BG Biogeosciences BG Biogeosciences 1726-4189 Copernicus Publications Göttingen, Germany 10.5194/bg-7-3491-2010 Autotrophic and heterotrophic metabolism of microbial planktonic communities in an oligotrophic coastal marine ecosystem: seasonal dynamics and episodic events Bonilla-Findji O. 1 2 Gattuso J.-P. 1 2 Pizay M.-D. 1 2 Weinbauer M. G. 1 2 INSU-CNRS, Laboratoire d'Océanographie de Villefranche, UMR 7093, B.P. 28, 06234 Villefranche-sur-Mer Cedex, France Université Pierre et Marie-Curie-Paris6, Laboratoire d'Océanographie de Villefranche, UMR 7093, 06230 Villefranche-sur-mer, France 08 11 2010 7 11 3491 3503 Copyright: © 2010 O. Bonilla-Findji et al. 2010 This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/ This article is available from https://bg.copernicus.org/articles/7/3491/2010/bg-7-3491-2010.html The full text article is available as a PDF file from https://bg.copernicus.org/articles/7/3491/2010/bg-7-3491-2010.pdf

A 18 month study was performed in the Bay of Villefranche to assess the episodic and seasonal variation of autotrophic and heterotrophic ecosystem processes. A typical spring bloom was encountered, where maximum of gross primary production (GPP) was followed by maxima of bacterial respiration (BR) and production (BP). The trophic balance (heterotrophy vs. autotrophy) of the system did not exhibit any seasonal trend although a strong intra-annual variability was observed. On average, the community tended to be net heterotrophic with a GPP threshold for a balanced metabolism of 1.1 μmol O<sub>2</sub> l<sup>−1</sup> d<sup>−1</sup>. Extended forest fires in summer 2003 and a local episodic upwelling in July 2003 likely supplied orthophosphate and nitrate into the system. These events were associated with an enhanced bacterioplankton production (up to 2.4-fold), respiration (up to 4.5-fold) and growth efficiency (up to 2.9-fold) but had no effect on GPP. A Sahara dust wet deposition event in February 2004 stimulated bacterial abundance, production and growth efficiency but not GPP. Our study suggests that short-term disturbances such as wind-driven upwelling, forest fires and Sahara dust depositions can have a significant but previously not sufficiently considered influence on phytoplankton- and bacterioplankton-mediated ecosystem functions and can modify or even mask the seasonal dynamics. The study also indicates that atmospheric deposition of nutrients and particles not only impacts phytoplankton but also bacterioplankton and could, at times, also shift systems stronger towards net heterotrophy.

 References Alonso-Saez, L., Vazquez-Dominguez, E., Cardelus, C., Pinhassi, J., Sala, M. M., Lekunberri, I., Balagué, V., Vila-Costa, M., Unrein, F., Massana, R., Simo, R., and Gasol, J. M.: Factors controlling the year-round variability in carbon flux through bacteria in a coastal marine system, Ecosystems, 11, 397–409, 2008. Anderson, L., Haraldson, C., and Roger, L.: Gran linearization of potentiometric Winkler titration, Mar. Chem., 37, 179–190, 1992. Anderson, T., Charlson, R., Schwartz, S., Knutti, R., Boucher, O., and Rohde, H.: Climate forcing by aerosols – a hazy picture, Science, 300, 1103–1104, 2003. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., and Thingstad, T. F.: The ecological role of water-column microbes in the sea, Mar. Ecol. Prog. Ser., 10, 257–263, 1983. Baines, S. B. and Pace, M. L.: The production of dissolved organic matter by phytoplankton and its importance to bacteria: patterns across marine and freshwater system, Limnol. Oceanogr., 36, 1078–1090, 1991. Bustillos-Guzmán, J., Claustre, H., and Marty, J.