Antonie van Leeuwenhoek

, Volume 81, Issue 1–4, pp 413–434 | Cite as

Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria

  • Klaus Jürgens
  • Carsten Matz


Predation is a major mortality factor of planktonic bacteria and an important shaping force for the phenotypic and taxonomic structure of bacterial communities. In this paper we: (1) summarise current knowledge on bacterial phenotypic properties which affect their vulnerability towards grazers, and (2) review experimental evidence demonstrating that this phenotypic heterogeneity results in shifts of bacterial community composition during enhanced protist grazing pressure. Size-structured interactions are especially important in planktonic systems and bacterial cell size influences the mortality rate and the type of grazer to which bacteria are most susceptible. When protists are the major bacterivores, both very small and large bacterial cells gain some size refuge. Recent studies have revealed that also various non-morphological traits such as motility, physicochemical surface characters and toxicity affect bacterial vulnerability and protist feeding success. These properties are effective at different stages during the feeding process of interception feeding flagellates (encounter, capture, ingestion, digestion). Grazing-resistant bacteria in natural communities can account for a substantial portion of the total bacterial biomass at least in more productive aquatic systems. In field and laboratory experiments it has been demonstrated that increased protozoan grazing results in shifts in the phenotypic and genotypic composition of the bacterial assemblage. The importance of this shaping force for the bacterial community structure depends, however, on the overall food web structure, especially on the composition of the metazooplankton. Whereas the structuring impact of bacterial grazers is well documented, relatively little is known about how grazing-mediated changes in bacterial communities influence microbially mediated processes and biogeochemically important transformations.

bacterial community structure bacterioplankton phenotypic properties predation predator–prey interactions protozoa 


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  1. Arndt H (1993) Rotifers as predators on components of the microbial web (bacteria, heterotrophic flagellates, ciliates) - a review. Hydrobiologia 255/256: 231–246.CrossRefGoogle Scholar
  2. Arndt H, Dietrich D, Auer B, Cleven E-J, Gräfenhan T, Weitere M & Mylnikov A (2000) Functional diversity of heterotrophic flagellates in aquatic ecosystems. In: Leadbeater B & Green J (Eds) The Flagellates (pp 240–268). Taylor and Francis, London.Google Scholar
  3. Bennett SJ, Sanders RW & Porter KG (1988) Chemosensory responses of heterotrophic and mixotrophic flagellates to potential food sources. Bull. Mar. Sci. 43: 764–771.Google Scholar
  4. Bernard L, Courties C, Servais P, Troussellier M, Petit M & Lebaron P (2000) Relationships among bacterial cell size, productivity, and genetic diversity in aquatic environments using cell sorting and flow cytometry. Microb. Ecol. 40: 148–158.PubMedGoogle Scholar
  5. Bianchi M (1989) Unusual bloom of a star-like prosthecate bacteria and filaments as a consequence of grazing pressure. Microb. Ecol. 17: 137–142.CrossRefGoogle Scholar
  6. Billen G, Servais P & Becquevort S (1990) Dynamics of bacterioplankton in oligotrophic and eutrophic aquatic environments: bottom-up or top-down control? Hydrobiologia 207: 37–42.CrossRefGoogle Scholar
  7. Blackburn N, Fenchel T & Mitchell J (1998) Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282: 2254–2256.CrossRefPubMedGoogle Scholar
