Experimental evidence of the potential bioavailability for marine heterotrophic bacteria of aerosols organic matter

Aix-Marseille Univ., Université de Toulon, CNRS, IRD, MIO UM 110, 13288, Marseille, France 2 Molecular and Cellular Biology, The University of Arizona, Tucson, USA 3 IRA (Institut des Régions Arides) de Médenine, El Fjé4119, Tunisia 4 iEES Paris (Institut d’Ecologie et des Sciences de l’Environnement de Paris), UMR IRD 242, Université Paris Est 10 Créteil—Sorbonne Université—CNRS—INRA—Université de Paris, F-93143 Bondy, France 5 LISA, UMR7583, Université de Paris, Université Paris-Est-Créteil, Institut Pierre Simon Laplace (IPSL), Créteil, France. Correspondence to: kdjaoudi@email.arizona.edu 15


Introduction
Marine dissolved organic matter (DOM) is the largest reservoir of reduced carbon in the ocean. Estimated at 662 Pg C, which is comparable to that present as atmospheric CO2, DOM plays a key role in the ocean carbon cycle as it 60 is an important pathway of carbon export (Hansell et al., 2009;Moran et al., 2016). At the global scale, dissolved organic carbon (DOC) export from the surface to the deep ocean contributes to 20% of the total organic carbon flux (Hansell et al., 2009). This percentage reaches more than 50% of the total carbon export in the oligotrophic oceans (Carlson et al., 1994;Guyennon et al., 2015;Letscher and Moore, 2015;Roschan and DeVeries, 2017).
Nutrient availability and microbial community structure regulate the accumulation and the remineralization of 65 DOM, influencing thus the DOC export efficiency (Carlson et al., 2002;Letscher and Moore., 2015;Romera-Castillo et al., 2016). From extensive field studies, it is well known that DOM flux into heterotrophic bacteria is a major pathway in the regulation of carbon fluxes in the ocean (i.e. Azam et al., 1983;Moran et al., 2016). Heterotrophic bacteria are an especially important component of marine oligotrophic regions in which their biomass is comparable to that of phytoplankton. In such oligotrophic areas, half of oceanic primary production is channeled via heterotrophic 70 bacteria to the microbial loop (Fuhrman, 1992;Azam, 1998), driving a wide range of biogeochemical processes that are important for the carbon cycle (Bunse and Pinhassi, 2017;Gasol and Kirchman, 2018 and references therein).
Among these processes, the microbial activity has been identified as involved in the alteration of the chemical composition of the DOM pool, influencing thereby the residence time of the carbon in the ocean (Microbial carbon pump, Jiao et al., 2010).

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The open ocean receives from the atmosphere a continuous flux of anthropogenic particles, resulting from both industrial and agricultural activities, as well as pulsed fluxes of natural origin such as desert dust (De Leeuw et al., 2014 and references therein). During their transport to the ocean, dust particles mix with anthropogenic aerosols/gas supplying the water column with a wide variety of compounds including macro-and micro-nutrients (N, P, Fe…) (Duce et al., 1991;Jickells et al., 2005), as well as potentially toxic elements (Paytan et al., 2009;Jordi et al., 80 2012). By bringing new nutrients to the upper waters, atmospheric deposition plays a key role in the stratified oligotrophic regions (Guieu et al., 2014). The relative response of phytoplankton and heterotrophic bacteria to dust deposition has been shown to depend on the nutritional status of the environment in which they develop. Indeed, the reported positive effect of dust deposition on the primary production in the central Atlantic Ocean decreased with increasing oligotrophy of the seawater (Maranon et al., 2010), suggesting a competitive advantage of heterotrophic 85 bacteria over phytoplankton in the oligotrophic ocean. Nevertheless, recently, the contrasted influence of Saharan dust versus anthropogenic aerosols on bacterioplankton composition and metabolism is getting attention (Herut et al., 2016;Marín et al., 2017a).
Most studies on the biogeochemical role of atmospheric deposition have focused on the potential of inorganic compounds to relieve nutrient limitation (i.e. Duce et al., 1991;Guieu et al., 2014). However, there is increasing 90 evidence that a significant fraction of atmospheric deposition occurs as organic forms (Duce et al., 2008;Kanakidou et al., 2012;Djaoudi et al., 2018;Violaki et al., 2018;Vila-Costa et al., 2019). The extent of organic compounds coating onto dust has been related, among others, to the transport pathway and the reactivity of organic species in the https://doi.org/10.5194/bg-2020-187 Preprint. Discussion started: 23 July 2020 c Author(s) 2020. CC BY 4.0 License.

