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Bacterial metabolism of algal extracellular carbon

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Abstract

Measurements of microbial utilization of extracellular organic carbon (EOC) released by phytoplankton commonly consider only EOC fractions subject to rapid uptake. Questions remain whether other EOC fractions are metabolized, what portion is labile, and with what assimilation efficiency this carbon substrate is utilized. 14C-EOC was prepared by incubation of the natural mixed planktonic community from an oligotrophic lake with H14CO3 in the light. 14C-EOC which was not rapidly removed by heterotrophs remained in solution and was isolated by filtration. This residual EOC was inoculated with lake microheterotrophs in laboratory microcosms, and utilization kinetics were determined through long-term assays of cumulative 14CO2 production. Time-courses for 14CO2 production were consistent for all assays and were well described by a deterministic mixed-order degradation model. On twelve sampling occasions, from 29% to 76% of residual 14C-EOC was labile to further metabolism by lake heterotrophs. First-order rate constants for EOC utilization showed a mode of 0.05 to 0.15 per day. From 33% to 78% of gross 14C-EOC uptake was respired (mean 50%), indicating appreciable return of algal EOC to the pelagic food web as microbial biomass.

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References

  • Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil & F. Thingstad, 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. prog. Ser. 10: 257–263.

    Google Scholar 

  • Bell, R. T. & J. Kuparinen, 1984. Assessing phytoplankton and bacterioplankton production during early spring in Lake Erken, Sweden. Appl. envir. Microbiol. 48: 1221–1230.

    Google Scholar 

  • Bell, W. H., 1980. Bacterial utilization of algal extracellular products. 1. The kinetic approach. Limnol. Oceanogr. 25: 1007–1020.

    Google Scholar 

  • Bell, W. H., 1984. Bacterial adaptation to low-nutrient conditions as studied with algal extracellular products. Microb. Ecol. 10: 217–230.

    Google Scholar 

  • Berman, T. & B. Kaplan, 1984. Diffusion chamber studies of carbon flux from living algae to heterotrophic bacteria. Hydrobiologia 108: 127–134.

    Google Scholar 

  • Bjørnsen, P. K., 1986. Bacterioplankton growth yield in continuous seawater cultures. Mar. Ecol. prog. Ser. 30: 191–196.

    Google Scholar 

  • Brock, T. D. & J. Clyne, 1984. Significance of algal excretory products for growth of epilimnetic bacteria. Appl. envir. Microbiol. 47(4): 731–734.

    Google Scholar 

  • Brunner, W. & D. D. Focht, 1984. Deterministic three-half-order kinetic model for microbial degradation of added carbon substrates in soil. Appl envir. Microbiol. 47: 167–172.

    Google Scholar 

  • Buddemeyer, E. U., G. M. Wells, R. Hutchinson, M. D. Cooper & G. S. Johnston, 1978. Radiometric estimation of the replication time of bacteria in culture: An objective and precise approach to quantitative microbiology. J. Nucl. Med. 19: 619–625.

    PubMed  Google Scholar 

  • Chrost, R. J. & M. A. Faust, 1983. Organic carbon release by phytoplankton: its composition and utilization by bacterioplankton. J. Plankton Res. 5: 477–493.

    Google Scholar 

  • Cole, J. J., G. E. Likens & D. L. Strayer, 1982. Photosynthetically produced dissolved organic carbon: An important carbon source for planktonic bacteria. Limnol. Oceanogr. 27: 1080–1090.

    Google Scholar 

  • Coveney, M. F., 1982. Bacterial uptake of photosynthetic carbon from freshwater phytoplankton. Oikos 38: 8–20.

    Google Scholar 

  • Coveney, M. F. & R. G. Wetzel, 1984. Improved double-vial radiorespirometric technique for mineralization of 14C-labeled substrates. Appl. envir. Microbiol. 47: 1154–1157.

    Google Scholar 

  • Ducklow, H. W., D. A. Purdie, P. J. LeB. Williams & J. M. Davies, 1986. Bacterioplankton: a sink for carbon in a coastal marine plankton community. Science 232: 865–867.

    Google Scholar 

  • Fuhrman, J. A., R. W. Eppley, Å. Hagström & F. Azam, 1985. Diel variations in bacterioplankton, phytoplankton, and related parameters in the Southern California Bight. Mar. Ecol. prog. Ser. 27: 9–20.

    Google Scholar 

  • Hobbie, J. E. & C. C. Crawford, 1969. Respiration corrections for bacterial uptake of dissolved organic compounds in natural waters. Limnol. Oceanogr. 14: 528–532.

    Google Scholar 

  • Hoppe, H. G., 1978. Relations between active bacteria and heterotrophic potential in the sea. Neth. J. Sea Res. 12: 78–98.

    Article  Google Scholar 

  • Iturriaga R. & H.-G. Hoppe, 1977. Observations of heterotrophic activity on photoassimilated organic matter. Mar. Biol. 40: 101–108.

    Google Scholar 

  • Iturriaga, R. & A. Zsolnay, 1983. Heterotrophic uptake and transformation of phytoplankton extracellular products. Bot. Mar. 26: 375–381.

    Google Scholar 

  • Jensen, L. M., 1983. Phytoplankton release of extracellular organic carbon, molecular weight composition, and bacterial assimilation. Mar. Ecol. prog. Ser. 11: 39–48.