  8. Boenigk J & Arndt H (2000a) Comparative studies on the feeding behavior of two heterotrophic nanoflagellates: the filter-feeding choanoflagellate Monosiga ovata and the raptorial-feeding kinetoplastid Rhynchomonas nasuta. Aquat. Microb. Ecol. 22: 243–249.Google Scholar
  9. Boenigk J & Arndt H (2000b) Particle handling during interception feeding by four species of heterotrophic nanoflagellates. J. Euk. Microbiol. 47: 350–358.CrossRefPubMedGoogle Scholar
  10. Boenigk J, Matz C, Jürgens K & Arndt H (2001a) Confusing selective feeding with differential digestion in bacterivorous nanoflagellates. J. Euk. Microbiol. 48: 425–432.CrossRefPubMedGoogle Scholar
  11. Boenigk J, Matz C, Jürgens K & Arndt H (2001b) The influence of preculture conditions and food quality on the ingestion and digestion process of three species of heterotrophic nanoflagellates. Microb. Ecol. 42: 168–176.PubMedGoogle Scholar
  12. Boenigk J, Matz C, Jürgens K & Arndt H (2002) Food concentration dependent regulation of food selectivity of interceptionfeeding bacterivorous nanoflagellates. Aquat. Microb. Ecol. 27: 195–202.Google Scholar
  13. Bohannan BJM & Lenski RE (2000) The relative importance of competition and predation varies with productivity in a model community. Am. Nat. 156: 329–340.CrossRefGoogle Scholar
  14. Boonaert CJP & Rouxhet PG (2000) Surface of lactic acid bacteria: Relationships between chemical composition and physicochemical properties. Appl. Environ. Microbiol. 66: 2548–2554.CrossRefPubMedGoogle Scholar
  15. Brendelberger H (1991) Filter mesh size of cladocerans predicts retention efficiency for bacteria. Limnol. Oceanogr. 36: 884–894.Google Scholar
  16. Brown R, Bass H & Coombs J (1975) Carbohydrate binding proteins involved in phagocytosis by Acanthamoeba. Nature 254: 434–435.CrossRefPubMedGoogle Scholar
  17. Choi JW, Sherr BF & Sherr EB (1999) Dead or alive? A large fraction of ETS-inactive marine bacterioplankton cells, as assessed by reduction of CTC, can become ETS-active with incubation and substrate addition. Aquat. Microb. Ecol. 18: 105–115.Google Scholar
  18. Christaki U, Dolan JR, Pelegri S & Rassoulzadegan F (1998) Consumption of picoplankton-size particles by marine ciliates: Effects of physiological state of the ciliate and particle quality. Limnol. Oceanogr. 43: 458–464.Google Scholar
  19. Christoffersen K (1996) Ecological implications of cyanobacterial toxins in aquatic food webs. Phycologia 35: 42–50.CrossRefGoogle Scholar
  20. Chrzanowski TH & Šimek K (1990) Prey-size selection by freshwater flagellated protozoa. Limnol. Oceanogr. 35: 1429–1436.Google Scholar
  21. Cole JJ (1999) Aquatic microbiology for ecosystem scientists: New and recycled paradigms in ecological microbiology. Ecosystems 2: 215–225.CrossRefGoogle Scholar
  22. Cotner JB, Gardner WS, Johnson JR, Sada RH, Cavaletto JF & Heath RT (1995) Effects of zebra mussels (Dreissena polymorpha) on bacterioplankton - evidence for both size-selective consumption and growth stimulation. J. Great Lakes Res. 21: 517–528.Google Scholar
  23. Cottrell MT & Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low-and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol. 66: 1692–1697.CrossRefPubMedGoogle Scholar
  24. Decho AW (1990) Microbial exopolymer secretions in oceanic environments: Their role(s) in food webs and marine processes. Oceanogr. Mar. Biol. Annu. Rev. 28: 73–153.Google Scholar
  25. Del Giorgio PA, Gasol JM, Vaqué D, Mura P, Agusti S & Duarte CM (1996) Bacterioplankton community structure - protists control net production and the proportion of active bacteria in a coastal marine community. Limnol. Oceanogr. 41: 1169–1179.CrossRefGoogle Scholar
