Microbial Extracellular Enzyme Activity: A New Key Parameter in Aquatic Ecology

  • Hans-Georg Hoppe
Part of the Brock/Springer Series in Contemporary Bioscience book series (BROCK/SPRINGER)

Abstract

Three general pathways of organic matter degradation exist in natural aquatic environments. These are based on predation, particle feeding, and dissolved organic matter (DOM) uptake. Bacteria are involved in the latter two in that they are able to hydrolyze nonliving particles thereby competing with particle feeders, and take up small organic molecules, which is their exclusive domain. Particle hydrolysis is mediated by extracellular enzymes in the intestines of animals and by the enzymatic activity of attached bacteria. Therefore, successful competition for organic matter among tropic levels is also a question of extra-cellular enzymatic efficiencies. The decomposition of dissolved organic macromolecules is mediated mainly by the enzymes of free-living bacteria, which subsequently incorporate the small molecules resulting from enzymatic hydrolysis. Therefore, bacterial activity has a strong influence on the concentration and speciation of dissolved organic molecules in the water. A major fraction of the DOM-pool in the water can be expected to consist of dissolved macromolecules since extracellular hydrolysis is a relatively slow process in comparison to the uptake of low-molecular-weight organic matter (LMWOM). The efficiency of animals feeding on particles may vary considerably, depending on various factors. Microbial hydrolysis of particles will depend greatly on the chemical composition and the size of the particles. Thus competition for organic particles between animals and microbes will be determined on the one hand, by the slow but continuous microbial component and, on the other hand, by pulse-feeding activities of animals (Joint and Morris, 1982). In detail, it has been pointed out that efficiencies of microbial decomposition of fast-sinking large particles and nonsinking small particles may be different (Cho and Azam, 1988; Karl et al., 1988).