    Google Scholar 

  • Jensen, L. M., N. O. G. Jørgensen & M. Søndergaard, 1985. Specific activity. Significance in estimating release rates of extracellular dissolved organic carbon (EOC) by algae. Verh. int. Ver. Limnol. 22: 2893–2897.

    Google Scholar 

  • Kato, K. & H.-H, Stabel, 1984. Studies on the carbon flux from phyto- to bacterioplankton communities in Lake Constance. Arch. Hydrobiol. 102: 177–192.

    Google Scholar 

  • King, G. M. & T. Berman, 1984. Potential effects of isotopic dilution on apparent respiration in 14C heterotrophy experiments. Mar. Ecol. prog. Ser. 19: 175–180.

    Google Scholar 

  • Lancelot, C., 1984. Extracellular release of small and large molecules by phytoplankton in the Southern Bight of the North Sea. Estuarine, Coastal and Shelf Science 18: 65–77.

    Google Scholar 

  • Larsson, U. & Å. Hagstrom, 1982. Fractionated phytoplankton primary production, exudate release and bacterial production in a Baltic eutrophication gradient. Mar. Biol. 67: 57–70.

    Google Scholar 

  • Lovell, C. R. & A. Konopka, 1985. Excretion of photosynthetically fixed organic carbon by metalimnetic phytoplankton. Microb. Ecol. 11: 1–9.

    Google Scholar 

  • McKinley, V. L., T. W. Federle & J. R. Vestal, 1983. Improvements in and environmental applications of double-vial radiorespirometry for the study of microbial mineralization. Appl. envir. Microbiol. 45: 255–259.

    Google Scholar 

  • Payne, W. J., 1970. Energy yields and growth of heterotrophs. Ann. Rev. Microbiol. 24: 17–52.

    Article  Google Scholar 

  • Riemann, B. & M. Søndergaard, 1984a. Measurements of diel rates of bacterial secondary production in aquatic environments. Appl. envir. Microbiol 47: 632–638.

    Google Scholar 

  • Riemann, B. & M. Søndergaard, 1984b. Bacterial growth in relation to phytoplankton primary production and extracellular release of organic carbon. In J. E. Hobbie & P. J. leB. Williams (eds), Heterotrophic Activity in the Sea. Plenum press, N.Y.: 233–248.

    Google Scholar 

  • Riemann, B., M. Søndergaard, H.-H. Schierup, S. Bosselmann, G. Christensen, J. Hansen & B. Nielsen, 1982. Carbon metabolism during a spring diatom bloom in the eutrophic Lake Mosso. Int. Reveu ges. Hydrobiol. 67: 145–185.

    Google Scholar 

  • Scavia, D. & G. A. Laird, 1987. Bacterioplankton in Lake Michigan: dynamics, controls, and significance to carbon flux. Limnol. Oceanogr. 32: 1017–1033.

    Google Scholar 

  • Scow, K. M., S. Simkins & M. Alexander, 1986. Kinetics of mineralization of organic compounds at low concentrations in soil. Appl. envir. Microbiol. 51: 1028–1035.

    Google Scholar 

  • Simkins, S. & M. Alexander, 1984. Models for mineralization kinetics with the variables of substrate concentration and population density. Appl. envir. Microbiol. 47: 1299–1306.

    Google Scholar 

  • Søndergaard, M. & H.-H. Schierup, 1982. Release of extracellular organic carbon during a diatom bloom in Lake Mossø: molecular weight fractionation. Freshwat. Biol. 12: 313–320.

    Google Scholar 

  • Storch, T. A. & G. W. Saunders, 1978. Phytoplankton extracellular release and its relation to the seasonal cycle of dissolved organic carbon in a eutrophic lake. Limnol. Oceanogr. 23: 112–119.

    Google Scholar 

  • Valley, G. & L.F. Rettger, 1927. The influence of carbon dioxide on bacteria. J. Bact. 14: 101–137.

    Google Scholar 

  • Walker, H. H., 1932. Carbon dioxide as a factor affecting lag in bacterial growth. Science 76: 602–604.

    Google Scholar 

  • Wetzel, R. G., 1983. Limnology. 2nd Ed. W. B. Saunders Co. 860 p.

  • Williams, P. J. LeB., 1984. Bacterial production in the marine food chain: the emperor's new suit of clothes? In Fasham, M. J. R. (Ed.), Flows of Energy and Materials in Marine Ecosystems: Theory and Practice. Plenum Press, N.Y.: 271–299.

    Google Scholar 

  • Wolter, K., 1982. Bacterial incorporation of organic substances released by natural phytoplankton populations. Mar. Ecol. prog. Ser. 7: 287–295.

    Google Scholar 

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Authors and Affiliations

  1. W. K. Kellogg Biological Station, Michigan State University, 49060, Hickory Corners, MI

    Michael F. Coveney & Robert G. Wetzel

  2. Water Resources Department, St. Johns River Water Management District, P.O. Box 1429, 32078-1429, Palatka, FL, U.S.A.

    Michael F. Coveney

  3. Department of Biology, The University of Michigan, 48109, Ann Arbor, MI, U.S.A.

    Robert G. Wetzel

Authors
  1. Michael F. Coveney
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  2. Robert G. Wetzel
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Contribution No. 596, W. K. Kellogg Biological Station, Michigan State University.

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Coveney, M.F., Wetzel, R.G. Bacterial metabolism of algal extracellular carbon. Hydrobiologia 173, 141–149 (1989). https://doi.org/10.1007/BF00015524

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