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There is a paucity of information's regarding the bioavailability of atmospheric organic carbon and his fate in the ocean (Djaoudi et al., 2018). In this context, we investigate here the bioavailability to marine heterotrophic bacteria of dissolved organic carbon (DOC) leached from aerosols. For this purpose, we performed a set of in vitro biodegradation experiments in which a marine bacterial inoculum was exposed to water-soluble fractions of anthropogenic and Saharan dust aerosols, as well as to glucose-amended and non-amended (control) treatments. High volume samplers were calibrated for flow rate just before sampling. Aerosol filters were individually wrapped in a double pre-combusted aluminum foil and then stored at -20 °C until the start of the experiment.

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The content of total organic carbon (TOC) in collected aerosols was analyzed using a thermo-optical method (EC/OC analyzer, Sunset Laboratories Inc.) on the basis of EUSAAR protocol (Cavalli et al., 2010). The amount of DOC contained in the water-soluble fraction of both anthropogenic and Saharan dust aerosols was assessed by leaching 1 cm 2 of filters in 30 mL of ultrapure water. After sonication during 40 min, it was filtered through a precombusted (450 °C, 6 h) GF/F filter prior to analysis.

Experimental design
Bioassay experiments were run in triplicates (7 L each) on DOC-free artificial seawater in order to set aerosolderived DOC as the sole carbon source for marine heterotrophic bacteria. Artificial seawater was obtained by adding pre-combusted NaCl (450 °C, 6 h) in ultrapure water to get a salinity of 36 g L -1 . The DOC concentration in the artificial seawater was 6 µM. To avoid nutrient limitation, artificial seawater was enriched with nitrogen (NH4Cl + 120 NaNO3) and phosphate (KH2PO4), to final concentrations of 1 µM and 0.3 µM in the incubation bottles, respectively.
The experiment consisted of 3 treatments differing on the carbon source at a similar initial concentration.
Experimental treatments (i.e., N-and P-enriched artificial seawater) were amended with Saharan dust (D), anthropogenic aerosols (A), and glucose (G) as a proxy of bioavailable carbon source. An unamended DOC treatment (control; C) was run in parallel and consisted only on (N-and P-enriched) artificial seawater. As the amount of DOC 125 in the water-soluble fraction was lower in Saharan dust than anthropogenic aerosols (Table 1), the amount of aerosol added was set based on the C content in Saharan dust aerosols filter in order to fix a similar initial DOC concentration among all amended incubation bottles (36 µM). To do so, particles from two whole Saharan dust filters and from 7.9 https://doi.org/10.5194/bg-2020-187 Preprint. Discussion started: 23 July 2020 c Author(s) 2020. CC BY 4.0 License.
x 7.9 cm 2 of the anthropogenic aerosol filter were firstly leached, each in 650 mL ultrapure water. After being sonicated for 40 min, the suspended particles were filtered through pre-combusted GF/F filters (450 °C, 6 h) to recover the 130 dissolved fraction. A volume of 200 mL of each leachate was finally introduced in the corresponding aerosol amended treatments (D and A). The same DOC concentration (36 µM) was also set for the glucose-treatment.
A microbial inoculum was introduced in all incubation bottles. To prepare the microbial inoculum, surface seawater was collected at 5-m depth with a Niskin bottle at the MOOSE-Antares offshore station in the Mediterranean Sea (42°48′ N, 6°10′ E; Fig. 1), on board R/V Téthys II. Seawater was first filtered on board through a 40-µm mesh 135 plankton and then through 0.8-µm pre-cleaned (10% HCl and ultrapure water) polycarbonate filter to remove larger particles and plankton. Once in the laboratory, the microbial inoculum was further concentrated 30 times on a 0.2-μm pre-cleaned (10% HCl and ultrapure water) polycarbonate filter in a final volume of 180 mL. The DOC concentration in the 180-mL inoculum was 120 µM. A volume of 15 mL of the bacterial inoculum was added to each experimental bottle. This approach minimizes the volume of seawater (and therefore the amount of DOC) added to the experimental 140 bottles with the microbial inoculum (i.e. Lechtenfeld et al., 2015), allowing setting the aerosol-derived DOC as the main carbon source for heterotrophic bacteria. After dilution in the incubated volume (7 L), the contribution of marine DOC was < 0.3 µM. All experimental bottles were incubated in a controlled temperature room at 18 °C during 16 days in the dark and were regularly gently shaken.

