Abstract
We simultaneously measured bacterial production (BP), bacterial respiration (BR), alkaline phosphatase activity (phos) and ectoaminopeptidase activity (prot) in relation to biogeochemical parameters, nutritive resources and in situ temperature over a 1-year survey at the long-term observatory the SOLEMIO station (Marseille bay, NW Mediterranean Sea). Despite its proximity to the coast, oligotrophic conditions prevailed at this station (yearly mean of Chl a = 0.43 μg dm−3, NO3 = 0.55 μmol dm−3 and PO4 = 0.04 μmol dm−3). Episodic meteorological events (dominant winds, inputs from the Rhone River) induced rapid oscillations (within 15 days) in temperature and sometimes salinity that resulted in rapid changes in phytoplankton succession and a high variability in C/P ratios within the particulate and dissolved organic matter. Throughout the year, BP ranged from 0.01 to 0.82 μg C dm−3 h−1 and bacterial growth efficiency varied from 1 to 39 %, with higher values in summer. Enrichment experiments showed that BP was limited most of the year by phosphorus availability (except in winter). A significant positive correlation was found between in situ temperature, BP, BR and phos. Finally, we found that temperature and phosphate availability were the main factors driving heterotrophic bacterial activity and thus play a fundamental role in carbon fluxes within the marine ecosystem.
Similar content being viewed by others
References
Alonso-Sáez L, Gasol JM (2007) Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in northwestern Mediterranean coastal waters. Appl Environ Microbiol 73:3528–3535
Alonso-Sáez L, Vázquez-Domínguez E, Cardelús C, Pinhassi J, Sala MM, Lekunberri I, Balagué V, Vila-Costa M, Unrein F, Massana R, Simó R, Gasol JM (2008) Factors controlling the year-round variability in carbon flux through bacteria in a coastal marine system. Ecosystems 11:397–409
Aminot A, Kérouel R (2004) Dissolved organic carbon, nitrogen and phosphorus in the N–E Atlantic and the N–W Mediterranean with particular reference to non-refractory fractions and degradation. Deep Sea Res Part I Oceanogr Res Pap 51:1975–1999
Apple JK, del Giorgio PA, Kemp WM (2006) Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aquat Microb Ecol 43:243–254
Aranguren-Gassis M, Teira E, Serret P, Martínez-García S, Fernández E (2012) Potential overestimation of bacterial respiration rates in oligotrophic plankton communities. Mar Ecol Prog Ser 453:1–10
Berggren M, Laudon H, Jonsson A, Jansson M (2010) Nutrient constraints on metabolism affect the temperature regulation of aquatic bacterial growth efficiency. Microb Ecol 60:894–902
Bouvy M, Bettarel Y, Bouvier C, Domaizon I, Jacquet S, Le Floc’h E, Montanié H, Mostajir B, Sime-Ngando T, Torréton JP, Vidussi F, Bouvier T (2011) Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change. Environ Microbiol 13:1842–1857
Broche P, Devenon J-L, Forget P, de Maistre J-C, Naudin J-J, Cauwet G (1998) Experimental study of the Rhone plume. Part I: physics and dynamics. Oceanol Acta 21:725–738
Cauwet G (1994) HTCO method for dissolved organic carbon analysis in seawater: influence of catalyst on blank estimation. Mar Chem 47:55–64
Céa B, VanWambeke F, Lefèvre D, Chirurgien L (under review) How temperature and resources affect activities of marine heterotrophic bacteria? A seasonal study in Marseille’s Bay. Aquat Microb Ecol
Christakill U, Van Wambeke F, Dolan JR (1999) Nanoflagellates (mixotrophs, heterotrophs and autotrophs) in the oligotrophic eastern Mediterranean: standing stocks, bacterivory and relationships with bacterial production. Mar Ecol Prog Ser 181:297–307
