Microbial Ecology

, Volume 29, Issue 3, pp 231–248 | Cite as

Attached and free-living bacteria: Production and polymer hydrolysis during a diatom bloom

  • M. Middelboe
  • M. Søndergaard
  • Y. Letarte
  • N. H. Borch


Abundance, production and extracellular enzymatic activity of free-living and attached bacteria were measured during the development and collapse of a spring bloom in a eutrophic lake. Free-living bacteria accounted for most of the total bacterial production during the first part of the bloom. Their production had a significant positive correlation to chlorophyll (P < .01) and polysaccharide concentration (P < .02) and to potential β-glucosidase and aminopeptidase activity (P < .05), suggesting that algal release of dissolved polymeric compounds provided an important carbon source for bacterial production. As the bloom collapsed, we observed a change in the activity and structure of the microbial community. The mean contribution of attached bacteria to total bacterial production increased from 12% during the first part of the bloom to 26% at the end. Also, the extracellular enzymatic activity of attached bacteria increased as the bloom collapsed and constituted up to 75% of the total hydrolytic activity. An estimated disparity between hydrolytic activity and the corresponding carbon demand of attached bacteria suggested a net release of dissolved organic compounds from organic particles via polymer hydrolysis by attached bacteria.


Chlorophyll Hydrolytic Activity Bacterial Production Eutrophic Lake Spring Bloom 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Alpkem (1990) RFA-Methodology A303-S202, A303-S170A303-S020 Alpkem Corporation Clackamas, OregonGoogle Scholar
  2. 2.
    Baines SB, Pace ML (1991) The production of dissolved organic matter by phytoplankton and its importance to bacteria: patterns across marine and freshwater systems. Limnol Oceanogr 36:1078–1090Google Scholar
  3. 3.
    Bell RT, Kuparinen J (1984) Assessing phytoplankton and bacterioplankton production during early spring in Lake Erken, Sweden. Appl Environ Microbiol 48:1221–1230Google Scholar
  4. 4.
    Biddanda BA (1988) Microbial aggregation and degradation of phytoplankton-derived detritus in seawater. II. Microbial metabolism. Mar Ecol Prog Ser 42:89–95Google Scholar
  5. 5.
    Billen G (1990) Delayed development of bacterioplankton with respect to phytoplankton: a clue for understanding their trophic relationships. Arch Hydrobiol Beih Ergebn Limnol 34:191–201Google Scholar
  6. 6.
    Billen G (1991) Protein degradation in aquatic environments. In: Chróst RJ (ed) Microbial enzymes in aquatic environments. Springer-Verlag, New York, pp 123–143Google Scholar
  7. 7.
    Burney CM, Sieburth JMcN (1977) Dissolved carbohydrates in seawater. II. A spectrophotometric procedure for total carbohydrate analysis and polysaccharide estimation. Mar Chem 5:15–28Google Scholar
  8. 8.
    Chróst RJ (1991) Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. In: RJ Chróst (ed) Microbial enzymes in aquatic environments. Springer-Verlag, New York, pp 29–59Google Scholar
  9. 9.
    Chróst RJ, Münster U, Rai H, Albrecht D, Witzel PK, Overbeck J (1989) Photosynthetic production and exoenzymatic degradation of organic matter in the euphotic zone of an eutrophic lake. J Plankton Res 11(2):223–242Google Scholar
  10. 10.
    Chróst RJ, Rai H (1993) Ectoenzyme activity and bacterial secondary production in nutrient-impoverished and nutrient enriched freshwater mesocosms. Microb Ecol 25:131–150Google Scholar
  11. 11.
    DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934Google Scholar
  12. 12.
    Fletcher M (1991) The physiological activity of bacteria attached to solid surfaces. Adv Microb Physiol 32:53–85Google Scholar
  13. 13.