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Subsamples were collected from the experimental bottles at 13 selected times for heterotrophic bacterial abundance (BA) and heterotrophic bacterial production (BP) and at 3 selected times for ectoenzymatic activity (EEA), dissolved organic carbon (DOC), dissolved organic nitrogen (DON) and dissolved organic phosphorus (DOP) (see Table S1 for detail of subsampling).
Samples for BA (1.8 mL) were fixed with 18 µL of a preservative solution (Glutaraldehyde 0.25% final -Pluronic 150 0.01% final), kept during 15 min at room temperature in the dark and then transferred to a -80 °C freezer until analysis, within few days. Frozen samples were thawed at room temperature and were analysed using the FACSCalibur (BD Biosciences) flow cytometer (PRECYM flow cytometry platform, http://precym.mio.univ-amu.fr/). For BA cell counts, samples (0.3 mL) were incubated with SYBR Green II solution 1:10 (2 µL, Molecular Probes) for 15 min in the dark, in order to stain the nucleic acids. Each cell was characterized by 3 optical parameters: light diffusion 155 parameter side-scatter (SSC), green fluorescence (515-545 nm; SYBRgreen), and red fluorescence (670 LP; chlorophyll-a, in order to exclude autotrophic prokaryotes). Combining SYBRGreen fluorescence and SSC allowed to distinguish the cells from inorganic particles, detritus and free DNA (Marie et al., 2000). Data were processed using the CellQuest software (BD Biosciences), and BA was further determined using Summit 4.3 software (Beckman-Coulter).

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BP was estimated by 3 H-leucine incorporation applying the centrifugation method (Smith and Azam, 1992).
Samples (1.5 mL) were incubated in the dark between 1 and 6 h at 18 °C with a mixture of 3 H-leucine (Perkin Elmer ® specific activity 106 Ci mmol -1 ) and non-radioactive leucine to a final concentration of 20 nM (6 nM 3 H-leucine + 14 nM cold leucine) in 2-mL Eppendorf tubes. Incorporations were stopped by addition of trichloroacetic acid (TCA) https://doi.org/10.5194/bg-2020-187 Preprint. Discussion started: 23 July 2020 c Author(s) 2020. CC BY 4.0 License. to a final concentration at 5%. The control was prepared for each treatment by the addition of TCA, before the addition 165 of 3 H-leucine. Samples were then centrifuged for 10 min at 16,000 g three times, first with the fixed sample, second with TCA 5% and finally with ethanol 80%. After resuspension of the pellet in 1.5 mL scintillation liquid (Ultima-Gold MV), radioactivity was determined by a liquid scintillation counter. Leucine incorporation rates were converted into carbon production using the conversion factors of 1.5 kg C per mole of leucine incorporated (Kirchman, 1993). EEA were measured fluorometrically, using 2 fluorogenic model substrates, 4 methylumbelliferyl -βD-170 glucopyranoside (MUF-βglu) and L-leucine-7-amido-4-methyl-coumarin (Leu-MCA) as representative of βglucosidase and aminopeptidase respectively (Hoppe, 1983). Hydrolysis rates were determined by incubating in black 24 microtiter-plate 2 mL of D and A treatments with 6 (0.05; 0.2; 1; 2; 5 and 10 µM) concentrations of each substrate model. To ensure linearity of the hydrolysis rate, the increase of fluorescence was measured at multiple time points during the incubation period (ex/em: 380/440 nm for MCA and 365/450 nm for MUF, wavelength width 5 nm) in a 175 VARIOSCAN LUX microplate reader. The instrument was calibrated with standards of MCA and MUF solutions diluted in < 0.2 μm filtered seawater.
Samples for DOC analysis (10 mL) were filtered online from the incubation bottles, through pre-combusted (450 °C, 6 h) 47-mm GF/F filters. The filtrates were then transferred into pre-combusted glass tubes where 50 µL of phosphoric acid (H3PO4, 85%) was added. The glass tubes were sealed and stored in the dark at 4 °C until analysis. Prior to analysis, TDN and TDP were submitted to a wet oxidation according to Pujo-Pay and Raimbault (1994). The detection limits for DIN (NO3 -+ NO2and DIP (PO4 3-) analysis were 0.05 µM and 0.02 µM, respectively.
Bacterial growth efficiency (BGE, %) was calculated by dividing the time integrated BP by the corresponding labile fraction of DOC (LDOC).
Maximum hydrolysis rate (Vmax) and Michaelis-Menten constant (Km) were determined by fitting the EEA data using a nonlinear regression on the rectangular hyperbolic function following:

= +
Where V is the MUF-βglu or MCA-leu hydrolysis rate and S the concentration of the fluorogenic substrate.

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The three-replicate average values of bacterial activity (BA, BP and EEA) and nutrient concentrations (DOC, DON and DOP) in the G, D, A and C treatments were compared, over the incubation period, using a one-way ANOVA statistical test. ANOVA returns a p-value higher than 0.05 for the null hypothesis that the means of the different studied treatments are equal.

Total and dissolved organic carbon content of aerosols
The content of TOC in aerosols and of DOC in the water-soluble fractions were higher in anthropogenic (0.155 and 0.05 g C/g aerosols, respectively) than in Saharan dust aerosols (0.063 and 0.008 g C/g aerosol, respectively) (Table 1). Likewise, the dissolved fraction resulting from leaching was higher in the anthropogenic aerosols (32%) than in Saharan dust (13%) ( Table 1). One hour after aerosols amendments (T0), the measured initial 215 concentration of DOC was 40 ± 3 µM in the G-treatment, 36 ± 2 µM in the A-treatment and 34 ± 3 µM in the Dtreatment. Over the incubation period, DOC concentration decreased in all treatments ( Fig. 2A). This decrease was highest in the G-treatment (22 ± 2 µM) followed by both D (9 ± 2 µM) and A (9 ± 4 µM) treatments and then the Ctreatment (5 ± 1 µM) ( Table 2; Fig. 2A). The resulted labile DOC fractions were 55 ± 2%, 25 ± 4% and 24 ± 8% in G, D and A treatments, respectively (Table 2). 220

Dissolved organic nitrogen and phosphate
The initial DON and DOP concentrations in the C-treatment were 1.6 ± 0.1 µM and below the detection limit, respectively. The G-treatment exhibited the same initial DON concentration as the C-treatment, with values of 1.8 ± 0.2 µM while DOP concentrations reached 0.03 ± 0.01 (Fig. 1B, C). In A and D-treatments, the concentration of both DON and DOP increased immediately after aerosol addition (T0). The DON concentration reached 4.3 ± 0.7 µM and 225 3.7 ± 0.2 µM in the A and D-treatments, respectively (Fig. 1A), resulting in lower C:N and higher N:P elemental ratios in A and D treatments than in G-treatment (Table S2). The increase in DOP after aerosol addition in the D-treatment was of 0.02 ± 0.005 µM and was similar to that observed in the G-treatment. In the A-treatment, the increase in DOP https://doi.org/10.5194/bg-2020-187 Preprint. Discussion started: 23 July 2020 c Author(s) 2020. CC BY 4.0 License.
was slightly higher reaching a value of 0.04 ± 0.007 (Fig. 2B), which resulted in lower C:P ratios in A than in both D and G in the beginning of the experiment (Table S2).