Cole JJ, Pace ML (1995) Bacterial secondary production in oxic and anoxic freshwaters. Limnol Oceanogr 40:1019–1027
Cotner JB, Ammerman JW, Peele ER, Bentzen E (1997) Phosphorus-limited bacterioplankton growth in the Sargasso Sea. Aquat Microb Ecol 13:141–149
Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66:1692–1697
Daneri G, Riemann B, Williams PJL (1994) In-situ bacterial production and growth-yield measured by thymidine, leucine and fractionated dark oxygen-uptake. J Plankton Res 16:105–113
del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541
del Giorgio PA, Williams PJ (2005) Respiration in aquatic ecosystems. Oxford University Press, Oxford, pp 1–17
Del Negro P, Celussi M, Crevatin E, Paoli A, Aubry FB, Pugnetti A (2008) Spatial and temporal prokaryotic variability in the northern Adriatic Sea. Mar Ecol 29:375–386
Estournel C, Broche P, Marsaleix P, Devenon J-L, Auclair F, Vehil R (2001) The Rhone River plume in unsteady conditions: numerical and experimental results. Estuar Coast Shelf Sci 53:25–38
Fischer U, Velimirov B (2002) High control of bacterial production by viruses in a eutrophic oxbow lake. Aquat Microb Ecol 27:1–12
Fraysse M, Pinazo C, Faure VM, Fuchs R, Lazzari P, Raimbault P, Pairaud I (2013) Development of a 3D coupled physical-biogeochemical model for the Marseille coastal area (NW Mediterranean Sea): what complexity is required in the coastal zone? PLoS ONE 8:e80012
Fraysse M, Pinazo C, Pairaud I (2014) Rôle du forçage physique sur l’écosystème à l'est du Golfe du Lion: Modulation de l'impact des apports anthropiques en sels nutritifs et matière organique étudiée par modélisation 3D couplée physique et biogéochimique, pH-D Thesis, Aix-Marseille University, 339 pp
Fraysse M, Pairaud I, Ross ON, Faure VM, Pinazo C (under review) Intrusion of Rhone River diluted water into the bay of Marseille: generation processes and impacts on ecosystem functioning. Geophys Res
Gatti J (2008) Intrusions du courant nord méditerranéen sur la partie est du plateau continental du golfe du Lion.
Gatti J, Petrenko A, Devenon J-L, Leredde Y, Ulses C (2006) The Rhone River dilution zone present in the northeastern shelf of the Gulf of Lion in December 2003. Cont Shelf Res 26:1794–1805
Grégori G, Colosimo A, Denis M (2001) Phytoplankton group dynamics in the Bay of Marseilles during a 2-year survey based on analytical flow cytometry. Cytometry 44:247–256
Hoppe HG (1983) Signifiance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser 11:299–308
Hoppe HG (2003) Phosphatase activity in the sea. Hydrobiologia 493:187–200
Hoppe H, Kim S, Gocke K (1988) Microbial decomposition in aquatic environments: combined process of extracellular enzyme activity and substrate uptake. Appl Environ Microbiol 54:784–790
Jahnke RA, Craven DB (1995) Quantifying the role of heterotrophic bacteria in the carbon cycle: a need for respiration rate measurements. Limnol Oceanogr 40:436–441
Kirchman D, K’nees E, Hodson R (1985) Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49:599–607
Kragh T, Søndergaard M, Tranvik L (2008) Effect of exposure to sunlight and phosphorus-limitation on bacterial degradation of coloured dissolved organic matter (CDOM) in freshwater. FEMS Microbiol Ecol 64:230–239
Kritzberg E, Arrieta J, Duarte C (2010a) Temperature and phosphorus regulating carbon flux through bacteria in a coastal marine system. Aquat Microb Ecol 58:141–151
Kritzberg ES, Duarte CM, Wassmann P (2010b) Changes in Arctic marine bacterial carbon metabolism in response to increasing temperature. Polar Biol 33:1673–1682
Kroer N (1993) Bacterial growth efficiency on natural dissolved organic matter. Limnol Oceanogr 38:1282–1290