    Fuhrman JA, Azam F (1980) Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica and California. Appl Environ Microbiol 39:1085–1095Google Scholar
  14. 14.
    Fukami K, Simidu U, Taga N (1983) Change in a bacterial population during the process of degradation of a phytoplankton bloom in a brackish lake. Mar Biol 76:253–255Google Scholar
  15. 15.
    Fukami K, Simidu U, Taga N (1983) Distribution of heterotrophic bacteria in relation to the concentration of particulate organic matter in seawater. Can J Microbiol 29:570–575Google Scholar
  16. 16.
    Griffith P, Shiah FK, Gloersen K, Ducklow HW Fletcher M (1994) Activity and distribution of attached bacteria in Chesapeake Bay. Mar Ecol Prog Ser 108:1–10Google Scholar
  17. 17.
    Grossart H-P, Simon M (1993) Linmetic macroscopic organic aggregates (lake snow): occurrence, characteristics, and microbial dynamics in Lake Constance. Limmol Oceanogr 38:532–546Google Scholar
  18. 18.
    Hansen B, Christoffersen K (1995) Specific growth rates of heterotrophic plankton organisms in a eutrophic lake during a spring bloom. F. Plankton Res. 17:413–430.Google Scholar
  19. 19.
    Hoppe H-G (1991): Microbial extracellular enzyme activity: a new key parameter in aquatic ecology. In: RJ Chróst (ed) Microbial enzymes in aquatic environments. Springer-Verlag, New York, pp 60–83Google Scholar
  20. 20.
    Hoppe H-G, Ducklow H, Karrasch B (1993) Evidence for dependency of bacterial growth on enzymatic hydrolysis of particulate organic matter in the mesopelagic ocean. Mar Ecol Prog Ser 93:277–283Google Scholar
  21. 21.
    Hoppe H-G, Kim S-J, Gocke K (1988) Microbial decomposition in aquatic environments: combined process of extracellular enzyme activity and substrate uptake. Appl Environ Microbiol 54:784–790Google Scholar
  22. 22.
    Iriberri J, Unanue M, Ayo B, Barcina I, Egea L (1990) Bacterial production and growth rate estimation from [3H]-thymidine incorporation for attached and free-living bacteria in aquatic systems. Appl Environ Microbiol 56:483–487Google Scholar
  23. 23.
    Jespersen A-M, Christoffersed K (1987) Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Arch Hydrobiol 109:445–454Google Scholar
  24. 24.
    Johnson KM, Sieburth JMcN (1977) Dissolved carbohydrates in seawater. I. A precise spectrophotometric analysis for monosaccharides. Mar Chem 5:1–13Google Scholar
  25. 25.
    Jonas RB, Tuttle JH (1990) Bacterioplankton and organic carbon dynamics in the lower mesohaline Chesapeake Bay. Appl Environ Microbiol 56:747–757Google Scholar
  26. 26.
    Jumars PA, Penry DL, Baross JA, Perry MJ, Frost BW (1989) Closing the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals. Deep-Sea Res 36(4):483–495Google Scholar
  27. 27.
    Kamer M, Fuks D, Herndl GJ (1992) Bacterial activity along a trophic gradient. Microb Ecol 24:243–257Google Scholar
  28. 28.
    Kamer M, Herndl GJ (1992) Extracellular enzymatic activity and secondary production in free-living and marine-snow-associated bacteria. Mar Biol 113:341–347Google Scholar
  29. 29.
    Kirchman DL (1983) The production of bacteria attached to particles in a freshwater pond. Limnol Oceanogr 28:858–872Google Scholar
  30. 30.
    Kirchman DL, Ducklow HW (1987) Trophic dynamics of particle-bound bacteria in pelagic ecosystems: a review. In: DJW Moriarty and RSV Pullin (eds) Detritus and microbial ecology in aquaculture. International Center for Living Aquatic Resource Management, Manila, pp 54–82Google Scholar
  31. 31.
    Kirchman DL, Mitchell R (1982) Contribution of particle-bound bacteria to total microheterotrophic activity in five ponds and two marshes. Appl Environ Microbiol 43:200–209Google Scholar
  32. 32.
    Lancelot C, Billen G (1984) Activity of heterotrophic bacteria and its coupling to primary production during the spring phytoplankton bloom in the southern bight of the North Sea. Limnol Oceanogr 29:721–730Google Scholar
