BG Biogeosciences BG 1726-4189 Copernicus GmbH Göttingen, Germany 10.5194/bg-7-1701-2010 Response of heterotrophic and autotrophic microbial plankton to inorganic and organic inputs along a latitudinal transect in the Atlantic Ocean Martínez-García S. 1 Fernández E. 1 Calvo-Díaz A. 2 3 Marañón E. 1 Morán X. A. G. 2 Teira E. 1 Departamento Ecoloxía e Bioloxía Animal, Universidade de Vigo, Campus Lagoas-Marcosende 36310 Vigo, Spain Instituto Español de Oceanografía, Centro Oceanográfico de Xixón, Camín de L'Arbeyal s/n, 33212 Xixón, Spain Present address: Department of Biological Oceanography, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB Den Burg, The Netherlands; and Department of Marine Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria 25 05 2010 7 5 1701 1713 This is an open-access article ditributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. This article is available from http://www.biogeosciences.net/7/1701/2010/bg-7-1701-2010.html The full text article is available as a PDF file from http://www.biogeosciences.net/7/1701/2010/bg-7-1701-2010.pdf

The effects of inorganic and/or organic nutrient inputs on phytoplankton and heterotrophic bacteria have never been concurrently assessed in open ocean oligotrophic communities over a wide spatial gradient. We studied the effects of potentially limiting inorganic (nitrate, ammonium, phosphate, silica) and organic nutrient (glucose, aminoacids) inputs added separately as well as jointly, on microbial plankton biomass, community structure and metabolism in five microcosm experiments conducted along a latitudinal transect in the Atlantic Ocean (from 26° N to 29° S). <br><br> Primary production rates increased up to 1.8-fold. Bacterial respiration and microbial community respiration increased up to 14.3 and 12.7-fold respectively. Bacterial production and bacterial growth efficiency increased up to 58.8-fold and 2.5-fold respectively. The largest increases were measured after mixed inorganic-organic nutrients additions. Changes in microbial plankton biomass were small as compared with those in metabolic rates. A north to south increase in the response of heterotrophic bacteria was observed, which could be related to a latitudinal gradient in phosphorus availability. Our results suggest that organic matter inputs will result in a predominantly heterotrophic versus autotrophic response and in increases in bacterial growth efficiency, particularly in the southern hemisphere. Subtle differences in the initial environmental and biological conditions are likely to result in differential microbial responses to inorganic and organic matter inputs.

 References Agawin, N. S. R., Duarte, C. M., and Agustí, S.: Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production, Limnol. Oceanogr., 45, 591–600, 2000. Ammerman, J. W., Hood, R. R., Case, D. A., and Cotner, J. B.: Phosphorous deficiency in the Atlantic: An emerging paradigm in oceanography, Eco Trans AGU 84, 165–170, 2003. Alonso-Sáez, L., Gasol, J. M., Arístegui, J., Vilas, J. C., Vaqué, D., Duarte, C. M., and Agustí, S.: Large-scale variability in surface bacterial carbon demandand growth efficiency in the subtropical northeast Atlantic Ocean, Limnol. Oceanogr., 52, 533–546, 2007. Arrigo, K. R.: Marine microorganisms and global nutrientcycles, Nature, 437, 349–355, 2005. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Rail, L. A., and Thingstad, F.: The ecological role of water-column microbes in the sea, Mar. Ecol. Prog.