Skip to main content
SpringerLink
Log in

Grazing of attached bacteria by heterotrophic microflagellates

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Four species of heterotrophic microflagellates were examined for their ability to graze attached and unattached bacteria. The species tested displayed pronounced differences in their ability to graze the bacteriumPseudomonas halodurans attached to chitin particles. Two species of microflagellates (Monas andCryptobia sp.) efficiently grazed unattached bacteria but showed little or no ability to graze attached or aggregated cells. In contrast,Rhynchomonas nasuta andBodo sp. showed marked preferences for attached and aggregated bacteria and a limited ability to graze unattached cells. The density of attached bacteria was reduced by an order of magnitude due to grazing byBodo andR. nasuta, even though the density of unattached bacteria was ∼5–90× the density of attached cells. The maximum densities attained by microflagellates in the cultures were related to the density of unattached bacteria forMonas andCryptobia but not forBodo andR. nasuta. Growth of the latter two species appeared to be related to the density of attached or aggregated bacteria. Based on the results of these experiments, it is concluded that the pelagic existence of microflagellates that graze attached bacteria may be strongly linked to the distribution of suspended particles and their associated bacteria. In addition, the removal of attached bacteria by microflagellates can significantly affect the density of bacteria attached to particles in the plankton. This activity may have important implications for the controversy concerning the relative importance of attached and free-living bacteria in the plankton.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Google Scholar 

  2. Azam F, Hodson RE (1977) Size distribution and activity of marine microheterotrophs. Limnol Oceanogr 22:492–501

    Google Scholar 

  3. Bell CR, Albright LJ (1981) Attached and free-floating bacteria in the Fraser River Estuary, British Columbia, Canada. Mar Ecol Prog Ser 6:317–327

    Google Scholar 

  4. Bent EJ, Goulder R (1981) Planktonic bacteria in the Humber Estuary: seasonal variation in population density and heterotrophic activity. Mar Biol 62:35–45

    Article  Google Scholar 

  5. Burzell LA (1973) Observations on the proboscis-cytopharynx complex and flagella ofRhynchomonas metabolita Pshenin, 1964 (Zoomastigophorea: Bodonidae). J Protozool 20:385–393

    PubMed  Google Scholar 

  6. Caron DA (1984) The role of heterotrophic microflagellates in plankton communities. Ph.D. Thesis, Woods Hole Oceanogr Inst and Mass Inst of Tech, Woods Hole

    Google Scholar 

  7. Caron DA, Davis PG, Madin LP, Sieburth JMcN (1982) Heterotrophic bacteria and bacterivorous protozoa in oceanic macroaggregates. Science 218:795–797

    Google Scholar 

  8. Caron DA, Davis PG, Madin LP, Sieburth JMcN (1986) Enrichment of microbial populations in macroaggregates (marine snow) from surface waters of the North Atlantic. J Mar Res 44:543–565

    Google Scholar 

  9. Cole JJ, Likens GE (1979) Measurements of mineralization of phytoplankton detritus in an oligotrophic lake. Limnol Oceanogr 24:541–547

    Google Scholar 

  10. Davis PG (1982) Bacterivorous flagellates in marine waters. Ph.D. Thesis, University of Rhode Island

    Google Scholar 

  11. Davis PG, Sieburth JMcN (1982) Differentiation of the photosynthetic and heterotrophic populations of nanoplankters by epifluorescence microscopy. Ann Inst Oceanogr, Paris 58 (S): 249–259

    Google Scholar 

  12. Davis PG, Sieburth JMcN (1984) Predation of actively growing bacterial populations by estuarine and oceanic microflagellates. Mar Ecol Prog Ser 19:237–246

    Google Scholar 

  13. Davoll PG (1983) Life history and community structure of marine snow aggregates from Monterey Bay (Abstr). EOS 64:1020

    Google Scholar 

  14. Dawson MP, Humphrey BA, Marshall KC (1981) Adhesion: a tactic in the survival strategy of a marine vibrio during starvation. Current Micobiol 6:195–199

