Effects of different molecular weight fractions of dissolved organic matter on the growth of bacteria, algae and protozoa from a highly humic lake

  • T. Tulonen
  • K. Salonen
  • L. Arvola
Part of the Developments in Hydrobiology book series (DIHY, volume 73)

Abstract

Effects of different molecular size fractions (< 1000 MW, < 10000 MW, < 100000 MW and < 0.1 µm) of dissolved organic matter (DOM) on the growth of bacteria, algae and protozoa from a highly humic lake were investigated. DOM from catchment drainage water as well as from the lake consisted mostly (59–63%) of high molecular weight (HMW) compounds (> 10000 MW). With excess inorganic nutrients, the growth rate and yield of bacteria were almost identical in all size fractions. However, in < 1000 MW fractions and with glucose added, a longer lag phase occurred. Without added nutrients both the growth rates and biomasses of bacteria decreased towards the smaller size fractions and the percentage of dissolved organic carbon (DOC) used during the experiment and the growth efficiency of bacteria were lower than with excess nutrients. The growth efficiency of bacteria was estimated to vary between 3–66% in different MW fractions, largely depending on the nutrient concentrations, but the highest growth efficiencies were observed in HMW fractions and with glucose. The growth of algae was clearly lowest in the < 1000 MW fraction. In dim light no net growth of algae could be found. In contrast, added nutrients substantially enhanced algal growth and in deionized water with glucose, algae achieved almost the same growth rate and biomass as in higher MW fractions of DOM. The results suggested that bacteria and some algae were favoured by DOM, but protozoans seemed to benefit only indirectly, through bacterial grazing. The utilization of DOM by bacteria and algae was strongly affected by the availability of phosphorus and nitrogen.