-Ser., 10, 257–263, 1983. Baker, A. R., Weston, K., Kelly, S. D., Voss, M., Streu, P, and Cape, J. N.: Dry and wet deposition of nutrients from the tropical Atlantic atmosphere: Links to primary productivity and nitrogen fixation, Deep-Sea Res. Pt I, 54, 1704–1720, 2007. Bonnet, S., Guieu, C., Chiaverini, J., Ras, J., and Stock, A.: Effect of atmospheric nutrients on the autotrophic communities in a low nutrient, low chlorophyll syatem, Limnol. Oceanogr., 50, 1810–1819, 2005. Calvo-Díaz, A. and Morán, X. A. G.: Seasonal dynamics of picoplankton in shelf waters of the southern Bay of Biscay, Aquat. Microb. Ecol., 42, 159–174, 2006. Calvo-Díaz, A. and Morán, X. A. G.: Empirical leucine-to-carbon conversión factors for estimating heterotrophic bacterial production: seasonality and predictability in a temperate coastal ecosystem, Appl. Environ. Microbiol., 75, 3216–3221, 2009. Carlson, C. A., Giovannoni, S. J., Hansell, D. A., Goldberg, S. J., Parsons, R., Otero, M. P., Vergin, K., and Wheeler, B. R.: Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea, Aquat. Microb. Ecol., 30, 19–36, 2002. Caron, D. A., Lim, E. L., Sanders, R. W., Dennett, M. R., and Berninger, U. G.: Responses of bacterioplankton and phytoplankton to organic carbon and inorganic nutrient additions in contrasting oceanic ecosystems, Aquat. Microb. Ecol., 22, 176–184, 2000. Cermeño, P., Marañón, E., Rodríguez, J., and Fernández, E.: Large-sized phytoplankton sustain higher carbon-specific photosynthesis than smaller cells in a coastal eutrophic ecosystem, Mar. Ecol. Prog.-Ser., 297, 51–60, 2005. Church, M. J., Hutchins, D. A., and Ducklow, H. W.: Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean, Appl. Environ. Microbiol., 66, 455–466, 2000. Church, M. J.: Resource control of bacterial dynamics in the sea, in: Microbial Ecology of theOceans (2nd edition), edited by: Kirchman, D. L., Wiley-Liss, New York, 335–382, 2008.. Cornell, S., Rendell, A,, and Jickells, T.: Atmospheric inputs of dissolved organic nitrogen to the oceans, Nature, 376, 243–246, 1995. Cotner, J. B. and Biddanda, B. A.: Small players, large role: Microbial influence on biogeochemical processes in pelagic aquatic ecosystems, Ecosystems, 5, 105–121, 2002. Cullen, J. J., Yang, X., and Macintyre, H. L.: Nutrient limitation of marine photosynthesis, in: Primary Productivity and Biogeochemical Cycles in the Sea, edited by: Falkowski, P. G. and Woodhead, A., Plenum, New York, 69–88, 1992. Davey, M., Tarran, G. A., Mills, M. M., Ridame, C., Geider, R. J., and LaRoche, J.: Nutrient limitation of picophytoplankton photosynthesis and growth in the tropical North Atlantic, Limnol. Oceanogr., 53, 1722–1733, 2008. Davidson, K., Gilpin, L. C., Hart, M. C., Foilland, E., Mitchell, E., Álvarez-Calleja, I., Laurent, C., Miller, A. E. J., and Leakey, J. G.: The influence of the balance of inorganic and organic nitrogen on the trophic dynamics of microbial food webs, Limnol. Oceanogr., 52, 2147–2163, 2007. del Giorgio, P. A. and Cole, J. J.: Bacterial energetics and growth efficiency, in: MicrobialEcology of the Oceans (1st edition), edited by: Kirchman, D. L., Wiley-Liss, New York, 289–326, 2000. Dentener, F., Drevet, J., Lamarque, J. F., Bey, I., Eickhout, B., Fiore, A. M., Hauglustaine, D., Horowitz, L. W., Krol, M., Kulshrestha, U. C., Lawrence, M., Galy-Lacaux, C., Rast, S., Shindell,D., Stevenson, D., Van Noije, T., Atherton, C., Bell, N., Bergman, D., Butler, T., Cofala, J., Collins, B., Doherty, R., Ellingsen, K., Galloway, J., Gauss, M., Montanaro, V., Müller, F., Pitari, G., Rodriguez, J., Sanderson, M.,. Solmon, F., Strahan, S., Schultz, M., Sudo, K., Szopa, S., and Wild, O.: Nitrogen and sulfur deposition on regional scales: a multimodelevaluation, Global Biogeochem. Cy., 20, GB4003, doi:10.1029/2005GB002672, 2006. Duce, R. A., LaRoche, J., Altieri, K., Arrigo, K. R., Baker, A. R., Capone, D. G., Cornell, S., Dentener, F., Galloway, J., Ganeshram, R. S., Geider, R. J., Jickells, T., Kuypers, M. M., Langlois, R., Liss, P. S., Liu, S. M., Middelburg, J. J., Moore, C. M., Nickovic, S., Oschlies, A., Pedersen, T., Prospero, J., Schlitzer, R., Seitzinger, S., Sorensen, L. L., Uematsu, M., Ulloa, O., Voss, M., Ward, B., and