Cite this paper:
Michel DENIS, Dominique LEFEVRE, Melilotus THYSSEN, Ian R. JENKINSON, Gérald GRÉGORI. Pulsed export of carbon in the north-western Mediterranean Sea[J]. Journal of Oceanology and Limnology, 2023, 41(1): 189-202

Pulsed export of carbon in the north-western Mediterranean Sea

Michel DENIS1, Dominique LEFEVRE1, Melilotus THYSSEN1, Ian R. JENKINSON2,3, Gérald GRÉGORI1
1 Aix Marseille Université, Université de Toulon, CNRS/INSU, IRD, Institut Méditerranéen d'Océanologie(MIO), Marseille cedex09 13288, France;
2 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
3 Agency for Consultation and Research in Oceanography, Lavergne, 19320 La Roche Canillac, France
Abstract:
The short term (hourly scale) variability of heterotrophic prokaryote (HP) vertical distribution and respiratory activity, was investigated in the north-western (NW) Mediterranean Sea. HP vertical distribution was determined on board by flow cytometry analysis of seawater samples collected by series of CTD casts. Cell counts and viability were determined for all samples. HP respiratory rates were determined later in the laboratory from filtered seawater samples (23 dm3) from 300–1 150-m depth. The average cell viability was 94.8%±2.2% (n=240). There was no accumulation of dead cells, due to quick decay of damaged cells. In the epipelagic layer, three HP groups were distinguished, two (HNA1, HNA2) whose cells exhibited a high nucleic acid content and one (LNA) with low nucleic acid content cells. HNA2 was most populated at 50 m but not detected at 90 m and below, presumably aerobic anoxygenic photoheterotrophic bacteria (AAPs). The variability in HP abundance was mainly confined in the upper 80 m. A few secondary peaks of HP abundance were observed (80–150 m) in connection with abundance troughs in the surface layer. HP cells were continuously present in a wide layer around 500 m (mean 191×103 cells/cm3). Below this layer, HP abundance randomly exhibited peaks, coupled to respiratory rate peaks. The HP abundance and variability in the water column was suppressed during a strong wind event. The observed sporadic variability was tentatively interpreted through a pulsed carbon-export mechanism induced by the microorganism production of dissolved polysaccharides, followed by flocculation and rapid sinking. This mechanism would thus contribute to (i) preventing organic matter accumulation in the epipelagic layer, (ii) seeding the water column with live HP cells, and (iii) supplying the aphotic water column with fresh and labile organic matter. This important vertical flux mechanism needs further observations and modelling.
Key words:    north-western Mediterranean Sea|heterotrophic prokaryote (HP)|cell viability|cell respiration|transparent exopolymeric particle (TEP)|aggregation|flow cytometry   
Received: 2022-01-20   Revised:
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Articles by Michel DENIS
Articles by Dominique LEFEVRE
Articles by Melilotus THYSSEN
Articles by Ian R. JENKINSON
Articles by Gérald GRÉGORI
References:
Andersen V J, Sardou J. 1992. The diel migrations and vertical distributions of zooplankton and micronekton in the Northwestern Mediterranean Sea. 1. Euphausiids, mysids, decapods and fishes. Journal of Plankton Research, 14(8):1129-1154, https://doi.org/10.1093/plankt/14.8.1129.
Andersen V, Goutx M, Prieur L et al. 2009. Short-scale temporal variability of physical, biological and biogeochemical processes in the NW Mediterranean Sea: an introduction.Biogeosciences, 6(3): 453-461, https://doi.org/10.5194/bg-6-453-2009.
Andersen V, Gubanova A, Nival P et al. 2001a. Zooplankton community during the transition from spring bloom to oligotrophy in the open NW Mediterranean and effects of wind events. 2. Vertical distributions and migrations.Journal of Plankton Research, 23(3): 243-261, https://doi.org/10.1093/plankt/23.3.243.
Andersen V, Nival P, Caparroy P et al. 2001b. Zooplankton community during the transition from spring bloom to oligotrophy in the open NW Mediterranean and effects of wind events. 1. Abundance and specific composition.Journal of Plankton Research, 23(3): 227-242, https://doi.org/10.1093/plankt/23.3.227.
Annane S, St-Amand L, Starr M et al. 2015. Contribution of transparent exopolymeric particles (TEP) to estuarine particulate organic carbon pool. Marine Ecology Progress Series, 529: 17-34, https://doi.org/10.3354/meps11294.
Arístegui J, Gasol J M, Duarte C M et al. 2009. Microbial oceanography of the dark ocean’s pelagic realm.Limnology and Oceanography, 54(5): 1501-1529, https://doi.org/10.4319/lo.2009.54.5.1501.
Azam F, Smith D C. 1991. Bacterial influence on the variability in the ocean’s biogeochemical state: a mechanistic view.In: Demers S ed. Particle Analysis in Oceanography. NATO ASI Series, Vol 27. Springer-Verlag, Berlin, Heidelberg. p.213-236.