Keywords

Biomass Hydrolysis Chlorophyll Lipase Phytoplankton 

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References

  1. Alvarez, R.J. 1984. Use of fluorogenic assays for the enumeration of Escherichia coli from selected seafoods. Journal of Food Science 49: 1186–1187.CrossRefGoogle Scholar
  2. Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A. and T.F. Thingstad. 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10: 257–263.CrossRefGoogle Scholar
  3. Azam, F. and J.W. Ammerman. 1984. Cycling of organic matter by bacterioplankton in pelagic marine ecosystem: microenvironmental considerations. pp. 345–360 in Facham, M.J.R. (editor), Flows of Energy and Materials in Marine Ecosystems. Plenum Publishing Corp., New York.Google Scholar
  4. Berg, J.D. and L. Fiksdal. 1988. Rapid detection of total and fecal coliforms in water by enzymatic hydrolysis of 4-methylumbelliferyl-α-D-galactoside. Applied and Environmental Microbiology 54: 2118–2122.PubMedGoogle Scholar
  5. Boon, P.I. 1989. Organic matter degradation and nutrient regeneration in Australian freshwater: I. Methods for enzyme assays in turbid aquatic environments. Archiv für Hydrobiologie 115: 339–359.Google Scholar
  6. Cho, B.C. and F. Azam. 1988. Major role of bacteria in biochemical fluxes in the ocean’s interior. Nature 332: 441–443.CrossRefGoogle Scholar
  7. Chróst, R.J. 1989. Characterization and significance of ß-glucosidase activity in lake water. Limnology and Oceanography 34: 660–672.CrossRefGoogle Scholar
  8. Chróst, R.J. 1990. Microbial ectoenzymes in aquatic environments. pp. 47–78 in Overbeck, J. and Chróst, R.J. (editors), Aquatic Microbial Ecology: Biochemical and Molecular Approaches. Springer Verlag, New York. 190 pp.Google Scholar
  9. Chróst, R.J. and H.J. Krambeck. 1986. Fluorescence correction for measurements of enzyme activity in natural waters using methylumbelliferyl-substrates. Archiv für Hydrobiologie 106: 79–90.Google Scholar
  10. Chróst, R.J., Münster, U., Rai, H., Albrecht, D., Witzel, K.P. and J. Overbeck. 1989. Photosynthetic production and exoenzymatic degradation of organic matter in the euphotic zone of an eutrophic lake. Journal of Plankton Research 11: 223–242.CrossRefGoogle Scholar
  11. Chróst, R.J. and J. Overbeck. 1987. Kinetics of alkaline phosphatase activity and phosphorus availability for phytoplankton and bacterioplankton in Lake Plußsee (North German eutrophic lake). Microbial Ecology 13: 229–248.CrossRefGoogle Scholar
  12. Chróst, R.J., Siuda, W., Albrecht, D. and J. Overbeck. 1986. A method for determining enzymatically hydrolyzable phosphate (EHP) in natural waters. Limnology and Oceanography 31: 662–667.CrossRefGoogle Scholar
  13. Coffin, R.B. 1989. Bacterial uptake of dissolved free and combined amino acids in estuarine waters. Limnology and Oceanography 34: 531–542.CrossRefGoogle Scholar
  14. Fontigny, A., Billen, G. and J. Vives-Rego. 1987. Kinetic characteristics and regulation of exoproteolytic enzymes of marine bacterioplankton. Marine Ecology Progress Series 25: 127–133.Google Scholar
  15. Fuhrman, J.A. and F. Azam. 1982. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Marine Biology 66: 109–120.CrossRefGoogle Scholar
  16. Fukami, K., Simidu, U. and N. Taga. 1981. Fluctuation of the communities of heterotrophic bacteria during the decomposition process of phytoplankton. Journal of exploration in Biology and Ecology 55: 171–184.CrossRefGoogle Scholar
  17. Fukami, K., Simidu, U. and N. Taga. 1983. Change in a bacterial population during the process of degradation of a phytoplankton bloom in a brackish lake. Marine Biology 76: 253–255.CrossRefGoogle Scholar
  18. Garber, J.H. 1984. Laboratory study of nitrogen and phosphorus remineralization during the decomposition of coastal plankton and seston. Estuarine and Coastal Shelf Sciences 18: 685–702.CrossRefGoogle Scholar
  19. Gocke, K. 1977. Comparison of methods for determining the turnover times of dissolved organic compounds. Marine Biology 42: 131–141.CrossRefGoogle Scholar
  20. Goulder, R. 1990. Extracellular enzyme activities associated with epiphytic microbiota on submerged stems of the red Phragmites australis. Federation of European Microbiology Societies Microbiology Ecology 73: 323–330.Google Scholar