Zamora, L.: Impacts of atmospheric anthropogenic nitrogen on the open ocean, Science, 320, 893–897, 2008. Ducklow, H.: Bacterial production and biomass in the oceans, in: Microbial Ecology of theOceans (1st edition), edited by: Kirchman, D. L., Wiley-Liss, New York, 85–120, 2000. Falkowski, P. G.: Evolution of the nitrogen cycle and its influence on the biological sequestration of CO<sub>2</sub> in the ocean, Nature, 387, 272–275, 1997. Fanning, K. A.: Nutrient provinces in the Sea: Concentration Ratios, Reaction Rate Ratios, and Ideal Covariation, J. Geophys. Res., 97, 5693–5712, 1992. Faul, F., Erdfelder, E., Lang, A. G., and Buchner, A.: G*Power 3: A flexible statistical power analysis for the social, behavioural, and biomedical sciences, Behav. Res. Methods, 39, 175–191, 2007. Gasol, J. M. and del Giorgio, P. A.: Using flow citometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities, Sci. Mar., 64, 197–224, 2000. Gasol, J. M., Vázquez-Dominguez, E., Vaqué, D., Agustí, S., and Duarte, C. M.: Bacterial activity and diffusive nutrient supply in the oligotrophic Central Atlantic Ocean, Aquat. Microb. Ecol., 56, 1–12, 2009. Graziano, L. M., Geider, R. J., Li, W. K. W., and Olaizola, M.: Nitrogen limitation of North Atlantic phytoplankton: Analysis of physiological condition in nutrient enrichment experiments, Aquat. Microb. Ecol., 11, 53–64, 1996. Gundersen, K., Heldal, M., Norland, S., Purdie, D. A., and Knap, A. N.: Elemental C, N, and P cell content of individual bacteria collected at the Bermuda Atlantic Time-series Study (BATS) site, Limnol. Oceanogr., 47, 1525–1530, 2002. Herut, B., Zohary, T., Krom, M. D., Mantourad, R. F. C., Pitta, P., Psarra, S., Rassoulzadeganf, F., Tanaka, T., and Thingstadg, T. F.: Response of Mediterranean surface water to Saharan dust: On-board microcosm experiment and field observations, Deep-Sea Res. Pt II, 52, 3024–3040, 2005. Jacquet, S., Havskum, H., Thingstad, T. F., and Vaulot, D.: Effects of inorganic and organic nutrient addition on a coastal microbial community (Isefjord, Denmark), Mar. Ecol. Prog.-Ser., 228, 3–14, 2002. Joint, I., Henriksen, P., Fonnes, G. A., Bourne, D., Thingstad, T. F., and Riemann, B.: Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms, Aquat. Microb. Ecol., 29, 145–159, 2002. Jurado, E., Dachs, J., Duarte, C. M., and Simó, R.: Atmospheric deposition of organic and black carbon to the global oceans, Atmos. Environ., 4, 7931–7939, 2008. Jürgens, K. and Massana, R.: Protistan grazing on marine bacterioplankton, in: Microbial Ecology of the Oceans (2nd edition), edited by: Kirchman, D. L., Wiley-Liss, New York, 383–441, 2008. Kerouel, R. and Aminot, A. Fluorometric determination of ammonia in sea and estuarine waters by direct segmented flow analysis, Mar. Chem., 57, 265–275, 1997. Kirchman, D., K'nees, E., and Hodson, R.: Leucine incorporation and its potential as a mesure of protein synthesis by bacteria in natural aquatic systems, Appl. Environ. Microbiol., 49, 599–607, 1985. Lignell, R., Seppälä, J., Kuuppo, P., Tamminen, T., Andersen, T.,and Gismervik, I.: Beyond bulk properties: Responses of coastal summer plankton communities to nutrient enrichment in the northern Baltic Sea, Limnol. Oceanogr., 48, 189–209, 2003. Mace, K. A., Kubilay, N., and Duce, R. A.: Organic nitrogen in rain and aerosol in the easternMediterranean atmosphere: An association with atmospheric dust, J. Geophys. Res.-Atmos., 108, 4320, doi:10.1029/2002JD002997, 2003. Marañón, E., Holligan, P. M., Barciela, R., González, N., Mouriño, B., Pazó, M. J., and Varela, M.: Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments, Mar. Ecol. Prog.