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Changes in Nutrient and Carbon Availability and Temperature as Factors Controlling Bacterial Growth in the Northern Baltic Sea

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Abstract

The effects of inorganic nutrient (N and P) and glucose C treatments on bacterial growth were followed for 3 days in natural surface and deep water bacterial samples during the main post-spring bloom stages of phytoplankton growth in the northern Baltic Sea. In addition, the importance of photochemical degradation of dissolved organic matter on bacterial growth was investigated vertically (0.1–2.0 m) and spatially, in a salinity gradient from river mouth to open sea. Bacterial production was consistently C limited in the surface layer, with N or both N and P as the secondary limiting nutrients from spring to early summer and in late summer, respectively. In deep water, bacterial growth showed combined temperature and C limitation, and in spring, this also appeared to be true with surface samples. The effect of 1-day sunlight pre-treatment varied from no effect up to a 44% production increase, with clear bacterial production responses only being seen at the surface (10 cm depth). The implications of bacterial C limitation for the structure and function of the surface plankton ecosystem, including its CO2 exchange with the atmosphere are discussed.

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References

  • Ameryk, A., B. Podgórska, and Z. Witek. 2005. The dependence between bacterial production and environmental conditions in the Gulf of Gdańsk. Oceanologia 47: 27–45.

    Google Scholar 

  • Autio, R. 1992. Temperature regulation of brackish water bacterioplankton. Archiv für Hydrobiologie Beiheft Ergebnisse der Limnologie 37: 253–263.

    Google Scholar 

  • Autio, R. 1998. Response of a seasonally cold-water bacterioplankton to temperature and substrate treatments. Estuarine, Coastal and Shelf Science 46: 465–474.

    Article  Google Scholar 

  • Babin, M., D. Stramski, G.M. Ferrari, H. Claustre, A. Bricaud, G. Obolensky, and N. Hoepffner. 2003. Variations in the light absorption coefficients of phytoplankton, nonalgal particles, and dissolved organic matter in coastal waters around Europe. Journal of Geophysical Research 108(C7): 3211–3230.

    Article  Google Scholar 

  • Benner, R., and B. Biddanda. 1998. Photochemical transformations of surface and deep marine dissolved organic matter: Effects on bacterial growth. Limnology and Oceanography 43: 1373–1378.

    CAS  Google Scholar 

  • Børsheim, K.Y., and G. Bratbak. 1987. Cell volume to cell carbon conversion factors for a bacterivorous Monas sp Enriched from seawater. Marine Ecology. Progress Series 36: 171–175.

    Article  Google Scholar 

  • Carlson, C.A., H.W. Ducklow, and A.F. Michaelis. 1994. Annual flux of dissolved organic carbon from the euphotic zone in the northwestern Sargasso Sea. Nature 371: 405–408.

    Article  CAS  Google Scholar 

  • Cotner, J.B., J.W. Ammerman, E.R. Peele, and E. Bentzen. 1997. Phosphorus-limited bacterioplankton growth in the Sargasso Sea. Aquatic Microbial Ecology 13: 141–149.

    Article  Google Scholar 

  • Elser, J., L.B. Stabler, and R.P. Hasset. 1995. Nutrient limitation of bacterial growth and rates of bacterivory in lakes and oceans: a comparative study. Aquatic Microbial Ecology 9: 105–110.

    Article  Google Scholar 

  • Emerson, S., P. Quay, C. Winn, L. Tupas, and M. Landry. 1997. Experimental determination of the organic carbon flux from open-ocean surface waters. Nature 389: 951–954.

    Article  CAS  Google Scholar 

  • Engbrodt, R., and G. Kattner. 2005. On the biogeochemistry of dissolved carbohydrates in the Greenland Sea (Arctic). Organic Geochemistry 36: 937–948.

    Article  CAS  Google Scholar 

  • Grasshoff, K. 1976. Methods of seawater analysis. Weinheim: Verlag Chemie.

    Google Scholar 

  • Guzmán, M.I., M.R. Hoffmann, and A.J. Colussi. 2007. Photolysis of pyruvic acid in ice: Possible relevance to CO and CO2 ice core record anomalies. Journal of Geophysical Research 112: D10123.

    Article  CAS  Google Scholar 

  • Haas, L.W. 1982. Improved epifluorescence microscopy for observing planktonic microorganisms. Annales de l’Institut oceÂanographique Paris 58: 261–266.