  26. DeMott WR (1995) Food selection by calanoid copepods in response to between-lake variation in food abundance. Freshwat. Biol. 33: 171–180.CrossRefGoogle Scholar
  27. Ellwood DC & Tempest DW (1972) Effects of environment on bacterial wall content and composition. Adv. Microb. Phys. 7: 83–117.Google Scholar
  28. Elser JJ & Goldman CR (1991) Zooplankton effects on phytoplankton in lakes of contrasting trophic status. Limnol. Oceanogr. 36: 64–90.Google Scholar
  29. Engström-Öst J, Koski M, Schmidt K, Viitasalo M, Jonasdottir S, Kokkonen M, Repka S & Sivonen K (in press) Effects of toxic cyanobacteria on a plankton assemblage: community development during decay of Nodularia spumigena. Mar. Ecol. Prog. Ser.Google Scholar
  30. Fenchel T (1980) Relation between particle size selection and clearance in suspension-feeding ciliates. Limnol. Oceanogr. 25: 733–738.Google Scholar
  31. Fenchel T (1982a) Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Mar. Ecol. Prog. Ser. 8: 211–223.Google Scholar
  32. Fenchel T (1982b) Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol. Prog. Ser. 9: 35–41.Google Scholar
  33. Fenchel T (1984) Suspended marine bacteria as a food source. In: Fasham MJ (Ed) Flows of Energy and Materials in Marine Ecosystems (pp 301–315). Plenum Press, New YorkGoogle Scholar
  34. Fenchel T (1986) Protozoan filter feeding. Progr.Protistol. 1: 65–113.Google Scholar
  35. Fenchel T (2001) Eppur si muove: many water column bacteria are motile. Aquat. Microb. Ecol. 24: 197–201.Google Scholar
  36. Fenchel T & Harrison P (1976) The significance of bacterial grazing and mineral cycling for the decomposition of particulate detritus. In: Anderson JM & Macfadyen A (Eds) The Role of Terrestrial and Aquatic Organisms in Decomposition Processes (pp 285–299). Blackwell, Oxford.Google Scholar
  37. Flynn KJ, Davidson K & Cunningham A (1996) Prey selection and rejection by a microflagellate: Implications for the study and operation of microbial food webs. J. Exp. Mar. Biol. Ecol. 196: 357–372.CrossRefGoogle Scholar
  38. Frischer ME, Nierzwicki-Bauer SA, Parsons RH, Vathanodorn K & Waitkus KR (2000) Interactions between zebra mussels (Dreissena polymorpha) and microbial communities. Can. J. Fish. aquat. Sci. 57: 591–599.CrossRefGoogle Scholar
  39. Fuhrman J (2000) Impact of viruses on bacterial processes. In: Kirchman D (Ed) Microbial Ecology of the Oceans (pp 327–350). Wiley-Liss, New York.Google Scholar
  40. Gasol JM, Del Giorgio PA, Massana R & Duarte cm (1995) Active versus inactive bacteria: Size-dependence in a coastal marine plankton community. Mar. Ecol. Prog. Ser. 128: 91–97.Google Scholar
  41. Geesey GG (1982) Microbial exopolymers: ecological and economic considerations. ASM News 48: 9–14.Google Scholar
  42. Glöckner FO, Fuchs BM & Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl. Environ. Microbiol. 65: 3721–3726.PubMedGoogle Scholar
  43. González JM (1996) Efficient size-selective bacterivory by phagotrophic nanoflagellates in aquatic ecosystems. Mar. Biol. 126: 785–789.CrossRefGoogle Scholar
  44. González JM, Iriberri J, Egea L & Barcina I (1990a) Differential rates of digestion of bacteria by freshwater and marine phagotrophic protozoa. Appl. Environ. Microbiol. 56: 1851–1857.PubMedGoogle Scholar
  45. González JM, Sherr EB & Sherr BF (1990b) Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. Environ. Microbiol. 56: 583–589.PubMedGoogle Scholar
  46. González JM, Sherr EB & Sherr BF (1993) Differential feeding by marine flagellates on growing versus starving, and on motile versus nonmotile, bacterial prey. Mar. Ecol. Prog. Ser. 102: 257–267.Google Scholar