-Ser., 216, 43–56, 2001. Marañón, E., Behrenfeld, M. J., Gonzalez, N., Mourino, B., and Zubkov, M. V.: High variability of primary production in oligotrophic waters of the Atlantic Ocean: uncoupling from phytoplankton biomass and size structure, Mar. Ecol. Prog.-Ser., 257, 1–11, 2003. Marañón, E., Fernández, A., Huete-Ortega, M., Mouriño-Carballido, B., Cermeño, P., Chouciño, P., Martínez-García, S., Teira, E., Fernández, E., Calvo-Díaz, A., Morán, X. A. G., Bode, A., Moreno-Ostos, E., Varela, M. M., Patey, M., and Achterberg, E. P.: The degree of oligotrophy controls the response of microbial plankton to saharan dust, submitted to Limnol. Oceangr., 2010. Martínez-García, S., Fernández, E., Aranguren-Gassis, M., and Teira, E.: In vivo electron transport system activity: a method to estimate respiration in marine microbial planktonic communities, Limnol Oceanogr.-Meth., 7, 459–469, 2009. Mather, R. L., Reynolds, S. E., Wolff, G. A., Williams, R. G., Torres-Valdés, S., Woodward, E. M. S., Landolfi, A., Pan, X., Sanders, R., and Achterberg, E. P.: Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres, Nat. Geosci., 1, 439–443, 2008. Mills, M. M., Ridame, C., Davey, M., La Roche, J., and Geider, R. J.: Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic, Nature, 429, 292–294, 2004. Mills, M. M., Moore, C. M., Langlois, R., Milne, A., Achterberg, E., Nachtigall, K., Lochte, K., Geider, R. J., and La Roche, J.: Nitrogen and phosphorus co-limitation of bacterial productivity and growth in the oligotrophic subtropical North Atlantic, Limnol. Oceanogr., 53, 824–834, 2008. Moore, C. M., Mills, M. M., Milnes, A., Langlois, R., Achterberg, E. P., Lochte, K., Geider, R. J., and LaRoche, J.: Iron limits primary productivity during spring bloom development in the central North Atlantic, Glob. Change Biol., 12, 626–634, 2006. Moore, C. M., Mills, M. M., Langlois, R., Milne, A., Achterberg, E. P., La Roche, J., and Geider, R. J.: Relative influence of nitrogen and phosphorus availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical North Atlantic Ocean, Limnol. Oceanogr., 53, 291–305, 2008. Morán, X. A. G., Fernández, E., and Pérez, V.: Size-fractionated primary production, bacterial production and net community production in subtropical and tropical domains of the oligotrophic NE Atlantic in autumn, Mar. Ecol. Prog.-Ser., 274, 17–29, 2004. Norland, S., Fagerbakke, K. M., and Heldal, M.: Light Element Analysis of Individula Bacteria by X-ray Microanalysis, Appl. Environ. Microbiol., 61, 1357–1362, 1995. Paerl, H. W.: Coastal eutrophication and harmful algal blooms: Importance of atmospheric deposition and groundwater as "new" nitrogen and other nutrient sources, Limnol. Oceanogr., 42, 1154–1165, 1997. Partensky, F., Hess, W. R., and Vaulot, D.: Prochlorococcus, a marine photosynthetic prokaryote of global significance, Microbial Molecular Biology Reviews 63, 106–127, 1999. Paytan, A., Mackey, K. R. M., Cheng, Y., Lima, I. D., Doney, S. C., Mahowald, N., Labiosa, R., and Post, A. F.: Toxicity of atmospheric aerosols on marine phytoplankton. Proceedings of the National Academy of Sciences of the United States of America 106, 4601–4605, 2009. Peierls, B. L. and Paerl, H. W.: Bioavailability of atmospheric organic nitrogen deposition to coastal phytoplankton, Limnol. Oceanogr., 42, 1819–1823, 1997. Pomeroy, R., Sheldon, J. E., Sheldon, W. M., and Peters, F.: Limits to growth and respiration of bacterioplankton in the Gulf of Mexico, Mar. Ecol. Prog.