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In all treatments, over the incubation period, DON concentrations remained constant while DOP concentrations exhibited a significant increase between T0 and T=5.7 days, to finally decrease to values below the detection limit at the end of the incubation period ( Fig. 1B and 1C). Over the incubation period, C:N elemental ratios decreased slightly in A (ANOVA; p<0.05; F=5.3; df=8) and G (ANOVA; p<0.05; F=31.5; df=8) treatments while they remained constant in the D (ANOVA; p>0.05; F=0.1; df=8) and C (ANOVA; p>0.05; F=0.5; df=8) treatments (Table S2). In contrast, 235 C:P and N:P elemental ratios were similar in the A-treatment while they decreased significantly in both D and G treatments ( Table. S2).

Microbial activity over the incubation period
In all the experimental bottles, an increase in both bacterial abundance (BA) and bacterial production (BP) was observed during the incubation time. One replicate from the A-treatment diverged completely from the other replicates

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(it did not show any bacterial growth and BP fluxes collapsed suddenly on day 6) and it was excluded from the data processing.
At the beginning of the incubations (T0), BA was similar in all treatments (ANOVA; p>0.05; F=0.64; df=10), with an average value of 2.3 ± 0.1 x 10 5 cells mL -1 (Fig. 3A). After 1.7 days of incubation, BA exhibited a 3-fold decrease in all treatments. Following this decrease, a lag time phase was observed, during which BA continued to 245 decrease slowly in all treatments. This lag phase period was longer in the C-treatment (7.7 days), followed by both A and D-treatments (5.7 days) and finally by the G-treatment (3.7 days; Fig. 3A). After that period, an exponential growth of BA was observed first in the G-treatment, followed then by both A and D-treatments and finally by the Ctreatment (Table 3). During that exponential growth period, BA reached similar values (ANOVA; p=0.34; F=1.31; df=10) in G (6 ± 3 x 10 5 cells mL -1 ), A (5 ± 2 x 10 5 ), and D (5 ± 1 x 10 5 ) treatments (Fig. 3A). In the control treatment, 250 until t= 6.7 days, BA remained low, < 0.6 x 10 5 cells mL -1 and then increased up to 2.5 ± 0.6 x 10 5 cells mL -1 during the exponential growth phase (Fig. 3A). At the end of the incubation period, BA continued to increase in all treatments, reaching up to twice the observed BA during exponential growth phase (Fig. 3A).
Initial BP was low in all experimental bottles, with an average value of 0.042 ± 0.035 ng C L -1 h -1 (Fig. 3B). BP started to increase first in the G-treatment followed by D and then A treatments ( Fig. 3B; Table 3). Like BA, BP also 255 exhibited an exponential growth phase, which started after a lag phase shorter than that of BA (Table 3). During the exponential growth period (Table 3), BP growth rates were similar in G and D treatments (ANOVA, F=6.76; p>0.05; df=5) and were significantly higher than in A and C treatments (ANOVA, F=10.47; p<0.05; df=10) (Table 3).
The Michaelis Menten fit of aminopeptidase and β glucosidase activities were significant only at the end of the incubation period (T=15.7 days). Thereby, only these data are presented (Fig. S1) These differences between treatments were still observed considering specific Vm (per bacterial cell, Fig. 4). Indeed,

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In this study, the addition of Saharan dust and anthropogenic aerosols, as a sole C-source to marine bacteria stimulated both heterotrophic bacterial abundance (BA) and production (BP), evidencing the bioavailability of aerosol-derived DOC.
However, at the beginning of the experiment, a lag time period was observed in all treatments, during which BA dropped by 3 times of its initial value. This consistent decrease of BA may be attributed to a stress of marine 285 heterotrophic bacteria during the preparation of the inoculum and to their contact with new environment/matrix, containing an unusual source of carbon. Indeed, although a lag time period was also recorded in the G-treatment, it was shorter than that in A and D-treatments, which could suggest a non-immediate bioavailability of aerosol organic matter compared to glucose. This non-immediate bioavailability of the dissolved pool of organic matter has been After the lag phase, an increase in BA and BP was observed first in the G-treatment, followed by D and then Atreatment, with bacterial growth rates significantly higher in G and D-treatments than in A-treatment. In contrast to 295 Marín et al. (2017b), in which BA and BP exhibited a contrasted response following mineral dust and anthropogenic aerosols addition, the observed increase of both BA and BP in this study were higher in the D-treatment than in A.
Following this increase in bacterial activity, DOC was consumed, highlighting a higher LDOC fraction in the G-https://doi.org/10.5194/bg-2020-187 Preprint. Discussion started: 23 July 2020 c Author(s) 2020. CC BY 4.0 License. treatment than in A and D-treatments. In those two treatments, LDOC fractions were quantitatively similar, despite a higher solubility of organic carbon derived from anthropogenic aerosols compared to Saharan dust aerosols.