  47. González JM & Suttle CA (1993) Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar. Ecol. Prog. Ser. 94: 1–10.Google Scholar
  48. Grossart HP, Riemann L & Azam F (2001) Bacterial motility in the sea and its ecological implications. Aquat. Microb. Ecol. 25: 247–258.Google Scholar
  49. Güde H (1979) Grazing by protozoa as selection factor for activated sludge bacteria. Microb. Ecol. 5: 225–237.CrossRefGoogle Scholar
  50. Güde H (1982) Interactions between floc-forming and nonflocforming bacterial populations from activated sludge. Curr. Microbiol. 7: 347–350.CrossRefGoogle Scholar
  51. Güde H (1989) The role of grazing on bacteria in plankton succession. In: Sommer U (Ed) Plankton Ecology. Succession in Plankton Communities (pp 337–364). Springer Verlag, Berlin.Google Scholar
  52. Guixa-Boixereu N, Lysnes K & Pedrós-Alió C (1999) Viral lysis and bacterivory during a phytoplankton bloom in a coastal water microcosm. Appl. Environ. Microbiol. 65: 1949–1958.PubMedGoogle Scholar
  53. Hahn MW & Höfle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microb. Ecol. 35: 113–121.CrossRefGoogle Scholar
  54. Hahn MW & Höfle MG (1998) Grazing pressure by a bacterivorous flagellate reverses the relative abundance of Comamonas acidovorans Px54 and Vibrio strain Cb5 in chemostat cocultures. Appl. Environ. Microbiol. 64: 1910–1918.PubMedGoogle Scholar
  55. Hahn MW & Höfle MG (1999) Flagellate predation on a bacterial model community: Interplay of size-selective grazing, specific bacterial cell size, and bacterial community composition. Appl. Environ. Microbiol. 65: 4863–4872.PubMedGoogle Scholar
  56. Hahn MW, Moore ERB & Höfle MG (2000) Role of microcolony formation in the protistan grazing defense of the aquatic bacterium Pseudomonas sp MWH1. Microb. Ecol. 39: 175–185.PubMedGoogle Scholar
  57. Hahn MW, Moore ERB & Höfle MG (1999) Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Appl. Environ. Microbiol. 65: 25–35.PubMedGoogle Scholar
  58. Hammer A, Grüttner C & Schumann R (1999) The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina Dujardin (dinoflagellate). Protist 150: 375–382.PubMedCrossRefGoogle Scholar
  59. Hammond S, Lambert P & Rycoft A (1984) The Bacterial Cell Surface. Croom Helm, London.Google Scholar
  60. Havskum H & Hansen AS (1997) Importance of pigmented and colourless nano-sized protists as grazers on nanoplankton in a phosphate-depleted Norwegian fjord and in enclosures. Aquat. Microb. Ecol. 12: 139–151.Google Scholar
  61. Heissenberger A, Leppard GG & Herndl GJ (1996) Relationship between the intracellular integrity and the morphology of the capsular envelope in attached and free-living marine bacteria. Appl. Environ. Microbiol. 62: 4521–4528.PubMedGoogle Scholar
  62. Hirsch P & Müller M (1985) Planctomyces limnophilus sp. nov., a stalked and budding bacterium from freshwater. Syst. Appl. Microbiol. 6: 276–280.Google Scholar
  63. Holen DA & Boraas ME (1991) The feeding behavior of Spumella sp. as a function of particle size: Implications for bacterial size in pelagic systems. Hydrobiologia 220: 73–88.CrossRefGoogle Scholar
  64. Horwitz M & Silverstein S (1980) Influence of the Escherichia coli capsule on complement fixation and on phagocytosis and killing by human phagocytes. J. Clin. Invest. 65: 82–94.PubMedCrossRefGoogle Scholar
  65. Hunter R (1993) Introduction to Modern Colloid Science. Oxford University Press, Oxford.Google Scholar
  66. Jürgens K (1994) Impact ofDaphnia on planktonic microbial food webs - A review. Mar. Microb. Food Webs 8: 295–324.Google Scholar