-Ser., 117, 259–268, 1995. Pulido-Villena, E., Wagener, T., and Guieu, C.: Bacterial response to dust pulses in theWesternMediterranean: implications for carbon cycling in the oligotrophic ocean, Global Biogeochem. Cy., 22, GB1020, doi:10.1029/2007GB003091, 2008. Raimbault, P., Slawyk, G., Coste, B., and Fry, J.: Feasibility of Using an Automated Colorimetric Procedure for the Determination of Seawater Nitrate in the 0 to 100 nm Range – Examples from Field and Culture, Mar. Biol., 104, 347–351, 1990. Reche, I., Ortega-Retuerta, E., Romera, O., Pulido-Villena, E., Morales-Baquero, R., and Casamayor, E.: Effect of Saharan dust inputs on bacterial activity and community composition in Mediterranean lakes and reservoirs, Limnol. Oceanogr., 54, 869–879, 2009. Rivkin, R. B. and Anderson, M. R.: Inorganic nutrient limitation of oceanic bacterioplankton, Limnol. Oceanogr., 42, 730–740, 1997. Robinson, C.: Heterotrophic bacterial respiration, in: Microbial Ecology of the Oceans (2nd edition), edited by: Kirchman, D. L., Wiley-Liss, New York, 299–336, 2008. Saito, M. A., Goepfert, T. J., and Ritt, J. T.: Some thoughts on the concept of colimitation: Three definitions and the importance of bioavailability, Limnol. Oceanogr., 53, 276–290, 2008. Scheiner, S. M. and Gurevitch, J.: Design and analysis of ecological experiments, Chapman and Hall, London, 1993. Seitzinger, S. P. and Sanders, R. W.: Atmospheric inputs of dissolved organic nitrogen stimulate estuarine bacteria and phytoplankton, Limnol. Oceanogr., 44, 721–730, 1999. Smith, D. C. and Azam, F.: A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine, Mar. Microb. Food Webs, 6, 107–114, 1992. Tanaka, T., Thingstad, T. F., Gasol, J. M., Cardel\'us, C., Jezberra, J., Sala, M. M., Simek, K., and Unrein, F.: Determining the availability of phosphate and glucose for bacteria in P-limited mesocosms of NW Mediterranean surface waters, Aquat. Microb. Ecol., 56, 81–91, 2009. Thingstad, T. F. and Sakshaug, E.: Control of phytoplankton growth in nutrient recycling ecosystems. Theory and terminology, Mar. Ecol. Prog.-Ser., 63, 261–272, 1990. Thingstad, T. F. and Rassoulzadegan, F.: Nutrient limitations, microbial food webs, and "biological C-pumps": suggested interactions in a P-limited Mediterranean, Mar. Ecol. Prog.-Ser., 117, 299–306, 1995. 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. Tréguer, P. and Le Corre, P.: Manuel d'analyse des sels nutritifs dans l'eau de mer. Utilisation de l'auto analyseur II, Technicon. L.O.C. Univ. Bretagne Occidentale, Brest, 1975. Tyrrell, T.: The relative influences of nitrogen and phosphorus on oceanic primary production, Nature, 400, 525–531, 1999. Van Wambeke, F., Obernosterer, I., Moutin, T., Duhamel, S., Ulloa, O., and Claustre, H.: Heterotrophic bacterial production in the eastern South Pacific: longitudinal trends and coupling with primary production, Biogeosciences, 5, 157–169, doi:10.5194/bg-5-157-2008, 2008. Weisse, T., and Scheffel-Möser, U.: Un coupling the microbial loop: grow and grazing loss rates of bacteria and heterotrophic nanoflagellates in the North Atlantic, Mar. Ecol. Prog.-Ser., 71, 195–205, 1991. Williams, P. J. leB., and del Giorgio, P. A.: Respiration in aquatic ecosystems: history andbackground, in: Respiration in aquatic ecosystems, edited by: del Giorgio, P. A. and Williams P. J. leB., Oxford University Press, London, 1–18, 2005. Worden, A. Z., Nolan, J. K., and Palenik, B.: Assessing the dynamics and ecology of marine picophytoplamkton: The importance of the eukaryotic component, Limnol. Oceanogr., 49, 168–179, 2009. Wu, J., Sunda, W., Boyle, E. A., and Karl, D. M.: Phosphate depletion in Western Atlantic Ocean, Science, 289, 759–762, 2000. Zubkov, M. V., Sleigh, M. A., Tarran, G. A., Burkill, P. H., and Leakey, R. J. G.: Picoplanktonic community structure on an Atlantic transect from 50° N to 50° S, Deep-Sea Res. Pt I, 45, 1339–1355, 1998. Zubkov, M. V., Sleigh, M. A., Burkill, P. H., and Leakey, R. J. G.: Bacterial growth and grazing loss in contrasting areas of North and South Atlantic, J. Plankton Res., 22, 685–711, 2000. Zweifel, U. L., Norrman, B., and Hagström, A.: Consumption of dissolved organic carbon by marine bacteria and demand for inorganic nutrients, Mar. Ecol. Prog.-Ser., 101, 23–32, 1993.