    Google Scholar 

  • Hobbie, J.E., R.J. Daley, and S. Jasper. 1977. Use of nucleopore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology 33: 1225–1228.

    CAS  Google Scholar 

  • Hu, C., F.E. Muller-Karger, and R.G. Zepp. 2002. Absorbance, absorption coefficient, and apparent quantum yield: A comment on common ambiguity in the use of these optical concepts. Limnology and Oceanography 47: 1261–1267.

    Google Scholar 

  • Jespersen, A.-M., and K. Christoffersen. 1987. Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Archiv für Hydrobiologie 109: 445–454.

    CAS  Google Scholar 

  • Jørgensen, N.O.G., L.J. Tranvik, and G. Mine Berg. 1999. Occurence and bacterial cycling of dissolved nitrogen in the Gulf of Riga, the Baltic Sea. Marine Ecology Progress Series 191: 1–18.

    Article  Google Scholar 

  • Kirchman, D.L., and J.H. Rich. 1997. Regulation of bacterial growth rates by dissolved organic carbon and temperature in the Equatorial Pacific Ocean. Microbial Ecology 33: 22–30.

    Article  Google Scholar 

  • Kirchman, D.L., R.R. Malmstrom, and M.T. Cottrell. 2005. Control of bacterial growth by temperature and organic matter in the western Arctic. Deep-Sea Research II 52: 3386–3395.

    Article  Google Scholar 

  • Kivi, K., S. Kaitala, H. Kuosa, J. Kuparinen, E. Leskinen, R. Lignell, B. Marcussen, and T. Tamminen. 1993. Nutrient limitation and grazing control of the Baltic plankton community during annual succession. Limnology and Oceanography 38: 893–905.

    Google Scholar 

  • Koopmans, D.J., and D.A. Bronk. 2002. Photochemical production of dissolved inorganic nitrogen and primary amines from dissolved organic nitrogen in waters of two estuaries and adjacent surficial groundwaters. Aquatic Microbial Ecology 26: 295–304.

    Article  Google Scholar 

  • Kuparinen, J., and A. Heinänen. 1993. Inorganic Nutrient and Carbon Controlled Bacterioplankton Growth in the Baltic Sea. Estuarine, Coastal and Shelf Science 37: 271–285.

    Article  CAS  Google Scholar 

  • Laanemets, J., K. Kononen, J. Pavelson, and E.-L. Poutanen. 2004. Vertical location of seasonal nutriclines in the western Gulf of Finland. Journal of Marine Systems 52: 1–13.

    Article  Google Scholar 

  • Lignell, R. 1990. Excretion of organic carbon by phytoplankton: its relation to algal biomass, primary productivity and bacterial secondary productivity in the Baltic Sea. Marine Ecology Progress Series 68: 85–99.

    Article  Google Scholar 

  • Lignell, R., S. Kaitala, and H. Kuosa. 1992. Factors controlling phyto- and bacterioplankton in late spring on a salinity gradient in the northern Baltic. Marine Ecology Progress Series 86: 273–281.

    Article  Google Scholar 

  • Lignell, R., J. Seppälä, P. Kuuppo, T. Tamminen, T. Andersen, and I. Gismervik. 2003. Beyond bulk properties: Responses of coastal summer plankton communities to nutrient enrichment in the northern Baltic Sea. Limnology and Oceanography 48: 189–209.

    Article  Google Scholar 

  • Lignell, R., L. Hoikkala, and T. Lahtinen. 2008. Effects of inorganic nutrients, glucose and solar radiation treatments on bacterial growth and exploitation of dissolved organic carbon and nitrogen in the northern Baltic Sea. Aquatic Microbial Ecology 51: 209–221.

    Article  Google Scholar 

  • Massana, R., J.M. Gasol, P.K. Bjørnsen, M. Blackburn, Å. Hagström, S. Hietanen, B.H. Hygum, J. Kuparinen, and C. Pedrós-Alió. 1997. Measurement of bacterial size via image analysis of epifluorescence preparations: Description of an inexpensive system and solutions to some of the most common problems. Scientia Marina 61: 397–407.

    Google Scholar 

  • Moran, M.A., and R.G. Zepp. 1997. Role of Photoreactions in the formation of biologically labile compounds from dissolved organic matter. Limnology and Oceanography 42: 1307–1316.