Krom MD, Kress N, Brenner S, Gordon LI (1991) Phosphorus limitation of primary productivity in the eastern Mediterranean Sea. Limnol Oceanogr 36:424–432
Lami R, Ghiglione J-F, Desdevises Y, West NJ, Lebaron P (2009) Annual patterns of presence and activity of marine bacteria monitored by 16S rDNA–16S rRNA fingerprints in the coastal NW Mediterranean Sea. Aquat Microb Ecol 54:199–210
Lemée R, Rochelle-Newall E, Van Wambeke F, Pizay M-D, Rinaldi P, Gattuso J-P (2002) Erratum: seasonal variation of bacterial production, respiration and growth efficiency in the open NW Mediterranean Sea. Aquat Microb Ecol 29:227–237
López-Urrutia A, Morán XAG (2007) Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling. Ecology 88:817–822
Marie D, Partensky F, Jacquet S, Vaulot D (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR green I. Appl Environ Microbiol 63:186–193
Massana R, Pedros-Alio C, Casamayor EO, Gasol JM (2001) Changes in marine bacterioplankton phylogenetic composition during incubations designed to measure biogeochemically significant parameters. Limnol Oceanogr 46:1181–1188
Middelboe M, Søndergaard M (1993) Bacterioplankton growth yield: seasonal variations and coupling to substrate lability and beta-glucosidase activity. Appl Environ Microbiol 59:3916–3921
Millot C (1990) The Gulf of Lions’ hydrodynamics. Cont Shelf Res 10:885–894
Millot C, Wald L (1980) The effects of mistral wind on the Ligurian current near Provence. Oceanol Acta 3:399–402
Minas H (1968) A propos d’une remontée d’eaux “‘profondes’” dans les parages du golfe de Marseille (oct. 1964), conséquences biologiques. Cah Oceanogr 20:647–674
Obernosterer I, Kawasaki N, Benner R (2003) P limitation of respiration in the Sargasso Sea and uncoupling of bacteria from P regeneration in size-fractionation experiments. Aquat Microb Ecol 32:229–237
Para J, Coble PG, Charrière B, Tedetti M, Fontana C, Sempéré R (2010) Fluorescence and absorption properties of chromophoric dissolved organic matter (CDOM) in coastal surface waters of the northwestern Mediterranean Sea, influence of the Rhône River. Biogeosciences 7:4083–4103
Pairaud IL, Gatti J, Bensoussan N, Verney R, Garreau P (2011) Hydrology and circulation in a coastal area off Marseille: validation of a nested 3D model with observations. J Mar Syst 88:20–33
Pinhassi J, Gómez-Consarnau L, Alonso-Sáez L, Sala M, Vidal M, Pedrós-Alió C, Gasol J (2006) Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquat Microb Ecol 44:241–252
Raimbault P, Slawyk G, Coste B, Fry J (1990) Feasibility of using an automated procedure for the determination of seawater nitrate in the 0–100 nM range: examples from field and cultures. Mar Biol 104:347–351
Raimbault P, Diaz F, Pouvesle W, Boudjellal B (1999) Simultaneous determination of particulate organic carbon, nitrogen and phosphorus collected on filters, using a semi-automatic wet-oxidation method. Mar Ecol Prog Ser 180:289–295
Raimbault P, Lantoine F, Neveux J (2004) Rapid measurement of chlorophyll a and of phaeopigments a by fluorimetry after extraction with methanol. Comparison with the classic acetone extraction method. Océanis 30:189–205
Reffray G, Fraunie P, Marsaleix P (2004) Secondary flows induced by wind forcing in the Rhone region of freshwater influence. Ocean Dyn 54:179–196
Rivkin RB, Legendre L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400
Sala MM, Karner M, Arin L (2001) Measurement of ectoenzyme activities as an indication of inorganic nutrient imbalance in microbial communities. Aquat Microb Ecol 23:301–311
Sarmento H, Montoya JM, Vazquez-Dominguez E, Vaqué D, Gasol JM (2010) Warming effects on marine microbial food web processes: how far can we go when it comes to predictions? Philos Trans R Soc Lond B Biol Sci 365:2137–2149