-C.: Specific phytoplankton signatures and their relationship to hydrographic conditions in the coastal NW Mediterranean Sea. Mar. Ecol. Prog. Ser., 124, 247–258, 1995. Benner, R. and Strom, M.: A critical evaluation of the analytical blank associated with DOC measurements by high-temperature catalytic oxidation, Mar. Chem., 41, 153–160, 1993. Cattaneo, R., Rouvière, C., Rassoulzadegan, F., and Weinbauer, M. G.: Association of viruses and bacteria with reference black carbon particles in marine coastal waters: A scanning electron, epifluorescence and confocal laser scanning microscopy analysis, FEMS Microbiol. Ecol., 74, 382–396, 2010. Claustre, H., Marty, J.-C., and Cassiani, L.: Intraspecific differences in the biogeochemical composition of a diatom during a spring bloom in Villefranche-sur-mer Bay, J. Exp. Mar. Biol. Ecol., 129, 17–32, 1989. Cole, J. J., Findlay, S., and Pace, M. L.: Bacterial production in fresh and saltwater ecosystems: a cross-system overview, Mar. Ecol. Prog. Ser., 43, 1–10, 1988. Dachs, J., Calleja, M. L., Duarte, C. M., del Vento, S., Turpin, B., Polidori, M., Herndl, G. J., and Agusti, S.: High atmosphere-ocean exchange of organic carbon in the NE subtropical Atlantic, Geophys. Res. Lett., 32, L21807, https://doi.org/10.1029/2005GL023799, 2005. Del Giorgio, P. A. and Cole, J.: Bacterial growth efficiency in natural aquatic systems, Ann. Rev. Ecol. Syst. 29, 503–541, 1998. Del Giorgio, P. A., Cole, J., and Cimbleris, A.: Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems, Nature, 385, 148–151, 1997. Del Giorgio, P. A. and Williams, P. L.: Respiration in aquatic ecosystems, Oxford Univ. Press. Inc., Oxford, 2005. Dolan, J., Thingstad, T. F., and Rassoulzadegan, F.: Phosphate transfer between microbial size-fractions in Villefranche Bay (NW Mediterranean Sea), France in autumn 1992, Ophelia, 41, 71–85, 1995. Duarte, C. M. and Agusti, S.: The CO2 balance of unproductive aquatic ecosystems, Science, 281, 234–236, 1998. Duarte, C. M., Agusti, S., and Vaqué, D.: Controls on planktonic metabolism in the Bay of Blanes, NW Mediterranean littoral, Limnol. Oceanogr., 49, 2162–2170, 2004. Duarte, C. M. and Cebrian, J.: The fate of marine autotrophic production, Limnol. Oceanogr., 41, 1758–1766, 1996. Duarte, C. M., Middelburg, J. J., and Caraco, N.: Major role of marine vegetation on the oceanic carbon cycle, Biogeosciences, 2, 1–8, https://doi.org/10.5194/bg-2-1-2005, 2005. Duarte, C. M. and Regaudie-de-Gioux, A.: Thresholds of gross primary production for the metabolic balance of marine planktonic communities, Limnol. Oceanogr., 54, 1015–1022, 2009. Fuhrman, J. A. and Azam, F.: Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results, Mar. Biol., 66, 109–120, 1982. Gasol, J. and Del Giorgio, P. A.: Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities, Sci. Mar., 64, 197–224, 2000. Gaston, J.: Etude du courant géostrophique entre Villefranche-sur-mer et Calvi. Cah., Océanogr., 19, 329–345, 1967. Gazeau, F., Duarte, C. M., Gattuso, J.-P., Barrón, C., Navarro, N., Ruiz, S., Prairie, Y. T., Calleja, M., Delille, B., Frankignoulle, M., and Borges, A. V.: Whole-system metabolism and CO<sub>2</sub> fluxes in a Mediterranean Bay dominated by seagrass beds (Palma Bay, NW Mediterranean), Biogeosciences, 2, 43–60, https://doi.org/10.5194/bg-2-43-2005, 2005. Gonzalez, N., Gattuso, J.