  33. 33.
    Letarte Y, Hansen HJ, Søndergaard M, Pinel-Alloul, B (1992) Production and abundance of different bacterial sizeclasses: relationships with primary production and chlorophyll concentration. Arch Hydrobiol 126(1):15–26Google Scholar
  34. 34.
    Martinez M, Azam F (1993) Aminopeptidase activity in marine chroococcoid cyanobacteria. Appl Environ Microbiol 59:3701–3707Google Scholar
  35. 35.
    Middelboe M, Nielsen B, Søndergaard M (1992) Bacterial utilization of dissolved organic carbon (DOC) in coastal waters—determination of growth yield. Arch Hydrobiol Ergebn Limnol 37(6):51–61Google Scholar
  36. 36.
    Middelboe M, Søndergaard M (1993) Bacterioplankton growth yield: seasonal variations and coupling to substrate lability and β-glucosidase activity. Appl Environ Microbiol 59:3916–3921Google Scholar
  37. 37.
    Pedrós-Alió C, Brock TD (1983) The importance of attachment to particles for planktonic bacteria. Arch Hydrobiol 98:354–379Google Scholar
  38. 38.
    Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948Google Scholar
  39. 39.
    Servais P, Garnier J (1993) Contribution of heterotrophic bacterial production to the carbon budget of the River Seine (France). Microb Ecol 25:19–33Google Scholar
  40. 40.
    Simon M (1985) Specific uptake rates of amino acids by attached and free-living bacteria in a mesotrophic lake. Appl Environ Microbiol 49:1254–1259Google Scholar
  41. 41.
    Simon M (1987) Biomass and production of small and large free-living and attached bacteria in Lake Constance. Limnol Oceanogr 32:591–607Google Scholar
  42. 42.
    Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic bacteria. Mar Ecol Prog Ser 51:201–213Google Scholar
  43. 43.
    Simon M, Tilzer MM (1987) Bacterial response to seasonal changes in primary production and phytoplankton biomass in Lake Constance. J Plankton Res 9:535–552Google Scholar
  44. 44.
    Smith DC, Simon M, Alldredge AL, Azam F (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359:139–142Google Scholar
  45. 45.
    Smits JD, Riemann B (1988) Calculation of cell production from 3H-thymidine incorporation with freshwater bacteria. Appl Environ Microbiol 54(9):2213–2219Google Scholar
  46. 46.
    Søndergaard M (1991) Phototrophic picoplankton in temperate lakes: seasonal abundance and importance along a trophic gradient. Int Rev Hydrobiol 76:505–522Google Scholar
  47. 47.
    Søndergaard M (1993) Organic carbon pools in two Danish lakes: flow of carbon to bacterioplankton. Verb Internat Verein Limnol 25:593–598Google Scholar
  48. 48.
    Søndergaard M, Borch NH (1992) Decomposition of dissolved organic carbon (DOC) in lakes. Arch Hydrobiol Beih Ergebn Limnol 37:9–20Google Scholar
  49. 49.
    Søndergaard M, Middelboe M (1993) Measurements of particulate organic carbon: a note on the use of glass fiber (GF/F) and Anodisc filters. Arch Hydrobiol 127(1):73–85Google Scholar
  50. 50.
    Unanue M, Ayo B, Azua I, Barcina I, Iriberri J (1992) Temporal variability of attached and free-living bacteria in coastal waters. Microb Ecol 23:27–39Google Scholar
  51. 51.
    Vandevivere P, Kirchman DL (1993) Attachment stimulates exopolysaccharide synthesis by a bacterium. Appl Environ Microbiol 59:3280–3286Google Scholar
  52. 52.
    Vives Rego J, Billen G, Fontigny A, Somville M (1985) Free and attached proteolytic activity in water environments. Mar Ecol Prog Ser 21:245–249Google Scholar

Copyright information

© Springer-Verlag New York Inc 1995

Authors and Affiliations

  • M. Middelboe
    • 1
  • M. Søndergaard
    • 1
  • Y. Letarte
    • 1
  • N. H. Borch
    • 2
  1. 1.Freshwater Biological LaboratoryUniversity of CopenhagenHillerødDenmark
  2. 2.Roskilde University LibraryRoskildeDenmark

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