Key words

dissolved organic matter humic substances bacteria algae protozoa growth 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen, H. L., 1976. Dissolved organic matter in lakewater: Characteristics of molecular weight size-fractions and ecological implications. Oikos 27: 64–70.CrossRefGoogle Scholar
  2. Arvola, L. & T. Tulonen. Enhancement by dissolved organic matter of the growth of laboratory strains of bacteria and algae and the microorganisms of a highly humic lake. Manuscript.Google Scholar
  3. Arvola, L., K. Salonen & M. Rask, 1990. Chemical budgets for a small dystrophic lake in southern Finland. Limnologica (Berlin) 20: 243–251.Google Scholar
  4. Benner, R., J. Jay, E. K’nees & R. E. Hodson, 1988. Carbon conversion efficiency for bacterial growth on lignocellulose: Implications for detritus-based food webs. Limnol. Oceanogr. 33: 1514–1526.CrossRefGoogle Scholar
  5. Bennett, M. E. & J. E. Hobbie, 1972. The uptake of glucose by Chlamydomonas sp. J. Phycol. 8: 392–398.Google Scholar
  6. Bergström, I., A. Heinänen & K. Salonen, 1986. Comparison of acridine organge, acriflavine, and bisbenzimide stains for enumeration of bacteria in clear and humic waters. Appl. envir. Microbiol. 51: 664–667.Google Scholar
  7. Børsheim, K. Y. & G. Bratbak, 1987. Cell volume to cell carbon conversion factors for a bacteriovorous Monas sp. enriched from sea water. Mar. Ecol. Prog. Ser. 36: 171–175.CrossRefGoogle Scholar
  8. Bratbak, G. & I. Dundas, 1984. Bacterial dry matter content and biomass estimations. Appl. envir. Microbiol. 48: 755–757.Google Scholar
  9. Carlson, D. J., M. L. Brann, T. H. Mague & L. M. Mayer, 1985. Molecular weight distribution of dissolved organic materials in seawater determined by ultrafiltration: A re-examination. Mar. Chem. 16: 155–171.CrossRefGoogle Scholar
  10. CCAP, 1988. Culture collection of algae and protozoa. Catalogue of strains. Natural Environmental Research Council, 164 pp.Google Scholar
  11. Chen, Y., S. U. Khan & M. Schnitzer, 1978. Ultraviolet irradiation of dilute fulvic acid solutions. Soil Sci. Soc. Amer. J. 42: 292–296.CrossRefGoogle Scholar
  12. Chróst, R. J., 1989. Characterization and significance of ß-glucosidase activity in lake water. Limnol. Oceanogr. 34: 660–672.CrossRefGoogle Scholar
  13. Chróst, R. J., U. Münster, H. Rai, D. Albrecht, P. K. Witzel & J. Overbeck, 1989. Photosynthetic production and exoenzymatic degradation of organic matter in euphotic zone of an eutrophic lake. J. Plankton Res. 11: 223–242.CrossRefGoogle Scholar
  14. Coffin, R. B., 1989. Bacterial uptake of dissolved free and combined amino acids in estuarine waters. Limnol. Oceanogr. 34: 531–542.CrossRefGoogle Scholar
  15. De Haan, H., 1974. Effects of a fulvic acid fraction on the growth of a Pseudomonas from Tjeukemeer (The Netherlands). Freshwat. Biol. 4: 301–310.CrossRefGoogle Scholar
  16. De Haan, H., 1979. Effect of benzoate on the microbial decomposition of fulvic acids in Tjeukemeer (The Netherlands). Limnol. Oceanogr. 22: 38–44.CrossRefGoogle Scholar
  17. De Haan, H., R. I. Jones & K. Salonen, 1987. Does ionic strength affect the configuration of aquatic humic substances, as indicated by gel filtration? Freshwat. Biol. 17: 453–459.CrossRefGoogle Scholar
  18. Geller, A., 1983. Degradability of dissolved organic lake water compounds in cultures of natural bacterial communities. Arch. Hydrobiol. 99: 60–79.Google Scholar
  19. Geller, A., 1985. Degradation and formation of refractory DOM by bacteria during simultaneous growth on labile substrates and persistent lake water constituents. Schweiz. Z. Hydrol. 47: 27–44.CrossRefGoogle Scholar
  20. Gjessing, E. T., 1970. Reduction of aquatic humus in streams. Vatten 1: 14–23.Google Scholar
  21. Gjessing, E. T., 1976. Physical and chemical characteristics of aquatic humus. Ann. Arbor Sci. Publ., Inc., Ann Arbor (Michigan): 1–20.Google Scholar
  22. Goldman, J. C., D. A. Caron & M. R. Dennett, 1987. Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C:N ratio. Limnol. Oceanogr. 32: 1239–1252.CrossRefGoogle Scholar
  23. Hessen, D. O., 1985. The relation between bacterial carbon and dissolved humic compounds in oligotrophic lakes. FEMS Microbiol. Ecol. 31: 215–223.CrossRefGoogle Scholar
  24. Il’ln, N. P. & D. S. Orlov, 1973. Photochemical destruction of humic acids. Soviet Soil Sci. 13: 75–83.Google Scholar
  25. Jones, R. I. & K. Salonen, 1985. The importance of bacterial utilization of released phytoplankton photosynthate in two humic lakes in southern Finland. Holarct. Ecol. 8: 133–140.Google Scholar
  26. Jones, R. I., K. Salonen & H. De Haan, 1988. Phosphorus transformations in the epilimnion of humic lakes: abiotic interactions between dissolved humic materials and phosphate. Freshwat. Biol. 19: 357–369.CrossRefGoogle Scholar
  27. Jørgensen, S. E., 1986. Fundamentals of ecological modelling. Elsevier.Google Scholar
  28. Kaplan, L. A. & T. L. Bott, 1983. Microbial heterotrophic utilization of dissolved organic matter in a piedmont stream. Freshwat. Biol. 13: 363–377.CrossRefGoogle Scholar
  29. Kieber, R. J., X. Zhou & K. Mopper, 1990. Formation of carbonyl compounds from UV-induced photodegradation of humic substances in natural waters: Fate or riverine carbon in the sea. Limnol. Oceanogr. 35: 1503–1515.CrossRefGoogle Scholar
  30. Lee, S. & J. A. Fuhrman, 1987. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. envir. Microbiol. 53: 1298–1303.Google Scholar