-P., and Middelburg, J. J.: Oxygen production and carbon fixation in oligotrophic coastal bays and the relationships with gross and net primary production, Aquat. Microb. Ecol., 52, 119–130, 2008. Guerzoni, S., Landuzzi, W., Lenaz, R., Quarantotto, G., Cesari, G., Rampazzo, R., and Molinaroli, E.: Mineral atmospheric particulate from south to northwest Mediterranean: seasonal variations and characteristics, Water Poll. Res. Reports, 28, 483–493, 1992. Kirchman, D. L., K'Ness, E., and Hodson, R.: Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems, Appl. Environ. Microbiol., 49, 599–607, 1985. Kirchman, D. L. and Ducklow, H. W.: Estimating conversion factors for the thymidine and the leucine methods for measuring bacterial production, edited by: Kemp, P. F., Sherr, B. F., Sherr, E. B., and Cole, J. J., Handbook of Methods in Aquatic Microbial Ecology, Lewis Publishers, 513–518, 1993. Knap, A. H., Michaels, A. E., Close, A., Ducklow, H. W., and Dickson, A. G.: Protocols for the Joint Global Ocean Flux Study (JGOFS) core measurements, JGOFS Report Nr.&nbsp;19, Bergen, Norway, 1996. Lee, S. and Fuhrman, J. A.: Relationships between biovolume and biomass of naturally derived marine bacterioplankton, Appl. Environ. Microbiol., 53, 1298–1303, 1987. Legendre, L. and Le Fèvre, J.: Microbial food webs and the export of biogenic carbon in oceans, Aquat. Microb. Ecol., 9, 69–77, 1995. Lekunberri, I., Lefort, T., Romero, E., Vázquez-Domínguez, E., Marrasé, C. Peters, F., Weinbauer, M. G., and Gasol., J. M.: Effects of a dust deposition event on coastal marine microbial abundance and activity, bacterial community structure, and ecosystem function, J. Plankton Res., 381–396, 2010. Lorenzen, C.: A method for the continuous measurement of in vivo chlorophyll concentration, Deep-Sea Res. Pt.&nbsp;I, 13, 223–227, 1966. Migon, C. and Sandroni, V.: Phosphorus in rainwater: Partitioning inputs and impact on the surface coastal ocean, Limnol. Oceanogr., 44, 1160–1165, 1999. Morel, A. and André, J. M.: Pigment distribution and primary production in the Western Mediterranean as derived and modeled from coastal zone scanner observation, J. Geophys. Res., 86, 12685–12698, 1991. Moncoiffé, G., Alvarez-Salgado, X. A., Figueiras, F. G., and Savidge, G.: Seasonal and short-term-scale dynamics of microplankton community production and respiration in an inshore upwelling system, Mar. Ecol. Porg. Sr., 196, 111–126, 2000. Navarro, N., Agusti, S., and Duarte, C. M.: Plankton metabolism and dissolved organic carbon use in the Bay of Palma, NW Mediterranean Sea, Aquat. Microb. Ecol., 37, 47–54, 2004. Nival, P. and Corre, M. C.: Variation annuelle des charactéristiques hydrologiques de surface dans la rade de Villefranche-sur-mer, Ann. Inst. Océanogr. Paris, 52, 57–78, 1976. Nival, P., Malara, G., and Charra, R.: Evolution du plankton de la baie de Villefranche-sur-Mer à la fin du printemps (mai et juin 1971). I.&nbsp;Hydrologie, sels nutritifs, chlorophylle, Vie et Milieu, 25, 231–260, 1975 . Pulido-Villena, E., Wagener, T., and Guieu, C.: Bacterial response to dust pulses in the western Mediterranean: Implications for carbon cycling in the oligotrophic ocean, Global Biogeochem. Cy., 22, GB1020, https://doi.org/10.1029/2007GB003091, 2008. Ramanathan, V., Ramana, M. V., Roberts, G., Kim, D., Corrigan, C., Chung, C., and Winker, D.: Warming trends in Asia amplified by brown cloud solar absorption, Nature, 448, 575–578, 2007. Regaudie-de-Gioux, A., Vaquer-Sunyer, R., and Duarte, C. M.: Patterns in planktonic metabolism in the Mediterranean Sea, Biogeosciences, 6, 3081–3089, https://doi.org/10.5194/bg-6-3081-2009, 2009. Ridame, C. and Guieu, C. Saharan input of phosphate to the oligotrophic water of the open Western Mediterranean Sea, Limnol. Oceanogr., 47, 856–869, 2002. Robinson, C., Serret, P., Tilstone, G., Teira, E., Zubkov, M. V., Rees, A. P. and Woodward, M. S.: Plankton respiration in the eastern Atlantic Ocean, Deep Sea Res. Pt.