    Article  CAS  Google Scholar 

  • Myklestad, S.M., and K.Y. Børsheim. 2007. Dynamics of carbohydrates in the Norwegian Sea inferred from monthly profiles collected during 3 years at 66°N, 2°E. Marine Chemistry 107: 475–485.

    Article  CAS  Google Scholar 

  • Myklestad, S.M., E. Skånøy, and S. Hestmann. 1997. A sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater. Marine Chemistry 56: 279–286.

    Article  CAS  Google Scholar 

  • Nausch, M., and E. Kerstan. 2003. The relationship between dissolved carbohydrates and carbohydrate-degrading enzymes in the salinity gradient of the Pomeranian bight (southern Baltic). Oceanologia 45: 437–452.

    Google Scholar 

  • Niemi, Å. 1975. Ecology of phytoplankton in the Tvärminne area, SW coast of Finland. II. Primary production and environmental conditions in the archipelago and the sea zone. Acta Botanica Fennica 105: 1–73.

    Google Scholar 

  • Norland, S. 1993. The relationship between biomass and volume of bacteria. Handbook of Methods in Aquatic Microbial Ecology. Boca Raton: Lewis.

    Google Scholar 

  • Obernosterer, I., R. Sempéré, and G.J. Herndl. 2001. Ultraviolet radiation induces reversal of the bioavailability of DOM to marine bacterioplankton. Aquatic Microbial Ecology 24: 61–68.

    Article  Google Scholar 

  • Pakulski, J.D., and R. Benner. 1994. Abundance and distribution of carbohydrates in the ocean. Limnology and Oceanography 39: 930–940.

    Article  CAS  Google Scholar 

  • Pinhassi, J., L. Gómez-Consarnau, L. Alonso-Sáez, M.M. Sala, M. Vidal, C. Pedrós-Alió, and J.M. Gasol. 2006. Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquatic Microbial Ecology 44: 241–252.

    Article  Google Scholar 

  • Pomeroy, L.R., and W.J. Wiebe. 2001. Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquatic Microbial Ecology 23: 187–204.

    Article  Google Scholar 

  • Rich, J.H., H.W. Ducklow, and D.L. Kirchman. 1996. Concentrations and uptake of neutral monosaccharides along 140ºW in the equatorial Pacific: Contribution of glucose to heterotrophic bacterial activity and the DOM flux. Limnology and Oceanography 41: 595–604.

    CAS  Google Scholar 

  • Riemann, B., P.K. Bjørnsen, S. Newell, and R. Fallon. 1987. Calculation of cell production of coastal marine bacteria based on measured incorporation of [3H]thymidine. Limnology and Oceanography 32: 471–476.

    Article  CAS  Google Scholar 

  • Rivkin, R.B., and M.R. Anderson. 1997. Inorganic nutrient limitation of oceanic bacterioplankton. Limnology and Oceanography 42: 730–740.

    Article  CAS  Google Scholar 

  • Sala, M.M., F. Peters, J.M. Gasol, C. Pedrós-Alió, C. Marrasé, and D. Vaqué. 2002. Seasonal and spatial variations in the nutrient limitation of bacterioplankton growth in the northwestern Mediterranean. Aquatic Microbial Ecology 27: 47–56.

    Article  Google Scholar 

  • Siegenthaler, U., and J.L. Sarmiento. 1993. Atmospheric carbon dioxide and the ocean. Nature 365: 119–125.

    Article  CAS  Google Scholar 

  • Skoog, A., B. Biddanda, and R. Benner. 1999. Bacterial utilization of dissolved glucose in the upper water column of the Gulf of Mexico. Limnology and Oceanography 44: 1625–1633.

    Article  CAS  Google Scholar 

  • Smith, E.M., and R. Benner. 2005. Photochemical transformations of riverine dissolved organic matter: effects on estuarine bacterial metabolism and nutrient demand. Aquatic Microbial Ecology 40: 37–50.

    Article  Google Scholar 

  • Søndergaard, M., P.J.le B. Williams, G. Cauwet, B. Riemann, C. Robinson, S. Terzic, E.M.S. Woodward, and J. Worm. 2000. Net accumulation and flux of dissolved organic carbon and dissolved organic nitrogen in marine planktonic communities. Limnology and Oceanography 45: 1097–1111.

    Article  Google Scholar 

  • Thingstad, T.F., and R. Lignell. 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquatic Microbial Ecology 13: 19–27.