    Article  Google Scholar 

  15. Derenbach JB, Williams PJ leB (1974) Autotrophic and bacterial production: fractionation of plankton populations by differential filtration of samples from the English Channel. Mar Biol 25:263–269

    Article  Google Scholar 

  16. Fenchel T (1982a) Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Mar Ecol Prog Ser 8:211–223

    Google Scholar 

  17. Fenchel T (1982b) Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar Ecol Prog Ser 8:225–231

    Google Scholar 

  18. Fenchel T (1982d) Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar Ecol Prog Ser 9:35–42

    Google Scholar 

  19. Fenchel T (1986) The ecology of heterotrophic microflagellates. Adv Microb Ecol 9:57–97

    Google Scholar 

  20. Fenchel TM, Jorgensen BB (1977) Detritus food chains of aquatic ecosystems: the role of bacteria. Adv Microb Ecol 1:1–58

    Google Scholar 

  21. Ferguson RL, Rublee P (1976) Contribution of bacteria to standing crop of coastal plankton. Limnol Oceanogr 21:141–145

    Google Scholar 

  22. Fletcher M (1979) A microautoradiographic study of the activity of attached and free-living bacteria. Arch Microbiol 122:271–274

    Article  Google Scholar 

  23. Goulder R (1977) Attached and free bacteria in an estuary with abundant suspended solids. J Appl Bacteriol 43:399–405

    Google Scholar 

  24. Gude H (1979) Grazing by protozoa as selection factor for activated sludge bacteria. Microb Ecol 5:225–237

    Article  Google Scholar 

  25. Haas LW, Webb KL (1979) Nutritional mode of several non-pigmented microflagellates from the York River Estuary, Virginia. J. Exp Mar Biol Ecol 39:125–134

    Article  Google Scholar 

  26. Hanson RB, Wiebe WJ (1977) Heterotrophic activity associated with particle size fractions in aSpartina alterniflora salt-marsh estuary, Sapelo Island, Georgia, USA, and the continental shelf waters. Mar Biol 42:321–330

    Article  Google Scholar 

  27. Harvey RW, Young LY (1980) Enumeration of particle-bound and unattached respiring bacteria in the salt marsh environment. Appl Environ Microbiol 40:156–160

    Google Scholar 

  28. Hobbie JE, Daley RJ, Jaspar S (1977) Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228

    PubMed  Google Scholar 

  29. Hobbie JE, Holm-Hansen O, Packard TT, Pomeroy LR, Sheldon RW, Thomas JP, Wiebe WJ (1972) A study of the distribution and activity of microorganisms in ocean water. Limnol Oceanogr 17:544

    Google Scholar 

  30. Jannasch HW (1973) Bacterial content of particulate matter in offshore surface waters. Limnol Oceanogr 18:340–342

    Google Scholar 

  31. Jannasch HW, Pritchard PH (1972) The role of inert particulate matter in the activity of aquatic microorganisms. Mem Ist Ital Idrobiol 29 (S):289–308

    Google Scholar 

  32. Jordan MJ, Likens GE (1980) Measurement of planktonic bacterial production in an oligotrophic lake. Limnol Oceanogr 25:719–732

    Google Scholar 

  33. Kirchman D, Mitchell R (1982) Contribution of particle-bound bacteria to total microheterotrophic activity in five ponds and two marshes. Appl Environ Microbiol 43:200–209

    Google Scholar 

  34. Kjelleberg S, Humphrey BA, Marshall KC (1982) Effect of interfaces on small, starved marine bacteria. Appl Environ Microbiol 43:1166–1172

    Google Scholar 

  35. Linley EAS, Field JG (1982) The nature and ecological significance of bacterial aggregation in a nearshore upwelling ecosystem. Est Coastal Shelf Sci 14:1–11

    Google Scholar 

  36. Paerl HW (1975) Microbial attachment to particles in marine and freshwater ecosystems. Microb Ecol 2:73–83

    Article  Google Scholar 

  37. Paerl HW, Merkel SM (1982) Differential phosphorus assimilation in attached vs. unattached microorganisms. Arch Hydrobiol 93:125–134