  21. Güde, H. 1978. Model experiments on regulation of bacterial polysaccharide degradation in lakes. Archiv für Hydrobiologie, (supplement) 55: 157–185.Google Scholar
  22. Guilbault, G.G. and J. Hieserman. 1969. Fluorometric substrate for sulfatase and lipase. Analytical Chemistry 41: 2006–2009.PubMedCrossRefGoogle Scholar
  23. Hobbie, J.E., Daley, R.J. and S. Jasper. 1977. Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology 33: 1225–1228.PubMedGoogle Scholar
  24. Hollibaugh, J.T. and F. Azam. 1983. Microbial degradation of dissolved protein in seawater. Limnology and Oceanography 28: 1104–1116.CrossRefGoogle Scholar
  25. Holzapfel-Pschorn, A., Obst, U. and K. Haberer. 1985. Fluoreszenzspektroskopie zum empfindlichen Nachweis von Enzymaktivitäten in der Trinkwasseraufbereitung. Gewässerschutz Wasser Abwasser 79: 352–365.Google Scholar
  26. Hoppe, H.G. 1983. Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Marine Ecology Progress Series 11: 299–308.CrossRefGoogle Scholar
  27. Hoppe, H.G. 1984. Attachment of bacteria: advantage or disadvantage for survival in the aquatic environment. pp. 283–302 in Marshall, K.C. (editor), Microbial Adhesion and Aggregation. Dahlem Konferenzen, Life Sciences Research Report 31, Springer-Verlag, Berlin.Google Scholar
  28. Hoppe, H.G. 1986. Relations between bacterial extracellular enzymatic activities and heterotrophic substrate uptake in a brackish water environment. Proceedings of 2nd International Colloquium on Marine Bacteriology, Actes de Colloque 3, Brest: 119–128.Google Scholar
  29. Hoppe, H.G., Kim, S.J. and K. Gocke. 1988a. Microbial decomposition in aquatic environments: combined process of extracellular enzyme activity and substrate uptake. Applied and Environmental Microbiology 54: 784–790.Google Scholar
  30. Hoppe, H.G., Schramm, W. and P. Bacolod. 1988b. Spatial and temporal distribution of pelagic microorganisms and their proteolytic activity over a partly destroyed coral reef. Marine Ecology Progress Series 44: 95–102.CrossRefGoogle Scholar
  31. Hoppe, H.G., Gocke, K. and J. Kuparinen. 1990. Studies on the effect of H2S on heterotrophic substrate uptake, extracellular enzyme activity and growth of brackish water bacteria. Marine Ecology Progress Series 64: 157–167.CrossRefGoogle Scholar
  32. Ingham, E.R. and D.A. Klein. 1982. Relationship between fluorescein diacetate-stained hyphae and oxygen utilization, glucose utilization and biomass of submerged fungal batch cultures. Applied and Environmental Microbiology 44: 363–370.PubMedGoogle Scholar
  33. Jackson, G.A. 1989. Simulation of bacterial attraction and adhesion to falling particles in an aquatic environment. Limnology and Oceanography 34: 514–530.CrossRefGoogle Scholar
  34. Jacobsen, T.R. and H. Rai. 1988. Determination of aminopeptidase activity in lakewater by a short term kinetic assay and its application in two lakes of differing eutrophication. Archiv far Hydrobiologie 113: 359–370.Google Scholar
  35. Joint, I.R. and R.J. Morris. 1982. The role of bacteria in the turnover of organic matter in the sea. Oceanography and Marine Biology Annual Reviews 20: 65–118.Google Scholar
  36. Karl, D.M., Knauer, G.A. and J.H. Martin. 1988. Downward flux of particulate organic matter in the ocean: a particle decomposition paradox. Nature 332: 438–441.CrossRefGoogle Scholar
  37. Kim, S.J. 1985. Untersuchungen zur heterotrophen Stoffaufnahme and extrazellulären Enzymaktivität von freilebenden and angehefteten Bakterien in verschiedenen Gewässerbiotopen. Ph.D. Dissertation, University Kiel. 203 pp.Google Scholar
  38. Kim, S.J. and H.G. Hoppe. 1986. Microbial extracellular enzyme detection on agar plates by means of fluorogenic methylumbelliferyl-substrates. Proceedings of 2nd International Colloquium on Marine Bacteriology, Actes de Colloque 3, Brest, 175–183.Google Scholar
  39. King, G.M. 1986. Characterization of a-glucosidase activity in intertidal marine sediments. Applied and Environmental Microbiology 51: 373–380.PubMedGoogle Scholar
  40. Marshall, K.C. 1985. Bacterial adhesion in oligotrophic habitats. Microbiology Sciences 2: 321–325.Google Scholar
  41. Marshall, K.C., Stout, R. and R. Mitchell. 1971. Selective sorption of bacteria from seawater. Canadian Journal of Microbiology 17: 1413–1416.PubMedCrossRefGoogle Scholar