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Nevertheless, contrasted metabolic pathways were evolved by marine heterotrophic bacteria in A and D treatments over the time scale of the incubation period. Indeed, the BGE in the D-treatment (14.2 ± 5.5%) compares well with that of the G treatment (7.6 ± 2%) and both values were significantly higher than that of the A-treatment (1.7 ± 0.1%).
This result suggests that, in the experimental conditions of this study, the metabolic use of LDOC in G and Dtreatments was energetically equivalent, with evidences of approximatively 1/10 of DOC incorporated going into 305 structural components. In contrast, the carbon consumed in A-treatment was mostly catabolized.
The factors controlling whether organic carbon is catabolized or incorporated into microbial biomass is still poorly resolved. Nevertheless, the conversion of carbon into biomass only occurs after non-growth requirements have been satisfied and sufficient excess of carbon and energy are available (Del Giorgio and Cole, 1998). To explain the differences in BGE observed in this study among glucose, Saharan dust and anthropogenic aerosol amendments, 310 several hypotheses can be proposed (see below).

Potential controlling factors of the bacterial growth efficiency
A number of parameters were controlled at the beginning and/or during the incubation period and can thus be reasonably excluded. Indeed, temperature and initial microbial inoculum were equal among all treatments. Since DIN and DIP were added in excess, N and P availability were not growth limiting over the incubation period. In contrast,

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DOM composition or quality and/or micronutrients availability (i.e. Fe, Zn) may have influenced the BGE in A and D aerosols treatments, as they are reported as the main variables controlling the BGE in fresh and marine waters (Fenchel and Blackburn, 1979;Biddanda et al., 1994;Carlson and Ducklow, 1996;Kirchman et al., 2018 and references therein).
In this study, BGE was lower in A than in both D and G treatments, which could suggest a DOM pool of a lower 320 quality in anthropogenic aerosols with respect to Saharan dust. The observed differences in ectoenzymatic activities between D-and A-treatments support this hypothesis. The higher cell specific aminopeptidase activity in A treatment combined with its enzymatic system adapted to low concentrations (low Km), presumably suggest a lower bacterial access to amino acids despite a higher DON concentration in A than in D treatment. Thus, the versatility in catabolic enzymatic synthesis was probably limited due to less access to amino acids, contributing to the observed low BGE in 325 the A treatment. In the D treatment, the lower development of aminopeptidase together with a better development of β-glucosidase capacities (higher specific Vm; lower Km and thus a better affinity for substrate) suggested that molecules derived from carbohydrates were used for anabolism and as a source of energy in one hand and that organic nitrogen source were more available to heterotrophic bacteria in the other hand, leading to a better global benefit for heterotrophic bacteria as shown by the higher BGE.

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The observed differences in ectoenzymatic activities may have been potentially upregulated by trace metals and/or vitamins cofactors on one hand, or inhibited due to a supply of toxic elements, in the other hand. Saharan dust deposition has been suggested as an important source of iron to surface waters (Jickells et al., 2005). There is an increasing evidence on the potential role of iron as a cofactor requirement for several enzymes involved in photosynthesis, N2 fixation and remineralization (Wu et al., 2000;Twining et al., 2004;Browning et al., 2017). In this study, a potential supply of iron or other trace metal elements (i.e. zinc, cobalt) following Saharan dust aerosols addition may have stimulated the bacterial ectoenzymatic activity and/or other metabolic pathways in the D-treatment.
At the opposite, an eventual upload of toxic elements, following anthropogenic aerosols (Paytan et al., 2009;Jordi et al., 2012), may have constrained the bacterial biosynthesis in the A-treatment.
Besides micronutrients, a significant amount of dissolved organic nitrogen (DON) was leached from both A 340 and D aerosols, highlighting the important contribution of not only C, but also N containing organic molecules to atmospheric deposition, such as previously reported through atmospheric flux quantification and modeling (Markaki et al., 2010;Djaoudi et al., 2018;Kanakidou et al., 2012;Galleti et al., 2020, this special issue). This DON supply resulted in a significant decrease of C:N elemental ratios in both A and D treatments with respect to G, immediately after seeding (Table S2). BGE of natural assemblages of marine bacteria grown on a range of substrates 345 has been shown to be inversely related to the C:N ratio of the substrate. Indeed, Goldman al. (1987) showed that the BGE was independent of the source of C and N but increased as the C:N ratio of the substrate decreased. In this study, although C:N stoichiometric ratios were similar in D and A aerosols treatments over the incubation period, contrasted BGE were observed suggesting that elemental ratios alone were not sufficient to explain the differences between A and D treatments, in the condition of the experiment.