  31. Lytle, C. R. & E. M. Perdue, 1981. Free, proteinaceous, and humic-bound amino acids in river water containing high concentrations of aquatic humus. Envir. Sci. Technol. 15: 224–228.CrossRefGoogle Scholar
  32. Meyer, J. L., R. T. Edwards & R. Risley, 1987. Bacterial growth on dissolved organic matter from a blackwater river. Microb. Ecol. 13: 13–29.CrossRefGoogle Scholar
  33. Münster, U., 1985. Investigations about structure, distribution and dynamics of different organic substancies in the DOM of lake Plu see. Arch. Hydrobiol. Suppl. 70: 429–480.Google Scholar
  34. Münster, U., 1991. Extracellular enzyme activity in eutrophic and polyhumic lakes. In: R. J. Chróst (ed.), Microbial enzymes in aquatic environments, Brock/Springer Series, New York, (in Press).Google Scholar
  35. Münster, U. & R. J. Chróst, 1990. Origin, composition, and microbial utilization of dissolved organic matter. In: J. Overbeck & R. J. Chróst (eds.), Aquatic microbial ecology, Brock/Springer Series, New York. pp. 8–46.Google Scholar
  36. Münster, U., P. Einiö & J. Nurminen, 1989. Evaluation of the measurements of extracellular enzyme activities in a polyhumic lake by means of studies with 4-methyl-umbelliferyl-substrates. Arch. Hydrobiol. 115: 321–337.Google Scholar
  37. Ogura, N., 1975. Further studies on decomposition of dissolved organic matter in coastal seawater. Mar. Biol. 31: 101–111.CrossRefGoogle Scholar
  38. Rocha, O. & A. Duncan, 1985. The relationship between cell carbon and cell volume in freshwater algal species used in Zooplankton studies. J. Plankton Res. 7: 279–294.CrossRefGoogle Scholar
  39. Ryhänen, R., 1968. Die Bedeutung der Humus sub stanz en im Stoffhaushalt der Gewässer Finnlands. Mitt. int. Ver. Limnol. 14: 168–178.Google Scholar
  40. Salonen, K., 1979. A versatile method for the rapid and accurate determination of carbon by high temperature combustion. Limnol. Oceanogr. 24: 177–183.CrossRefGoogle Scholar
  41. Salonen, K., 1981. The ecosystem of the oligotrophic Lake Pääjärvi. 2. Bacterioplankton. Verh. int. Ver. Limnol. 21: 448–453.Google Scholar
  42. Salonen, K. & L. Arvola, 1988. A radiotracer study of Zooplankton grazing in two small humic lakes. Verh. int. Ver. Limnol. 23: 462–469.Google Scholar
  43. Salonen, K. & S. Jokinen, 1988. Flagellate grazing on bacteria in a small dystrophic lake. Hydrobiologia 161: 203–209.CrossRefGoogle Scholar
  44. Salonen, K., K. Kononen & L. Arvola, 1983. Respiration of plankton in two small, polyhumic lakes. Hydrobiologia 101: 65–70.CrossRefGoogle Scholar
  45. Salonen, K. & T. Tulonen, 1990. Photochemical and biological transformation of dissolved humic substances (Abstract). Verh. int. Ver. Limnol. 24: 294.Google Scholar
  46. Sederholm, H., A. Mauranen & L. Montonen, 1973. Some observations on the microbial degradation of humous substances in water. Verh. int. Ver. Limnol. 18: 1301–1305.Google Scholar
  47. Sherr, E. B., 1988. Direct use of high molecular weight polysaccharide by heterotrophic flagellates. Nature 335: 348–351.CrossRefGoogle Scholar
  48. Steinberg, C. & U. Münster, 1985. Geochemistry and ecological role of humic substances in lake water. In: Aiken,G. R., D. M. McKnight, R. L. Wershaw & P. MacCarthy (Eds.): Humic substances in soil, sediment, and water. Geochemistry, isolation and characterization. J. Wiley & Sons, P. 105-145.Google Scholar
  49. Stevenson, F. J., 1982. Humus chemistry. John Wiley & Sons, New York.Google Scholar
  50. Stewart, A. J. & R. G. Wetzel, 1981. Dissolved humic materials: photodegradation, sediment effects and reactivity with phosphate and calcium carbonate precipitation. Arch. Hydrobiol. 92: 265–286.Google Scholar
  51. Stockner, J. G., M. E. Klut & W. P. Cochlan, 1989. Leaky filters: a warning to aquatic ecologist. Can. J. Fish. aquat. Sci. 47: 16–23.CrossRefGoogle Scholar
  52. Strome, D. J. & M. C. Miller, 1978. Photolytic changes in dissolved humic substances. Verh. int. Ver. Limnol. 20: 1248–1254.Google Scholar
  53. Thurman, E. M., 1985. Organic geochemistry of natural waters. Mertinus Nijhoff/Dr. W. Junk.CrossRefGoogle Scholar
  54. 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
  55. 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
  56. Tranvik, L. J., 1990. Bacterioplankton growth on fractions of dissolved organic carbon of different molecular weights from humic and clear waters. Appl. envir. Microbiol. 56: 1672–1677.Google Scholar
  57. 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
  58. 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
  59. Utermöhl, H., 1958. Zur Vervollkommung der quantitativen Phytoplanktonmethodik. Mitt. int. Ver. Limnol. 9: 1–38.Google Scholar
  60. Vartiainen, T., A. Liimatainen & P. Kauranen, 1987. The use of TSK size exclusion columns in determination of the quality and quantity of humus in raw waters and drinking waters. Sci. Tot. Envir. 62: 75–84.CrossRefGoogle Scholar
  61. Visser, S. A., 1985. Effect of humic acids on numbers and activities of micro-organisms within physiological groups. Org. Geochem. 8: 81–85.CrossRefGoogle Scholar
  62. Ward, A. K. & R. G. Wetzel, 1984. Molecular weight fractionation of dissolved organic nitrogen and carbon compounds from two lakes of differing trophic status. Arch. Hydrobiol. 101: 481–488.Google Scholar
  63. Wetzel, R. G., 1983. Limnology, 2nd. edn. W.B. Saunders Co., Philadelphia.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1992

Authors and Affiliations

  • T. Tulonen
    • 1
  • K. Salonen
    • 1
  • L. Arvola
    • 1
  1. 1.Lammi Biological StationUniversity of HelsinkiLammiFinland

Personalised recommendations