    Article  Google Scholar 

  • Thingstad, T.F., E.F. Skjoldal, and R.A. Bohne. 1993. Phosphorus cycling and algal–bacterial competition in Sandsfjord, western Norway. Marine Ecology Progress Series 99: 239–259.

    Article  CAS  Google Scholar 

  • Thingstad, T.F., Å. Hagström, and F. Rassoulzadegan. 1997. Accumulation of degradable DOC in surface waters: Is it caused by a malfunctioning microbial loop? Limnology and Oceanography 42(2): 398–404.

    Article  CAS  Google Scholar 

  • Thingstad, T.F., U.L. Zweifel, and F. Rassoulzadegan. 1998. P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnology and Oceanography 43: 88–94.

    Article  CAS  Google Scholar 

  • Thingstad, T.F., H. Havskum, H. Kaas, T.G. Nielsen, B. Riemann, D. Lefevre, and P.J.le B. Williams. 1999. Bacteria–protist interactions and organic matter degradation under P-limited conditions: Analysis of an enclosure experiment using a simple model. Limnology and Oceanography 44: 62–79.

    Article  CAS  Google Scholar 

  • Thingstad, T.F., H. Havskum, U.L. Zweifel, E. Berdalet, M.M. Sala, F. Peters, M. Alcaraz, R. Scharek, M. Perez, S. Jacquet, G.A.F. Flaten, J.R. Dolan, C. Marrasé, F. Rassoulzadegan, Å. Hagstrøm, and D. Vaulot. 2007. Ability of a “minimum” microbial food web model to reproduce response patterns observed in mesocosms manipulated with N and P, glucose, and Si. Journal of Marine Systems 64: 15–34.

    Article  Google Scholar 

  • Thingstad, T.F., R.G.J. Bellerby, G. Bratbak, K.Y. Borsheim, J.K. Egge, M. Heldal, A. Larsen, C. Neill, J. Nejstgaard, S. Norland, R.A. Sandaa, E.F. Skjoldal, T. Tanaka, R. Thyrhaug, and B. Topper. 2008. Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455(7211): 387–390.

    Article  CAS  Google Scholar 

  • Utermöhl, H. 1958. Zur Vervollkommung der quantitativen Phytoplanktonmethodik. Mitteilungen der International Vereinigung fur Theoretische and Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Vähätalo, A.V., and R.G. Zepp. 2005. Photochemical mineralization of dissolved organic nitrogen to ammonium in the Baltic sea. Environmental Science and Technology 39: 6985–6992.

    Article  CAS  Google Scholar 

  • Vähätalo, A., K. Salonen, U. Münster, M. Järvinen, and R.G. Wetzel. 2003. Photochemical transformation of allochtonous organic matter provides bioavailable nutrients in a humic lake. Archiv für Hydrobiologie 156: 287–314.

    Article  CAS  Google Scholar 

  • Williams, P.J.le B. 1995. Evidence for the seasonal accumulation of carbon-rich dissolved organic material, its scale in comparison with changes in particulate material and the consequential effect on net C/N assimilation ratios. Marine Chemistry 51: 17–29.

    Article  CAS  Google Scholar 

  • Zweifel, U.L. 1999. Factors controlling accumulation of labile dissolved organic carbon in the Gulf of Riga. Estuarine, Coastal and Shelf Science 48: 357–370.

    Article  CAS  Google Scholar 

  • Zweifel, U.L., B. Norrman, and Å. Hagström. 1993. Consumption of dissolved organic carbon by marine bacteria and demands for inorganic nutrients. Marine Ecology Progress Series 101: 23–32.

    Article  CAS  Google Scholar 

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Acknowledgements

K. Kivi is acknowledged for counting phyto- and zooplankton samples. V. Norros and the Tvärminne staff, especially E. Salminen, M. Sjöblom and T. Sjölund, are thanked for their valuable contribution during sampling and laboratory work. This investigation was funded by the Walter and Andrée de Nottbeck Foundation, the Academy of Finland and EU project DANLIM (EVK3-2001-00049).

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Correspondence to Laura Hoikkala.

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Hoikkala, L., Aarnos, H. & Lignell, R. Changes in Nutrient and Carbon Availability and Temperature as Factors Controlling Bacterial Growth in the Northern Baltic Sea. Estuaries and Coasts 32, 720–733 (2009). https://doi.org/10.1007/s12237-009-9154-z

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  • DOI: https://doi.org/10.1007/s12237-009-9154-z

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