    Google Scholar 

  38. Palumbo AV, Ferguson RL, Rublee PA (1984) Size of suspended bacterial cells and association of heterotrophic activity with size fractions of particles in estuarine and coastal waters. Appl Environ Microbiol 48:157–164

    Google Scholar 

  39. Pedros-Alio C, Brock TD (1983) The importance of attachment to particles for planktonic bacteria. Arch Hydrobiol 98:354–379

    Google Scholar 

  40. Pomeroy LR (1983) Origin and distribution of flocculent aggregates (Abstr). EOS 64:1020

    Google Scholar 

  41. Robertson ML, Mills AL, Zieman JC (1982) Microbial synthesis of detritus-like particulates from dissolved organic carbon released by tropical seagrasses. Mar Ecol Prog Ser 7:279–285

    Google Scholar 

  42. Schleyer MH (1981) Microorganisms and detritus in the water column of a subtidal reef of Natal. Mar Ecol Prog Ser 4:307–320

    Google Scholar 

  43. Schoenberg SA, Maccubbin AE (1985) Relative feeding rates on free and particle-bound bacteria by freshwater macrozooplankton. Limnol Oceanogr 30:1084–1090

    Google Scholar 

  44. Seki H (1970) Microbial biomass on particulate organic matter in seawater of the euphotic zone. Appl Microbiol 19:960–962

    Google Scholar 

  45. Sherr BF, Sherr EB, Berman T (1983) Grazing, growth and ammonium excretion rates of a heterotrophic microflagellate fed with four species of bacteria. Appl Environ Microbiol 45: 1196–1201

    Google Scholar 

  46. Sieburth JMcN, Davis PG (1982) The role of heterotrophic nanoplankton in the grazing and nurturing of planktonic bacteria in the Sargasso and Caribbean Sea. Ann Inst Oceanogr, Paris 58 (S):285–296

    Google Scholar 

  47. Sorokin JI (1971) On the role of bacteria in the productivity of tropical oceanic waters. Int Revue Ges Hydrobiol 56:1–48

    Google Scholar 

  48. Taga N, Matsuda O (1974) Bacterial populations attached to plankton and detritus in seawater. In: Colwell RR, Morita RY (eds) Effect of the ocean environment on microbial activities. University Park Press, pp 433–448

  49. Telkova LA (1964) New data on food seizing in the genusRhynchomonas (Flagellatae). Zool Zhur 43:606–607

    Google Scholar 

  50. Watson SW, Novitsky TJ, Quinby HL, Valois FW (1977) Determination of bacterial number and biomass in the marine environment. Appl Environ Microbiol 33:940–946

    PubMed  Google Scholar 

  51. Wiebe WJ, Pomeroy LR (1972) Microorganisms and their association with aggregates and detritus in the sea: a microscopic study. Mem Ist Ital Idrobiol 29 (S):325–352

    Google Scholar 

  52. Williams PJ leB (1970) Heterotrophic utilization of dissolved organic compounds in the sea. I. Size distribution of population and relationship between respiration and incorporation of growth substrates. J Mar Biol Assoc UK 50:859–870

    Google Scholar 

  53. Wilson CA, Stevenson LH (1980) The dynamics of the bacterial population associated with a salt marsh. J Exp Mar Biol Ecol 48:123–138

    Article  Google Scholar 

  54. Zimmerman R (1978) Estimation of bacterial number and biomass by epifluorescence microscopy and scanning electron microscopy. In: Rheinheimer G (ed) Microbial ecology of a brackish water environment. Springer-Verlag, New York, pp 103–120

    Google Scholar 

  55. Zobell CE (1943) The effect of solid surfaces upon bacteria. J Bacteriol 46:39–56

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biology Department, Woods Hole Oceanographic Institution, 02543, Woods Hole, Massachusetts

    David A. Caron

Authors
  1. David A. Caron
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caron, D.A. Grazing of attached bacteria by heterotrophic microflagellates. Microb Ecol 13, 203–218 (1987). https://doi.org/10.1007/BF02024998

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02024998

Keywords

Search

Navigation