  67. Jürgens K, Arndt H & Rothhaupt KO (1994) Zooplankton-mediated changes of bacterial community structure. Microb. Ecol. 27: 27–42.CrossRefGoogle Scholar
  68. Jürgens K & DeMott WR (1995) Behavioral flexibility in prey selection by bacterivorous nanoflagellates. Limnol. Oceanogr. 40: 1503–1507.CrossRefGoogle Scholar
  69. Jürgens K, Gasol JM & Vaqué D (2000) Bacteria-flagellate coupling in microcosm experiments in the Central Atlantic Ocean. J. Exp. Mar. Biol. Ecol. 245: 127–147.CrossRefGoogle Scholar
  70. Jürgens K & Güde H (1994) The potential importance of grazingresistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112: 169–188.Google Scholar
  71. Jürgens K & Jeppesen E (2000) The impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. J. Plankton Res. 22: 1047–1070.CrossRefGoogle Scholar
  72. Jürgens K, Pernthaler J, Schalla S & Amann R (1999) Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl. Environ. Microbiol. 65: 1241–1250.PubMedGoogle Scholar
  73. Jürgens K & Sala MM (2000) Predation-mediated shifts in size distribution of microbial biomass and activity during detritus decomposition. Oikos 91: 29–40.CrossRefGoogle Scholar
  74. Jürgens K & Šimek K (2000) Functional response and particle size selection of Halteria cf. grandinella, a common freshwater oligotrichous ciliate. Aquat. Microb. Ecol. 22: 57–68.Google Scholar
  75. Jürgens K & Stolpe G (1995) Seasonal dynamics of crustacean zooplankton, heterotrophic nanoflagellates and bacteria in a shallow, eutrophic lake. Freshwat. Biol. 33: 27–38.CrossRefGoogle Scholar
  76. Jürgens K, Wickham SA, Rothhaupt KO & Santer B (1996) Feeding rates of macro-and microzooplankton on heterotrophic nanoflagellates. Limnol. Oceanogr. 41: 1833–1839.Google Scholar
  77. Kaprelyants AS, Gottschal JC & Kell DB (1993) Dormancy in nonsporulating bacteria. FEMS Microbiol. Rev. 104: 271–286.CrossRefGoogle Scholar
  78. Kemp PF, Newell SY & Krambeck C (1990) Effects of filter-feeding by the ribbed mussel Geukensia demissa on the water-column microbiota of a Spartina alterniflora saltmarsh. Mar. Ecol. Prog. Ser. 59: 119–132.Google Scholar
  79. King CH, Shotts EB, Wooley RE & Porter KG (1988) Survival of coliforms and bacterial pathogens within protozoa during chlorination. Appl. Environ. Microbiol. 54: 3023–3033.PubMedGoogle Scholar
  80. King KR, Hollibaugh JT & Azam F (1980) Predator-prey interactions between the larvacean Oikopleura dioica and bacterioplankton in enclosed water columns. Mar. Biol. 56: 49–57.CrossRefGoogle Scholar
  81. Kjelleberg S, Albertson N, Flärdh K, Holmquist L, Jouper-Jaan A, Marouga R, Östling J, Svenblad B & Weichart D (1993) How do non-differentiating bacteria adapt to starvation? Antonie van Leeuwenhoek 63: 333–341.CrossRefPubMedGoogle Scholar
  82. Koval SF (1993) Predation on bacteria possessing S-layers. In: Beveridge TJ & Koval SF (Eds) Advances in Bacterial Paracrystalline Surface Layers (pp 85–92). Plenum Publishing Corporation, New York.Google Scholar
  83. Lampert W (1987) Predictability in lake ecosystems: the role of biotic interactions. In: Schulze ED & Zwölfer H (Eds) Potential and Limitations of Ecosystem Analysis. Ecological Studies 61 (pp 333–346). Springer-Verlag, Berlin.Google Scholar
  84. Landry MR, Lehner-Fournier JM, Sundstrom JA, Fagerness VL & Selph KE (1991) Discrimination between living and heat-killed prey by a marine zooflagellate Paraphysomonas vestita Stokes. J. Exp. Mar. Biol. Ecol. 146: 139–152.CrossRefGoogle Scholar
  85. Langenheder S & Jürgens K (2001) Regulation of bacterial biomass and community structure by metazoan and protozoan predation. Limnol. Oceanogr. 46: 121–134.CrossRefGoogle Scholar
