Dissolved Organic Matter in Lacustrine Ecosystems pp 107-114 | Cite as
Allochthonous dissolved organic matter as an energy source for pelagic bacteria and the concept of the microbial loop
Abstract
Substantial evidence exists that allochthonous dissolved organic matter (DOM) can provide an important carbon source for pelagic bacteria. On the other hand, it is implicit in the concept of the ‘microbial loop’ that the degradation of recalcitrant, allochthonous DOM should be retarded in the pelagic environment, as bacteria able to utilize recalcitrant DOM compounds for slow growth would be outcompeted by faster-growing bacteria utilizing more labile DOM compounds. Several possible solutions of this apparent paradox are suggested in this paper, including formation of labile DOM from recalcitrant DOM by e.g. photochemical reactions, and mechanisms enabling the maintenance of a metabolically diverse bacterioplankton. These mechanisms include an explanation analogous to Hutchinson’s classical solution to the ‘paradox of plankton’, and differential mortality of different populations within the bacterioplankton enabled by selective grazing, infections by bacteriophages and predatory bacteria, and spatial micropatchiness.
Key words
allochthonous DOM recalcitrant DOM bacterioplankton microbial loopPreview
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References
- Andersson, A., U. Larsson & Å. Hagström, 1986. Size-selective grazing by a microflagellate on pelagic bacteria. Mar. Ecol. Prog. Ser. 33: 51–57.CrossRefGoogle Scholar
- Azam, F. & B. C. Cho, 1987. Bacterial utilization of organic matter in the sea. In M. Fletcher, T. R. G. Gray & J. G. Jones (eds), Ecology of microbial Communities. Cambridge University Press, Cambridge: 261–281.Google Scholar
- Azam, F., T. Fenchel, F. G. Field, J. S. Gray, L.-A. Meyer-Reil & F. Thingstad, 1983. The ecological role of watercolumn microbes in the sea. Mar. Ecol. Prog. Ser. 10: 257–263.CrossRefGoogle Scholar
- Bergh, Ö., K. Y. Börsheim, G. Bratbak & M. Heldal, 1989. High abundance of viruses found in aquatic environments. Nature 340: 467–468.PubMedCrossRefGoogle Scholar
- Bloem, J., M. Starink, M.-J. B. Bär-Gilissen & T. E. Cappenberg, 1988. Protozoan grazing, bacterial activity, and mineralization in two-stage continuous cultures. Appl. envir. Microbiol. 54: 3113–3121.Google Scholar
- Bloem, J., F. M. Ellenbroek, M.-J. B. Bär-Gilissen & T. E. Cappenberg, 1989. Protozoan grazing and bacterial production in stratified lake Vechten estimated with fluorescently labeled bacteria and by thymidine incorporation. Appl. envir. Microbiol. 55: 1787–1795.Google Scholar
- Bosselmann, S. & B. Riemann, 1986. Zooplankton. In B. Riemann & M. Søndergaard (eds), Carbon Dynamics in eutrophic, temperate Lakes. Elsevier: 199–236.Google Scholar
- Börsheim, K. Y., 1984. Clearance rates of bacteria-sized particles by freshwater ciliates, measured with monodisperse fluorescent latex beads. Oecologia 63: 286–288.CrossRefGoogle Scholar
- Caron, D. A., P. G. Davis, L. P. Madin & J. McN. Sieburth, 1982. Heterotrophic bacteria and bacterivorous protozoa in oceanic macro aggregates. Science 218: 795–797.PubMedCrossRefGoogle Scholar
- De Haan, H., 1977. Effect of benzoate on microbial decomposition of fulvic acids in Tjeukemeer (The Netherlands). Limnol. Oceanogr. 22: 38–44.CrossRefGoogle Scholar
- Fenchel, T., 1982. Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol. Prog. Ser. 9: 35–42.CrossRefGoogle Scholar
- Fenchel, T., 1986. Ecology of protozoa. The biology of free-living phagotrophic protists. Brock/Springer Series in Contemporary Bioscience. Springer-Verlag, Berlin.Google Scholar
- Fenchel, T., 1988. Marine plankton food chains. Ann. Rev. Ecol. Syst. 19: 19–38.CrossRefGoogle Scholar
- Fuhrman, J. A. & F. Azam, 1980. Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Appl. envir. Microbiol. 39: 1085–1095.Google Scholar
- Fuhrman, J. A. & F. Azam, 1982. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: Evaluation and field results. Mar. Biol. 66: 109–120.CrossRefGoogle Scholar
- Gast, V., 1985. Bacteria as a food source for microzooplankton in the Schlei Fjord and Baltic Sea with special reference to ciliates. Mar. Ecol. Prog. Ser. 22: 107–120.CrossRefGoogle Scholar