Baltar F, Arístegui J, Sintes E et al. 2009. Prokaryotic extracellular enzymatic activity in relation to biomass production and respiration in the meso- and bathypelagic waters of the (sub)tropical Atlantic. Environmental Microbiology, 11(8): 1998-2014, https://doi.org/10.1111/j.1462-2920.2009.01922.
Beauvais S. 2003. Etude des Particules Exopolymériques Transparentes (TEP) en milieu marin. Dynamique et rôle dans le cycle du carbone. Thesis Université Pierre et Marie Curie - Paris VI.
Boyd P W, Sherry N D, Berges J A et al. 1999. Transformations of biogenic particulates from the pelagic to the deep ocean realm. Deep Sea Research Part II: Topical Studies in Oceanography, 46(11-12): 2761-2792, https://doi.org/10.1016/S0967-0645(99)00083-1.
Cavicchioli R, Ripple W J, Timmis K N et al. 2019. Scientists’ warning to humanity: microorganisms and climate change. Nature Reviews Microbiology, 17(9): 569-586, https://doi.org/10.1038/s41579-019-0222-5.
Del Giorgio P A, Duarte C M. 2002. Respiration in the open ocean. Nature, 420(6914): 379-384, https://doi.org/10.1038/nature01165.
Denis M, Martin V, Momzikoff A et al. 2003. Pulsed remineralisation in the northwestern Mediterranean Sea:a hypothesis. Journal of Marine Systems, 39(1-2): 19-41, https://doi.org/10.1016/S0924-7963(02)00244-0.
Engel A, Thoms S, Riebesell U et al. 2004. Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature, 428(6986): 929-932, https://doi.org/10.1038/nature02453.
Falkowski P G, Wilson C. 1992. Phytoplankton productivity in the North Pacific Ocean since 1900 and implications for absorption of anthropogenic CO2. Nature, 358(6389):741-743.
Field C B, Behrenfeld M J, Randerson J T et al. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science, 281(5374): 237-240, https://doi.org/10.1126/science.281.5374.237.
Gasol J M, Zweifel U L, Peters F et al. 1999. Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Applied and Environmental Microbiology, 65(10): 4475-4483, https://doi.org/10.1128/aem.65.10.4475-4483.1999.
Ghiglione J F, Palacios C, Marty J C et al. 2008. Role of environmental factors for the vertical distribution (0-1000 m) of marine bacterial communities in the NW Mediterranean Sea. Biogeosciences, 5(6): 1751-1764, https://doi.org/10.5194/bg-5-1751-2008
Grégori G, Citterio S, Ghiani A et al. 2001. Resolution of viable and membrane-compromised bacteria in freshwater and marine waters based on analytical flow cytometry and nucleic acid double staining. Applied and Environmental Microbiology, 67(10): 4662-4670, https://doi.org/10.1128/AEM.67.10.4662-4670.2001.
Grégori G, Denis M, Lefèvre D et al. 2003. Viabilité des bactéries hétérotrophes dans la baie de Marseille.Comptes Rendus Biologies, 326(8): 739-750, https://doi.org/10.1016/j.crvi.2003.07.001.
Isla A, Scharek R, Latasa M. 2015. Zooplankton diel vertical migration and contribution to deep active Carbon flux in the NW Mediterranean. Journal of Marine Systems, 143:86-97, https://doi.org/10.1016/j.jmarsys.2014.10.017.
Jenkinson I R, Biddanda B A, Turley C M et al. 1991.Rheological properties of marine organic aggregates importance for vertical flux, turbulence and microzones.Oceanologica Acta, 11: 101-107.
Jenkinson I R. 1986. Oceanographic implications of non-Newtonian properties found in phytoplankton cultures. Nature, 323(6087): 435-437, https://doi.org/10.1038/323435a0.
Karl D M, Hebel D V, Björkman K et al. 1998. The role of dissolved organic matter release in the productivity of the oligotrophic North Pacific Ocean. Limnology and Oceanography, 43(6): 1270-1286.
Kelly T B, Davison P C, Goericke R et al. 2019. The importance of mesozooplankton diel vertical migration for sustaining a mesopelagic food web. Frontiers in Marine Science, 9:508, https://doi.org/10.3389/fmars.2019.00508.
Kolber Z S, Van Dover C L, Niederman R A et al. 2000.Bacterial photosynthesis in surface waters of the open ocean. Nature, 407(6801): 177-179.
Larsson M E, Bramucci A R, Collins S et al. 2022. Mucospheres produced by a mixotrophic protist impact ocean carbon cycling. Nature Communications, 13: 1301, https://doi.org/10.1038/s41467-022-28867-8.
Le Moigne F A C. 2019. Pathways of organic carbon downward transport by the oceanic biological carbon pump. Frontiers in Marine Science, 6: 634, https://doi.org/10.3389/fmars.2019.00634.
Lefèvre D, Denis M, Lambert C E et al. 1996. Is DOC the main source of organic matter remineralization in the ocean water column? Journal of Marine Systems, 7(2-4):281-291.