  86. Lavrentyev PJ, Gardner WS & Johnson JR (1997) Cascading trophic effects on aquatic nitrification - experimental evidence and potential implications. Aquat. Microb. Ecol. 13: 161–175.Google Scholar
  87. Lebaron P, Servais P, Troussellier M, Courties C, Muyzer G, Bernard L, Schäfer H, Pukall R, Stackebrandt E, Guindulain T & Vives-Rego J (2001) Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in abundances, activity and composition. FEMS Microb. Ecol. 34: 255–266.CrossRefGoogle Scholar
  88. Leibold MA (1989) Resource edibility and the effects of predators and productivity on the outcome of trophic interactions. Am. Nat. 134: 922–949.CrossRefGoogle Scholar
  89. Lenski RE, Mongold JA, Sniegowski PD, Travisano M, Vasi F, Gerrish PJ & Schmidt TM (1998) Evolution of competitive fitness in experimental population of E. coli: What makes one genotype a better competitor than another? Antonie van Leeuwenhoek 73: 35–47.CrossRefPubMedGoogle Scholar
  90. Levrat P, Pussard M & Alabouvette C (1992) Enhanced bacterial metabolism of a Pseudomonas strain in response to the addition of culture filtrate of a bacteriophagous amoeba. Europ. J. Protistol. 28: 79–84.Google Scholar
  91. Matz C, Boenigk J, Arndt H & Jürgens K (2002a) Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquat. Microb. Ecol. 27: 137–148.Google Scholar
  92. Matz C, Deines P & Jürgens K (2002b) Phenotypic variation in Pseudomonas sp. CM10 determines microcolony formation and survival under protozoan grazing. FEMS Microb. Ecol. 39: 57–65.CrossRefGoogle Scholar
  93. Matz C & Jürgens K (2001) Effects of hydrophobic and electrostatic cell surface properties of bacteria on feeding rates of heterotrophic nanoflagellates. Appl. Environ. Microbiol. 67: 814–820.CrossRefPubMedGoogle Scholar
  94. Mitchell JG, Pearson L, Bonazinga A, Dillon S, Khouri H & Paxinos R (1995a) Long lag times and high velocities in the motility of natural assemblages of marine bacteria. Appl. Environ. Microbiol. 61: 877–882.PubMedGoogle Scholar
  95. Mitchell JG, Pearson L, Dillon S & Kantalis K (1995b) Natural assemblages of marine bacteria exhibiting high-speed motility and large accelerations. Appl. Environ. Microbiol. 61: 4436–4440.PubMedGoogle Scholar
  96. Monger BC & Landry MR (1990) Direct-interception feeding by marine zooflagellates: the importance of surface and hydrodynamic forces. Mar. Ecol. Prog. Ser. 65: 123–140.Google Scholar
  97. Monger BC & Landry MR (1991) Prey-size dependency of grazing by free-living marine flagellates. Mar. Ecol. Prog. Ser. 74: 239–248.Google Scholar
  98. Monger BC & Landry MR (1992) Size-selective grazing by heterotrophic nanoflagellates: an analysis using live-stained bacteria and dual-beam flow cytometry. Arch. Hydrobiol. Beih. Ergebn. Limnol. 37: 173–185.Google Scholar
  99. Monger BC, Landry MR & Brown SL (1999) Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey. Limnol. Oceanogr. 44: 1917–1927.CrossRefGoogle Scholar
  100. Morita RY (1982) Starvation-survival of heterotrophs in the marine environment. Adv. Microb. Ecol. 6: 171–198.Google Scholar
  101. Mozes N, Leonard AJ & Rouxhet PG (1988) On the relations between the elemental surface composition of yeasts and bacteria and their charge and hydrophobicity. Biochim. Biophys. Acta 945: 324–334.CrossRefPubMedGoogle Scholar
  102. Nagata T & Kirchman DL (1992) Release of dissolved organic matter by heterotrophic protozoa: implications for microbial food webs. Arch. Hydrobiol. Beih. Ergebn. Limnol. 35: 99–109.Google Scholar
  103. Nold S & Zwart G (1998) Patterns and governing forces in aquatic microbial communities. Aquat. Ecol. 32: 17–35.CrossRefGoogle Scholar