Sebastian M, Ammerman JW (2009) The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J 3:563–572
Simó R, Vila-Costa M, Alonso-Sáez L, Cardelús C, Guadayol Ò, Vázquez-Domínguez E, Gasol J (2009) Annual DMSP contribution to S and C fluxes through phytoplankton and bacterioplankton in a NW Mediterranean coastal site. Aquat Microb Ecol 57:43–55
Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microbial Food Webs 6:107–114
Thingstad TF, Zweifel UL, Rassoulzadegan F (1998) P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnol Oceanogr 43:88–94
Thyssen M, Mathieu D, Garcia N, Denis M (2008) Short-term variation of phytoplankton assemblages in Mediterranean coastal waters recorded with an automated submerged flow cytometer. J Plankton Res 30:1027–1040
Torréton J-P, Talbot V, Garcia N (2000) Nutrient stimulation of bacterioplankton growth in Tuamotu atoll lagoons. Aquat Microb Ecol 21:125–137
Tréguer P, Corre P Le (1975) Manuel d’analyse des sels nutritifs dans l'eau de mer (utilisation de l'autoAnalyseur II Technicon). Laboratoire d'Océanographie chimique, Université de bretagne occidentale
Vallino JJ, Hopkinson CS, Hobbie JE (1996) Modeling bacterial utilization of dissolved organic matter: optimization replaces Monod growth kinetics. Limnol Oceanogr 4:1591–1609
Van Wambeke F, Christaki U, Giannakourou A, Moutin T, Souvemerzoglou K (2002) Longitudinal and vertical trends of bacterial limitation by phosphorus and carbon in the Mediterranean Sea. Microb Ecol 43:119–133
Van Wambeke F, Bonnet S, Moutin T, Raimbault P, Alarc G (2008) Factors limiting heterotrophic bacterial production in the southern Pacific Ocean. Biogeosciences 5:833–845
Van Wambeke F, Ghiglione J-F, Nedoma J, Mével G, Raimbault P (2009) Bottom up effects on bacterioplankton growth and composition during summer-autumn transition in the open NW Mediterranean Sea. Biogeosciences 6:705–720
Vázquez-Domínguez E, Vaqué D, Gasol JM (2007) Ocean warming enhances respiration and carbon demand of coastal microbial plankton. Glob Chang Biol 13:1327–1334
Williams PJL, Jenkinson NW (1982) A transportable microprocessor-controlled precise Winkler titration suitable for field station and shipboard use. Limnol Oceanogr 27:576–584
Zweifel UL, Norrman B, Hagstrom A (1993) Consumption of dissolved organic carbon by marine bacteria and demand for inorganic nutrients. Mar Ecol Prog Ser 101:23–32
Acknowledgements
This work was supported by the EC2CO (Ecosphère Continentale et Cotière) program and DEMO2 (Dégradation de la Matière Organique) project. We are very grateful to the crew of the R/V Antedon II for their excellent service at sea and the SOMLIT staff for providing CTD data from SOLEMIO. Ph.D. scholarship to B. Céa was provided by the Provence Alpes Côte d’Azur region. We also wish to thank Beatrice Beker for her data of the microphytoplankton and Christophe Yohia for his wind direction compass. Special thanks go to Karine Le Blanc, Bernard Queguiner the CYBELE team from MIO for their helpful comments. We are grateful to Dr. Philippe Garrigues for helpful comments on the manuscript and to the reviewer for their useful criticisms. This is a contribution to the SOMLIT network.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Céa, B., Lefèvre, D., Chirurgien, L. et al. An annual survey of bacterial production, respiration and ectoenzyme activity in coastal NW Mediterranean waters: temperature and resource controls. Environ Sci Pollut Res 22, 13654–13668 (2015). https://doi.org/10.1007/s11356-014-3500-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-014-3500-9