Maerz J, Six K D, Stemmler I et al. 2020. Microstructure and composition of marine aggregates as co-determinants for vertical particulate organic carbon transfer in the global ocean, Biogeosciences, 17(7): 1765-1803, https://doi.org/10.5194/bg-17-1765-2020
Marx V. 2020. When microbiologists plunge into the ocean.Nature Methods, 17(2): 133-136, https://doi.org/10.1038/s41592-020-0736-9.
Méjanelle L, Dachs J. 2009. Short scale (6 h) temporal variation of sinking fluxes of planktonic and terrigeneous lipids at 200 m in the NW Mediterranean Sea. Biogeosciences, 6(12): 3017-3034.
Menzel D W, Ryther J H. 1968. Organic carbon and the oxygen minimum in the South Atlantic Ocean. Deep Sea Research and Oceanographic Abstracts, 15(3): 327-337.
Mével G, Vernet M, Goutx M et al. 2008. Seasonal to hour variation scales in abundance and production of total and particle-attached bacteria in the open NW Mediterranean Sea (0-1000 m). Biogeosciences, 5(6): 1573-1586.
Packard T T, Berdalet E, Blasco D et al. 1996. Oxygen consumption in the marine bacterium Pseudomonas nautica predicted from ETS activity and bisubstrate enzyme kinetics. Journal of Plankton Research, 18(10):1819-1835, https://doi.org/10.1093/plankt/18.10.1819.
Packard T T, Christensen J P. 2004. Respiration and vertical carbon flux in the Gulf of Maine water column. Journal of Marine Research, 62(1): 93-115.
Packard T T, Denis M, Rodier M et al. 1988. Deep-ocean metabolic CO2 production: calculations from ETS activity.Deep Sea Research Part A. Oceanographic Research Papers, 35(3): 371-382.
Packard T T, Williams P J Le B. 1981. Rates of respiratory oxygen consumption and electron transport in surface seawater from the Northwest Atlantic. Oceanologica Acta, 4(3): 351-358.
Packard T T. 1971. The measurement of respiratory electrontransport activity in marine phytoplankton. Journal of Marine Research, 29: 235-244.
Passow U, Alldredge A L, Logan B E. 1994. The role of particulate carbohydrate exudates in the flocculation of diatom blooms. Deep Sea Research Part I: Oceanographic Research Papers, 41(2): 335-357.
Passow U. 2002. Transparent exopolymer particles (TEP) in aquatic environments. Progress in Oceanography, 55(3-4): 287-333.
Raybaud V, Nival P, Mousseau L et al. 2008. Short term changes in zooplankton community during the summer-autumn transition in the open NW Mediterranean Sea: species composition, abundance and diversity, Biogeosciences, 5(6): 1765-1782, https://doi.org/10.5194/bg-5-1765-2008.
Savenkoff C, Lins da Silva N, Lefèvre D et al. 1992.Contribution of the different planktonic microbial assemblages to ETS activity in the Ligurian frontal area:north-west Mediterranean Sea. Journal of Plankton Research, 14(6): 835-850.
Savenkoff C, Prieur L, Reys J P et al. 1993. Deep microbial communities evidenced in the Liguro-Provencal front by their ETS activity. Deep Sea Research Part I:Oceanographic Research Papers, 40(4): 709-725.
Shapiro H M. 2003. Practical Flow Cytometry. 4th edn. Wiley, Hoboken, NJ. 736p.
Silovic T, Grégori G, Dugenne M et al. 2017. A new automated flow cytometer for high frequency in situ characterisation of heterotrophic microorganisms and their dynamics in aquatic ecosystems. In: Proceedings IMEKO International Conference on Metrology for the Sea. Naples, Italy. p.58-61.
Smith D C, Simon M, Alldredge A L et al. 1992. Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature, 359(6391): 139-142.
Smriga S, Fernandez V I, Mitchell J G et al. 2016.Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proceedings of the National Academy of Sciences of the United States of America, 113(6): 1576-1581, https://doi.org/10.1073/pnas.1512307113
Stemmann L, Picheral M, Gorsky G. 2000. Diel variation in the vertical distribution of particulate matter (>0.15 mm) in the NW Mediterranean Sea investigated with the Underwater Video Profiler. Deep Sea Research Part I:Oceanographic Research Papers, 47(3): 505-531, https://doi.org/10.1016/S0967-0637(99)00100-4.
Verdugo P, Alldredge A L, Azam F et al. 2004. The oceanic gel phase: a bridge in the DOM-POM continuum. Marine Chemistry, 92(1-4): 67-85, https://doi.org/10.1016/j.marchem.2004.06.017.
Williams P J Le B. 1981. Microbial contribution to overall marine plankton metabolism: direct measurements of respiration. Oceanologica Acta, 4: 359-364.
Zhao Y C, Zhao Y, Zheng S et al. 2020. Virioplankton distribution in the tropical western Pacific Ocean in the vicinity of a seamount. Microbiology Open, 9(6): 1207-1224, https://doi.org/10.1002/mbo3.1031.
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