  42. Marxsen, J. and K.-P. Witzel. 1990. Measurement of exoenzymatic activity in stream-bed sediments using methylumbelliferyl substrates. Archiv für Hydrobiologie Beihefte Ergebnisse Limnologie 34: 21–28.Google Scholar
  43. Meyer-Reil, L.A. 1986. Measurements of hydrolytic activity and incorporation of dissolved organic substrates by microorganisms in marine sediments. Marine Ecology Progress Series 31: 143–149.CrossRefGoogle Scholar
  44. Meyer-Reil, L.A. 1987. Seasonal and spatial distribution of extracellular enzymatic activities and microbial incorporation of dissolved organic substrates in marine sediments. Applied and Environmental Microbiology 53: 1748–1755.PubMedGoogle Scholar
  45. Mitchell, J.G., Okubo, A. and J.A. Fuhrman. 1985. Microzones surrounding phytoplank- ton form the basis for a stratified marine microbial ecosystem. Nature 316: 58–59.CrossRefGoogle Scholar
  46. Mow-Robinson, J.M. and G. Rheinheimer. 1985. Comparison of bacterial populations from the Kiel Fjord in relation to the presence or absence of benthic vegetation. Botanica Marina 28: 29–39.CrossRefGoogle Scholar
  47. Münster, U., Einö, P. and J. Nurminen. 1989. Evaluation of the measurements of extra-cellular enzyme activities in a polyhumic lake by means of studies with 4-methylumbelliferyl-substrates. Archiv für Hydrobiologie 115: 321–337.Google Scholar
  48. O’Brien, M. and R.R. Colwell. 1987. A rapid test for chitinase activity that uses 4-methylumbelliferyl-N-acetyl-α-D-glucosaminide. Applied and Environmental Microbiology 53: 1718–1720.PubMedGoogle Scholar
  49. Pancholy, S.K. and J.Q. Lynd. 1972. Quantitative fluorescence analysis of soil lipase activity. Soil Biology and Biochemistry 4: 257–259.CrossRefGoogle Scholar
  50. Pedersen, K. 1982. Factors regulating microbial biofilm development in a system with slowly flowing seawater. Applied and Environmental Microbiology 44: 1196–1204.PubMedGoogle Scholar
  51. Perry, M.J. 1972. Alkaline phosphatase activity in subtropical Central North Pacific waters using a sensitive fluorometric method. Marine Biology 15: 113–119.CrossRefGoogle Scholar
  52. Petterson, K. and M. Jansson. 1978. Determination of phosphatase activity in lake water, a study of methods. Verhandlungen der Internationalen Vereinigung für Theoretische and Angewandte Limnologie 20: 1226–1230.Google Scholar
  53. Priest, F.G. 1984. Extracellular Enzymes. Van Nostrand Reinhold (UK) Co. Ltd., Workingham. 79 pp.Google Scholar
  54. Rheinheimer, G., Gocke, K. and H.G. Hoppe. 1989. Vertical distribution of microbiological and hydrographic-chemical parameters in different areas of the Baltic Sea. Marine Ecology Progress Series 52: 55–70.CrossRefGoogle Scholar
  55. Rosso, A.L. and F. Azam. 1987. Proteolytic activity in coastal oceanic waters: depth distribution and relationship to bacterial populations. Marine Ecology Progress Series 41: 231–240.CrossRefGoogle Scholar
  56. Somville, M. 1984. Measurement and study of substrate specificity of exoglucosidase in natural water. Applied and Environmental Microbiology 48: 1181–1185.PubMedGoogle Scholar
  57. Somville, M. and G. Billen. 1983. A method for determining exoproteolytic activity in natural waters. Limnology and Oceanography 28: 190–193.CrossRefGoogle Scholar
  58. Snyder, A.P., Wang, T.T. and D.B. Greenberg. 1986. Pattern recognition analysis of in vivo enzyme-substrate fluorescence velocities in microorganisms detection and identification. Applied and Environmental Microbiology 51: 969–977.PubMedGoogle Scholar
  59. Vives-Rego, J.V., Billen, G., Fontigny, A. and M. Somville. 1985. Free and attached pro- teolytic activity in water environments. Marine Ecology Progress Series 21: 245–249.CrossRefGoogle Scholar
  60. Zimmerman, R. 1977. Estimation of bacterial number and biomass by epifluorescence microscopy and scanning electron microscopy. pp. 103–120 in Rheinheimer, G. (editor), Microbial Ecology of a Brackish Water Environment. Springer Verlag, Berlin.Google Scholar

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© Springer-Verlag New York Inc. 1991

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  • Hans-Georg Hoppe

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