&nbsp;I, 49, 787–813, 2002. Rochelle-Newall, E., Winter, C., Barron, C., Borges, A. V., Duarte, C. M., Elliott, M., Frankignoulle, M., Gazeau, F., Middelburg, J. J., Pizay, M.-D., and Gattuso, J.-P.: Artificial neural network analysis of factors controlling ecosystem metabolism in coastal systems, Ecol. Appl., 17, S185–S196, 2007. Satta, M., Agusti, S., Mura, M., Vaqué, D., and Duarte, C. M.: Microplankton respiration and net community metabolism in a bay on the NW Mediterranean coast, Aquat. Microb. Ecol., 10, 165–172, 1996. Schumann, A. W. and Sumner, M. E.: Chemical evaluation of nutrient supply from fly ash – biosolids mixtures, Soil Sci. Soc. Am. J., 64, 419–426, 2000. Serret, P., Fernández, E., Sostres, J. A., and Anadón, R.: Seasonal compensation of microbial production and respiration in a temperate sea, Mar. Ecol. Prog. Ser., 187, 43–57, 1999. Serret, P., Robinson, C., Fernandez, E., Teira, E., and Tilstone, G.: Latitudinal variation of the balance between plankton photosynthesis and respiration in the eastern Atlantic Ocean, Limnol. Oceanogr., 46, 1642–1652, 2001. Sheldon, R. W., Rassoulzadegan, F., Azam, F., Berman, T., Bezanson, D. S., Bianchi, M., Bonin, D., Hagström, Å., Laval-Peuto, M., Neveux, J., Raimbault, P., Rivier, A., Sherr, B., Sherr, E., Van Wambeke, F., Wikner, J., Wood, A. M., and Yentsch, C. M.: Nano- and picoplankton growth and production in the Bay of Villefranche sur Mer (N. W. Mediterranean), Hydrobiologia, 241, 91–106, 1992. Sheldon, R. and Parsons, T.: A continuous size spectrum for particulate matter in the sea, J. Fish Res. Bd. Canada, 24, 909–915, 1967. Sherr, E. B. and Sherr, B. F.: Temporal offset in oceanic production and respiration processes implied by seasonal changes in atmospheric oxygen, Aquat. Microb. Ecol., 11, 91–100, 1996. Smith, D. C. and Azam, F.: A simple, economical method for measuring bacterial protein synthesis rates in seawater using <sup>3</sup>H-leucine, Mar. Microb. Food Webs, 6, 107–114, 1992. Smith, E. and Kemp, W.: Size structure and the production/respiration balance in a coastal plankton community, Limnol. Oceanogr. 46, 473–485, 2001. Strickland, J. D. H. and Parsons, T. R.: A practical handbook of seawater analysis, Bull. 167 Fish. Res. Bd., Canada, 1972. Tanaka, T., Rassoulzadegan, F., and Thingstad, T. F.: Orthophosphate uptake by heterotrophic bacteria, cyanobacteria, and autotrophic nanoflagellates in Villefranche Bay, northwestern Mediterranean: Vertical, seasonal, and short-term variations of the competitive relationship for phosphorus, Limnol. Oceanogr., 49, 1063–1072, 2004. Thingstad, T. F., Hagström, A., and Rassoulzadegan, F.: Accumulation of degradable DOC in surface waters: Is it caused by a malfunctioning microbial loop?, Limnol. Oceanogr., 42, 398–404, 1997. Thingstad, T. F., Zweifel, U. L., and Rassoulzadegan, F.: P limitation of heterotrophic bacteria and phytoplankton in the northwestern Mediterranean, Limnol. Oceanogr., 43, 88–94, 1998. Williams, P. L.: The balance of plankton respiration and photosynthesis in the open ocean, Nature, 394, 55–57, 1998. Williams, P. L. and Bowers, D.: Regional carbon imbalances in the ocean, Science, 284, 173–174, 1999. Williams, P. L., Morris, P., and Karl, D. M.: Net community production and metabolic balance at the oligotrophic ocean site, station ALOHA, Deep Sea Res. Pt.&nbsp;I, 51, 1563–1578, 2004. Zhang, R., Weinbauer, M. G., and Qian, P.-Y.: Viruses and flagellates sustain apparent richness and reduce biomass accumulation of bacterioplankton in coastal marine waters, Environ. Microbiol., 9, 2008–2018, 2007.