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The contrasted BGE and ectoenzymatic development toward access to organic molecules in both D and A treatments may have been linked to the primary sources and the chemical composition and/or structure of aerosols as well. Anthropogenic aerosols are associated with various combustion processes, including industrial production; vehicles exhaust and domestically or waste burning, producing mainly soot particles (Li et al., 2001;Alves et al., 2012;Kanakidou et al., 2012;. These soot particles are generally coated with various organic compounds,

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forming complex mixtures of highly condensed organic matter. For example, polycyclic aromatic hydrocarbons and a large number of aliphatic compounds, are ubiquitous within anthropogenic aerosols (Omar et al., 2006;Alves et al., 2012;Barhoumi et al., 2018). However, these compounds have low water-solubility, and thus their contribution to the DOC pool could not explain alone the low BGE observed in the A-treatment with respect to both D and G-treatments.
In Mediterranean big cities, the atmospheric organic fraction is also related to secondary organic aerosols 360 (SOA) formation, with a contribution to the fine fraction of aerosols, ranging between 60 and 80% (Amato et al., 2015). In urban atmospheric aerosols, the water-soluble organic carbon has been highlighted as mostly aliphatic in nature (approximately 95% by C mass), with major contributions from alkyls and oxygenated alkyls (~ 80%), carboxylic acids (~ 10%), and to a lower extent from aromatic functional group (~ 4%). Among the organic species found in anthropogenic aerosols, alkyls or oxygenated alkyls, (poly)carboxylic acids/carboxylates (e.g. formate and 365 oxalate), sugars (e.g. levoglucosan) and HUmic-LIke Substances (HULIS) have been reported as the main contributors (Jaffrezo et al., 2005;Sannigrahi et al., 2006;Salma et al., 2013;Theodosi et al., 2018). Recently, HULIS, which are a mixture of high molecular weight organic (hydrophobic aliphatic and aromatic) compounds has been highlighted as contributing for a significant proportion of water-soluble organic carbon (up to 70%) (Zheng et al., 2013;Violotis et al., 2017).Thus, the HULIS compounds potential contribution to the DOC pool in the A-treatment, may have 370 constrained the overall bioavailability of energy and carbon, and thus the potential of marine bacteria for biosynthesis.
Otherwise, an enrichment of anthropogenic aerosols by organic compounds such as formate, acetate, oxalic and malonic acids has been previously reported in the atmosphere close to emission sources or after atmospheric transport (Sullivan and Prather, 2007;Leaitch et al., 2009;Paris et al., 2010). Some of these compounds (i.e. formate, malonic acids) as being involved in microbial metabolic pathways, could promote respiration and thus a low BGE.

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The most abundant organic compounds in dust aerosols revealed a vegetal origin and are more particularly highlighted as the reflect of the past vegetation cover of soils, from where dust aerosols were emitted (Eglinton, 2002).
Thus, organic carbon was associated with more or less decomposed biological residues, including micro-organisms debris, as well as humic substances (Conen et al., 2011). In this study, Saharan dust aerosols were locally sampled within the short time scale of the dust event (48 h). This may prevented from an internal mixing of Saharan dust 380 aerosols with other organic compounds in the atmosphere, revealing a higher bioavailable character of the Saharan dust derived-DOC for marine bacteria, when compared to the anthropogenic aerosols derived-DOC. Thereby, the higher BGE in D treatment with respect to A may have been the result of a DOC pool of a vegetal origin, more available to marine bacteria than that derived from anthropogenic emissions. For instance, a probable richness in cellulose -containing molecules in the "fresh" dust used in this study could explain the higher β glucosidase activity 385 in the D-treatment.