- Giovannoni, S. J., T. B. Britschgi, C. L. Moyer & K. G. Field, 1990. Genetic diversity of Sargasso Sea bacterioplankton. Nature 345: 60–63.PubMedCrossRefGoogle Scholar
- Goldman, J. C., 1984. Conceptual role for micro aggregates in pelagic waters. Bull. mar. Sci. 35: 462–476.Google Scholar
- Gonzalez, J. M., E. B. Sherr & B. F. Sherr, 1990. Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. envir. Microbiol. 56: 583–589.Google Scholar
- Güde, H., 1986. Loss processes influencing growth of planktonic bacterial populations in Lake Constance. J. Plankton Res. 8: 795–810.CrossRefGoogle Scholar
- Hagström, Å., U. Larsson, P. Hörstedt & S. Normark, 1979. Frequency of dividing cells, a new approach to the determination of bacterial growth rates in aquatic environments. Appl. envir. Microbiol. 37: 805–812.Google Scholar
- Hessen, D. O., 1985. The relation between bacterial carbon and dissolved humic compounds in oligotrophic lakes. FEMS Microbial. Ecol. 31: 215–223.CrossRefGoogle Scholar
- Hessen, D. O., T. Andersen & A. Lyche, 1990. Carbon metabolism in a humic lake; pool sizes and cycling through Zooplankton. Limnol. Oceanogr. 35: 84–99.CrossRefGoogle Scholar
- Hobbie, J. E., 1988. A comparison of the ecology of planktonic bacteria in fresh and salt water. Limnol. Oceanogr. 33: 750–764.CrossRefGoogle Scholar
- Horvath, R. S., 1972. Microbial co-metabolism and the degradation of organic compounds in nature. Bact. Rev. 36: 146–155.PubMedGoogle Scholar
- Hutchinson, G. E., 1961. The paradox of plankton. Am. Nat. 95: 137–145.CrossRefGoogle Scholar
- Höfle, M. G., 1990. RNA chemotaxonomy of bacterial isolates and natural microbial communities. In J. Overbeck & R. J. Chróst (eds), Aquatic microbial Ecology -biochemical and molecular Approaches. Brock/Springer Series in Contemporary Bioscience. Springer-Verlag, Berlin: 129–159.Google Scholar
- Jones, R. I. & K. Salonen, 1985. The importance of bacterial utilization of released phytoplankton photosynthate in two humic forest lakes in southern Finland. Holarct. Ecol. 8: 133–140.Google Scholar
- Kepkay, P. E. & B. D. Johnson, 1989. Coagulation on bubbles allows microbial respiration of oceanic dissolved organic carbon. Nature 338: 63–65.CrossRefGoogle Scholar
- Larsson, U. & Å. Hagström, 1979. Phytoplankton exudate release as an energy source for the growth of pelagic bacteria. Mar. Biol. 52: 199–206.CrossRefGoogle Scholar
- McManus, G. B. & J. A. Fuhrman, 1986. Bacterivory in sea water studied with the use of inert fluorescent particles. Limnol. Oceanogr. 31: 420–426.CrossRefGoogle Scholar
- Mitchell, G. C., J. H. Baker & M. A. Sleigh, 1988. Feeding of a freshwater flagellate, Bodo saltans, on diverse bacteria. J. Protozool. 35: 219–222.Google Scholar
- Mitchell, J. G., A. Okubo & J. A. Fuhrman, 1985. Microzones surrounding phytoplankton form the basis for a stratified marine microbial ecosystem. Nature 316: 58–59.CrossRefGoogle Scholar
- Moaledj, K., 1978. Qualitative analysis of an oligocarbophilic aquatic microflora in the Plussee. Arch. Hydrobiol. 82: 98–113.Google Scholar
- Mopper, K., X. Zhou, R. J. Kieber, D. J. Kieber, R. J. Sikorski & R. D. Jones, 1991. Photochemical degradation of dissolved organic carbon and its impact on the oceanic carbon cycle. Nature 353: 60–62.CrossRefGoogle Scholar
- Nygaard, K., K. Y. Börsheim & T. F. Thingstad, 1988. Grazing rates on bacteria by marine heterotrophic microflagellates compared to uptake rates of bacterial-sized monodisperse fluorescent latex beads. Mar. Ecol. Prog. Ser. 44: 159–165.CrossRefGoogle Scholar
- Pace, M. L., 1988. Bacterial mortality and the fate of bacterial production. Hydrobiologia 159: 41–49.CrossRefGoogle Scholar
- Pace, M. L. & M. D. Bailiff, 1987. Evaluation of a fluorescent microsphere technique for measuring grazing rates of ph-agotrophic microorganisms. Mar. Ecol. Prog. Ser. 40: 185–193.CrossRefGoogle Scholar
- Pomeroy, L. R., 1974. The oceans food web, a changing paradigm. BioScience 24: 499–504.CrossRefGoogle Scholar
- Porter, K. G., E. B. Sherr, B. F. Sherr, M. Pace & R. W. Sanders, 1985. Protozoa in planktonic food webs. J. Protozool. 32: 409–415.Google Scholar
- Proctor, L. M. & J. A. Fuhrman, 1990. Viral mortality of marine bacteria and cyanobacteria. Nature 343: 60–62.CrossRefGoogle Scholar