  104. Nyström T, Olsson RM & Kjelleberg S (1992) Survival stress resistance and alterations in protein expression in the marine Vibrio sp strain s14 during starvation for different individual nutrients. Appl. Environ. Microbiol. 58: 55–65.PubMedGoogle Scholar
  105. Ofek I, Goldhar J, Keisari Y & Sharon N (1995) Nonopsonic phagocytosis of microorganisms. Annu. Rev. Microbiol. 49: 239–276.CrossRefPubMedGoogle Scholar
  106. Pace ML & Cole JJ (1994) Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb. Ecol. 28: 181–193.CrossRefGoogle Scholar
  107. Pace ML & Cole JJ (1996) Regulation of bacteria by resources and predation tested in whole-lake experiments. Limnol. Oceanogr. 41: 1448–1460.Google Scholar
  108. Pearson A (1996) Scavenger receptors in innate immunity. Curr. Opin. Immunol. 8: 20–28.CrossRefPubMedGoogle Scholar
  109. Pernthaler J, Posch T, Šimek K, Vrba J, Amann R & Psenner R (1997) Contrasting bacterial strategies to coexist with a flagellate predator in an experimental microbial assemblage. Appl. Environ. Microbiol. 63: 596–601.PubMedGoogle Scholar
  110. Pernthaler J, Posch T, Šimek K, Vrba J, Pernthaler A, Glöckner FO, Nübel U, Psenner R & Amann R (2001) Predator-specific enrichment of Actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture. Appl. Environ. Microbiol. 67: 2145–2155.CrossRefPubMedGoogle Scholar
  111. Pernthaler J, Sattler B, Šimek K, Schwarzenbacher A & Psenner R (1996) Top-down effects on the size-biomass distribution of a freshwater bacterioplankton community. Aquat. Microb. Ecol. 10: 255–263.Google Scholar
  112. Plante CJ (2000) Role of bacterial exopolymeric capsules in protection from deposit-feeder digestion. Aquat. Microb. Ecol. 21: 211–219.Google Scholar
  113. Plante CJ & Shriver AG (1998) Differential lysis of sedimentary bacteria by Arenicola marina L.: Examination of cell wall structure and exopolymeric capsules as correlates. J. Exp. Mar. Biol. Ecol. 229: 35–52.CrossRefGoogle Scholar
  114. Posch T, Jezbera J, Vrba J, Šimek K, Pernthaler J, Andreatta S & Sonntag B (2001) Size selective feeding in Cyclidium glaucoma (Ciliophora, Scuticociliatida) and its effects on bacterial community structure: A study from a continuous cultivation system. Microb. Ecol. 42: 217–227.CrossRefPubMedGoogle Scholar
  115. Posch T, Šimek K, Vrba J, Pernthaler S, Nedoma J, Sattler B, Sonntag B & Psenner R (1999) Predator-induced changes of bacterial size-structure and productivity studied on an experimental microbial community. Aquat. Microb. Ecol. 18: 235–246.Google Scholar
  116. Psenner R & Sommaruga R (1992) Are rapid changes in bacterial biomass caused by shifts from top-down to bottom-up control? Limnol. Oceanogr. 37: 1092–1100.Google Scholar
  117. Ramoino P (1997) Lectin-binding glycoconjugates in Paramecium primaurelia: changes with cellular age and starvation. Histochem. Cell Biol. 107: 321–329.CrossRefPubMedGoogle Scholar
  118. Roszak DB & Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51: 365–379.PubMedGoogle Scholar
  119. Sakaguchi M, Murakami H & Suzaki T (2001) Involvement of a 40-kDA glycoprotein in food recognition, prey capture, and induction of phagocytosis in the protozoon Actinophrys sol. Protist 152: 33–41.CrossRefPubMedGoogle Scholar
  120. Sanders RW (1988) Feeding by Cyclidium sp. (Ciliophora, Scuticociliatida) on particles of different sizes and surface properties. Bull. mar. Sci. 43: 446–457.Google Scholar
  121. Sanders RW, Leeper DA, King CH & Porter KG (1994) Grazing by rotifers and crustacean zooplankton on nanoplanktonic protists. Hydrobiologia 288: 167–181.CrossRefGoogle Scholar
