process of these biomaterials took place in three stages. The first mass loss in the temperature range of approximately 20 to 150 °C was caused by the evaporation of moisture[START_REF] Tarchoun | Microcrystalline cellulose from Posidonia Oceanica brown algae: Extraction and characterization[END_REF]). The second mass loss in the range 230-360 °C was attributed to the preponderant process of decomposition of the carbohydrate phase of Posidonia made of hemicellulose (the most thermally unstable compound) and cellulose (e.g. dehydration, depolymerization, decarboxylation, and decomposition of glycosyl units). The third stage appearing in the range 375-1000 °C corresponded to char combustion and the inorganic-mineral decomposition[START_REF] Haddar | Synergetic effect of Posidonia Oceanica fibres and deinking paper sludge on the thermo-mechanical properties of high density polyethylene composites[END_REF]. According to the results described in previous reports[START_REF] Plis | Combustion performance evaluation of Posidonia Oceanica using TGA and bubbling fluidized-bed combustor (batch reactor)[END_REF], the main gases produced during the process and detected by MS and FTIR spectrometers are CH4, CO, H2O, light hydrocarbons (C2H4, C2H6, C3H6) and CO2. These gases reach their maximum yields in the temperature range of 230 to 530 °C. At higher temperatures, all gases are oxidized to CO2[START_REF] Plis | Thermo-chemical properties of biomass from Posidonia Oceanica[END_REF]. It is clear that the thermal behavior of the Posidonia is improved by decreasing its size throughout the temperature range studied. Indeed, the kinetics of degradation were slower for smaller sizes.

Figure 3 .

 3 Figure 3. Thermogravimetric analysis of POS-50, POS-75, POS-100 and POS-fiber biomaterials.

Figure 4 .

 4 Figure 4. Structure and pH-dependent surface speciation of oxytetracycline. The fractions of each ionic species are calculated using the log(Ka) values of OTC, where OTCH3 + , OTCH 2 0 (±), OTCH -, and OTC 2-represent the different ionic species of OTC.

Figure 5 .

 5 Figure 5. Zeta potential measurements of POS-50 at different pH.

Figure 6 .

 6 Figure 6. Optical microscopy pictures of POS-50, POS-75, POS-100 and POS-fiber in water under magnification (20).

Figure 7 .

 7 Figure 7. Effect of the mass of Posidonia biomaterials on adsorption of OTC from its aqueous solution. Solution volume = 10 mL; Concentration = 80 mg•L -1 ; contact time = 20 min; and temperature = 298 K.

  have been measured for adsorption to POS-50 after an equilibration time of 20 min. The bi-Langmuir theoretical adsorption model was fitted to the experimental data to infer the adsorption parameters of OTC onto POS-50 biomaterial at different pH. The most commonly used model of adsorption is the Langmuir model (Langmuir

  the number of data points and p the number of adjustable parameters.The excellent fit of the bi-Langmuir adsorption model to the experimental adsorption isotherms of the POS-50 at several pH definitely showed the presence of two types of adsorption sites within the bio-adsorbent, with different affinities toward target compounds. Such dual adsorption is obviously related to the chemical composition of Posidonia containing cellulose, hemicellulose and lignin that are monosaccharides and phenolic materials. The obtained parameters Q1,max and Q2,max for both active sites (Table4) remained at constant values in acidic and basic media because the number of sites in POS-50 is related to the chemical composition of Posidonia. On the contrary, the values of Kai varied with respect to pH because interactions with OTC depend on the ionic state of functional groups of the adsorption sites. It should be noted that Kai values were higher in slightly acidic media where OTC is under its protonated cationic or neutral forms. In basic medium (pH 8.0), both the Posidonia surface and the OTC molecules are strongly negatively charged. Strong electrostatic repulsions prevent adsorption, which is revealed by the low values of Kai for both types of sites. Electrostatic interactions are favoring adsorption in cases of opposite charges of Posidonia and OTC. Such effect vanishes in acidic medium when the pH reaches the pHPZC of Posidonia at pH 2. The electrostatic binding process is based on a cation exchange of OTC for sodium. Possible higher affinity of OTC than sodium might result from its more hydrophobic nature or hydrogen bonding interactions. The pH dependence of adsorption to sites 1 show such an characteristic effect of electrostatic interactions with a low affinity (small Ka1) at pH 2 because of lack of negative charge on Posidonia and at pH 8 because of strong electrostatic repulsions, and maximum affinity at intermediate pH. On the contrary, adsorption to sites 2 does not have such a strong dependence on pH, which reveals a lesser influence of electrostatic phenomena and a larger relative contribution of the types of interactions. Such characteristic pH dependence of

Figure 8 .

 8 Figure 8. The fit of the bi-Langmuir model to adsorption isotherms of OTC onto POS-50 at various pH at 298 K.

Figure 9 .