- Rodina, A. G., 1967. Bacterial populations of humified lakes. Microbiologiya 38: 531–537.Google Scholar
- Salonen, K., 1981. The ecosystem of the oligotrophic lake Pääjärvi. 2. Bacterioplankton. Int. Verein Theor. Angew. Limnol. Verh. 21: 448–553.Google Scholar
- Salonen, K. & T. Hammar, 1986. On the importance of dissolved organic matter in the nutrition of Zooplankton in some lake waters. Oecologia 68: 246–253.CrossRefGoogle Scholar
- Salonen, K., K. Kolonen & L. Arvola, 1983. Respiration of plankton in two small, polyhumic lakes. Hydrobiologia 101: 65–70.CrossRefGoogle Scholar
- Scavia, D. & G. A. Laird, 1987. Bacterioplankton in Lake Michigan: dynamics, control, and significance to carbon flux. Limnol. Oceanogr. 32: 1017–1033.CrossRefGoogle Scholar
- Sherr, E. B., 1988. Direct use of high molecular weight polysaccharide by heterotrophic flagellates. Nature 335: 348–351.CrossRefGoogle Scholar
- Sherr, B. F. & E. B. Sherr, 1984. Role of heterotrophic protozoa in carbon and energy flow in aquatic ecosystems. In M. J. Klug & C. A. Reddy (eds), Current Perspectives in microbial Ecology. American Society for Microbiology, Washington, D.C.: 412–423.Google Scholar
- Sherr, B. F., E. B. Sherr & R. D. Fallon, 1987. Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl. envir. Microbiol. 53: 958–965.Google Scholar
- Sherr, B. F., E. B. Sherr & C. S. Hopkinson, 1988. Trophic interactions within pelagic microbial communities: Indications of feedback regulation of carbon flow. Hydrobiologia 159: 19–26.CrossRefGoogle Scholar
- Sherr, B. F., E. B. Sherr & C. Pedrós-Alió, 1989. Simultaneous measurement of bacterioplankton production and protozoan bacterivory in estuarine water. Mar. Ecol. Prog. Ser. 54: 209–219.CrossRefGoogle Scholar
- Sibbald, M. J., L. J. Albright & P. R. Sibbald, 1987. Chemosensory responses of a heterotrophic microflagellate to bacteria and several nitrogen compounds. Mar. Ecol. Prog. Ser. 36: 201–204.CrossRefGoogle Scholar
- Sieburth, J. McN., 1979. Sea Microbes. Oxford University Press, New York.Google Scholar
- Sieburth, J. McN. & P. G. Davis, 1982. The role of heterotrophic nanoplankton in the grazing and nurturing of planktonic bacteria in the Sargasso and Caribbean seas. Ann. Inst. Oceanogr. 58: 285–296.Google Scholar
- Stevenson, L. H., 1978. A case for bacterial dormancy in aquatic systems. Microb. Ecol. 4: 127–133.CrossRefGoogle Scholar
- Tranvik, L. J., 1988. Availability of dissolved organic carbon for planktonic bacteria in oligotrophic lakes of differing humic content. Microb. Ecol. 16: 311–322.CrossRefGoogle Scholar
- Tranvik, L. J., 1989. Bacterioplankton growth, grazing mortality and quantitative relationship to primary production in a humic and a clearwater lake. J. Plankton Res. 11: 985–1000.CrossRefGoogle Scholar
- Tranvik, L. J. & M. G. Höfle, 1987. Bacterial growth in mixed cultures on dissolved organic carbon from humic and clear waters. Appl. envir. Microbiol. 53: 482–488.Google Scholar
- Tranvik, L. J. & J. McN. Sieburth, 1989. Effects of flocculated humic matter on free and attached pelagic microorganisms. Limnol. Oceanogr. 34: 688–699.CrossRefGoogle Scholar
- Wetzel, R. G., 1984. Detrital dissolved and particulate organic carbon functions in aquatic ecosystems. Bull. mar. Sci. 35: 503–509.Google Scholar
- Wikner, J., A. Andersson, S. Normark & Å Hagström, 1986. Use of genetically marked minicells as a probe in measurement of predation on bacteria in aquatic environments. Appl. envir. Microbiol. 52: 4–8.Google Scholar
- Williams, P. J. LeB., 1981. Incorporation of microheterotrophic processes into the classical paradigm of the planktonic food web. Kieler Meeresforsch. Sonderh. 5: 1–28.Google Scholar
- Williams, P. J. LeB. & C. S. Yentsch, 1976. An examination of photo synthetic production, excretion of photo synthetic products, and heterotrophic utilization of dissolved organic compounds with reference to results from a coastal subtropical sea. Mar. Biol. 35: 31–40.CrossRefGoogle Scholar
- Wright, R. T. & R. B. Coffin, 1984. Factors affecting bacterioplankton density and productivity in salt marsh estuaries. In M. J. Klug and C. A. Reddy (eds), Current perspectives in microbial ecology. American Society for Microbiology, Washington, D.C.: 485–494.Google Scholar