Potential implications for the marine carbon cycle in the Mediterranean Sea
Atmospheric fluxes of DOC in the Mediterranean Sea have been reported to be 6 times higher than river fluxes The contrasted metabolic pathways evolved by marine heterotrophic bacteria whether they are facing anthropogenic or Saharan dust aerosols, would potentially influence the fate of derived DOC. When facing anthropogenic aerosols, the result of the present study indicated that most of the consumed carbon is catabolized (BGE = 1.7 ± 0.1%), and thus would be returned to the atmosphere as CO2. However, when heterotrophic bacteria are facing 430 Saharan dust aerosols, approximatively 1/10 of the LDOC was incorporated into biomass, resulting in a BGE of 14.2 ± 5.5%. Nevertheless, atmospheric inputs of labile organic matter can lead to increased remineralization of the marine DOM, potentially acting as a priming effect. Likewise, the marine dissolved organic matter pool, by shaping bacterioplankton composition, could likely influence the microbial utilization of anthropogenic and Saharan dust derived organic matter as well, thus influencing BGE. Therefore, investigating the interplay between the different 435 sources of DOM in link with microbial activity would allow getting further insight regarding the striking interaction between atmospheric deposition and the marine carbon cycle, particularly regarding the role of marine bacteria as a link or sink of carbon.
Aside a potential contribution of atmospheric DOC deposition in sustaining secondary production, the semi-labile and/or refractory fractions of those atmospheric inputs, would influence the ocean surface biogeochemistry as well as 440 carbon export. DOC export has been highlighted as playing a critical role within the biological carbon pump in the Mediterranean Sea, leading to an export of 17 g C m -2 year -1 (Guyennon et al., 2015). Estimated as for LDOC, RDOC fluxes would range between 0.5-1.1 g C m -2 year -1 for Saharan dust deposition and between 0.5-1.2 g C m -2 year -1 for anthropogenic deposition. Thereby, the contribution of refractory DOC derived from Saharan dust and anthropogenic https://doi.org/10.5194/bg-2020-187 Preprint. Discussion started: 23 July 2020 c Author(s) 2020. CC BY 4.0 License.
deposition would contribute to the DOC export of 3-6.5% and 3-7%, respectively, likely influencing the biological 445 carbon pump especially in increasing scenarios of atmospheric emissions.

Conclusion
Organic carbon derived from anthropogenic aerosols exhibited a higher solubility (32%) with respect to Saharan dust (13%). Despite such a difference, the amount of bioavailable dissolved organic carbon (DOC) to marine 450 heterotrophic bacteria was quantitatively similar, with contributions of the labile dissolved organic carbon to the total dissolved organic fraction of 25 ± 4% and 24 ± 8% in Saharan dust and anthropogenic aerosols, respectively.
Interestingly, the bacterial growth efficiency (BGE) in the Saharan dust treatment (14.2 ± 5.5%) was higher than that of the anthropogenic treatment (1.7 ± 0.1%), suggesting differences in the metabolic response depending on the aerosol source. This study reveals a new link between atmospheric deposition and the oceanic carbon cycle. Indeed, inputs of 455 atmospheric anthropogenic carbon to the ocean, could promote its respiration by bacterial communities. In contrast, carbon derived from Saharan dust aerosols may contribute to biomass production. These results question the future trajectory of ocean-climate feedbacks in oligotrophic oceans, particularly in increasing scenarios of anthropogenic emissions.

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This work is a contribution to the Labex OT-Med (n° ANR-11-LABX-0061) funded by the French Government   Mean (± SD) 9 ± 2 25 ± 4 Table 3. Duration of the exponential growth phase for BA and BP, bacterial growth rate (µ) estimated from BP changes during the exponential growth phase, time integrated bacterial production (BP) during the exponential growth phase and bacterial growth efficiency (BGE). Data from each triplicate and average (± SD) 685 values are given for the control (C), glucose, anthropogenic and Saharan dust treatments.