 9 Figure 9. (a): Adsorption isotherms and bi-Langmuir non-linear fit to the adsorption data of OTC onto POS-50 biomaterial at different temperatures. (b): van't Hoff plot of the OTC binding constant onto POS-50 biomaterial against inverse temperature (green dots: site 1 and red dots: site 2).

  concentrations calculated by the equation of the pseudo-second order model are close to the values measured experimentally. It can be also seen that increasing the initial OTC concentration results in an increase in the adsorption capacity but the rate constant remains constant. The initial number of sites being the same, the competition on these sites becomes more and more important as the concentration of OTC increases. In addition, the average relative error (ARE, Eq 8) of the pseudo-second order model are small and lower than those obtained with the pseudo-first order model. At the same time, Fig.10clearly shows that the pseudo-second order kinetic model fits perfectly to the experimental data. According to comparable instances reported in the literature on various types of pollutants (organic and inorganic substances), the pseudo-second order kinetic model has commonly been used to describe adsorption processes[START_REF] Febrianto | Equilibrium and kinetic studies in adsorption of heavy metals using biosorbent: A summary of recent studies[END_REF][START_REF] Anirudhan | Heavy metals uptake from aqueous solutions and industrial wastewaters by humic acid-immobilized polymer/bentonite composite: Kinetics and equilibrium modeling[END_REF][START_REF] Bhatnagar | Utilization of agro-industrial and municipal waste materials as potential adsorbents for water treatment-A review[END_REF][START_REF] Miranda | Preparation and evaluation of hydrotalcite-iron oxide magnetic organocomposite intercalated with surfactants for cationic methylene blue dye removal[END_REF]).

Figure 10 .

 10 Figure 10. Experimental data of adsorption kinetics and nonlinear fits of the pseudo-first-order (red dashed lines) and pseudo-second-order (red solid lines) models for corresponding adsorption of OTC to (a): POS-75, POS-100 and POS-fiber at 20 mg•L -1 and (b): POS-50 at initial concentration 20 mg•L -1 , 50 mg•L -1 and 80 mg•L -1 .

Table 2 .

 2 pHPZC value and Boehm titration results of POS-50.

	pHPZC		Elemental composition (%)		Surface functional groups (mmol g -1 )
	2.11	C 39.75	H 5.57	N 0.91	S 2.53	Carboxylic 0.797	Phenolic 0.127	Lactonic 0.009

Table 3 .

 3 Mass losses from TGA of POS-50, POS-75, POS-100 and POS-fiber biomaterials.

	Bio-materials	1 st mass loss (%) (20-150 °C)	2 nd mass loss (%) (230-360 °C)	3 rd mass loss (%) (375-1000 °C)
	POS-fiber	10.0	49.3	31.8
	POS-100	10.0	44.8	21.5
	POS-75	9.2	45.2	19.4
	POS-50	9.4	43.3	18.8

Table 4 .

 4 Parameters of the fits of the bi-Langmuir model to experimental adsorption data of oxytetracycline onto POS-50 material at different pH.

	pH	Qmax,1 (µmol•g -1 )	Ka1	log(Ka1)	Qmax,2 (µmol•g -1 )	Ka2	log(Ka2)	ARE
	2.0	11.2	13147	9.4	4.5	26174	10.1	0.012
	4.5	11.5	19444	9.8	4.4	19851	9.8	0.053
	6.0	11.8	40156	10.6	4.4	41097	10.6	0.055
	8.0	11.0	6843	8.8	4.1	672	6.5	0.045

  Table 6 groups the coefficients of the equations obtained by considering a pseudo-first order or pseudo-second order kinetics for Posidonia biomaterials. It can be seen from this table that the values of the quantities adsorbed at equilibrium for all

Table 6 .

 6 Kinetic parameters of the pseudo-first order and pseudo-second order models of the adsorption study of OTC onto POS-50, POS-75, POS-100 and POS-fiber biomaterials.

	Posidonia	C0	Qe,exp	Pseudo-first-order model	Pseudo-second-order model
	biomaterials	(mg•L -1 )	(mg•g -1 )	k1 (min -1 )	Qe,calc (mg•g -1 )	ARE	k2 (g•mg -1 •min -1 )	Qe,calc (mg•g -1 )	ARE
		20	2.32	1.75	2.22	0.107	0.49	2.33	0.020
	POS-50	50	5.63	1.76	5.32	0.162	0.50	5.58	0.047
		80	8.64	1.70	8.18	0.164	0.50	8.59	0.031
	POS-75	80	7.04	1.42	6.85	0.060	0.40	7.00	0.031
	POS-100	80	6.05	1.45	5.97	0.039	0.43	6.06	0.011
	POS-fiber	80	5.63	1.45	5.39	0.097	0.49	5.57	0.048

Acknowledgments

This work was supported by the Cross-border project Italy-Tunisia "Méthodologies d'Économie Durable pour les Déchets Côtiers Utilisables des Plages" (MEDDé.Co.U.Plages IS_3.2_086).