  122. Sanders RW & Wickham SA (1993) Planktonic protozoa and metazoa: Predation, food quality and population control. Mar. Microb. Food Webs 7: 197–223.Google Scholar
  123. Schäfer H, Bernard L, Courties C, Lebaron P, Servais P, Pukall R, Stackebrandt E, Troussellier M, Guindulain T, Vives-Rego J & Muyzer G (2001) Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations. FEMS Microb. Ecol. 34: 243–253.Google Scholar
  124. Schmaljohann R, Pollingher U & Berman T (1987) Natural populations of bacteria in Lake Kinneret: Observations with scanning electron and epifluorescence microscopy. Microb. Ecol. 13: 1–12.CrossRefGoogle Scholar
  125. Sherr BF, del Giorgio P & Sherr EB (1999) Estimating abundance and single-cell characteristics of respiring bacteria via the redox dye CTC. Aquat. Microb. Ecol. 18: 117–131.Google Scholar
  126. Sherr BF & Sherr EB (1991) Proportional distribution of total numbers, biovolume and bacterivory among size classes of 2-20 µm nonpigmented marine flagellates. Mar. Microb. Food Webs 5: 227–237.Google Scholar
  127. Sherr BF, Sherr EB & Berman T (1982) Decomposition of organic detritus: A selective role for microflagellate protozoa. Limnol. Oceanogr. 27: 765–769.CrossRefGoogle Scholar
  128. Sherr EB (1988) Direct use of high molecular weight polysaccharide by heterotrophic flagellates. Nature 335: 348–351.CrossRefGoogle Scholar
  129. Sherr EB & Sherr BF (1987) High rates of consumption of bacteria by pelagic ciliates. Nature 325: 710–711.CrossRefGoogle Scholar
  130. Sibbald MJ, Albright LJ & Sibbald PR (1987) Chemosensory response of a heterotrophic microflagellate to bacteria and several nitrogen compounds. Mar. Ecol. Prog. Ser. 36: 201–201.Google Scholar
  131. Sih A (1993) Effects of ecological interactions on forager diets: competition, predation risk, parasitism and prey behaviour. In: Hughes RN (Ed) Diet Selection: An Interdisciplinary Approach to Foraging Behaviour (pp 182–211). Blackwell Scientific, Oxford.Google Scholar
  132. Šimek K, Bobkova J, Macek M, Nedoma J & Psenner R (1995) Ciliate grazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: A study at the species and community level. Limnol. Oceanogr. 40: 1077–1090.Google Scholar
  133. Šimek K & Chrzanowski TH (1992) Direct and indirect evidence of size-selective grazing on pelagic bacteria by freshwater nanoflagellates. Appl. Environ. Microbiol. 58: 3715–3720.PubMedGoogle Scholar
  134. Šimek K, Kojecka P, Nedoma J, Hartman P, Vrba J & Dolan JR (1999) Shifts in bacterial community composition associated with different microzooplankton size fractions in a eutrophic reservoir. Limnol. Oceanogr. 44: 1634–1644.Google Scholar
  135. Šimek K, Pernthaler J, Weinbauer MG, Hornak K, Dolan JR, Nedoma J, Masin M & Amann R (2001) Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl. Environ. Microbiol. 67: 2723–2733.CrossRefPubMedGoogle Scholar
  136. Šimek K, Vrba J, Pernthaler J, Posch T, Hartman P, Nedoma J & Psenner R (1997) Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Appl. Environ. Microbiol. 63: 587–595.PubMedGoogle Scholar
  137. Sime-Ngando T, Bourdier G, Amblard C & Pinel Alloul B (1991) Short-term variations in specific biovolumes of different bacterial forms in aquatic ecosystems. Microb. Ecol. 21: 211–226.Google Scholar
  138. Singh B (1942) Toxic effects of certain bacterial metabolic products on soil protozoa. Nature 149: 168.Google Scholar
  139. Snyder RA (1991) Chemoattraction of a bactivorous ciliate to bacteria surface compounds. Hydrobiologia 215: 205–214.CrossRefGoogle Scholar
  140. Sommaruga R & Psenner R (1995) Permanent presence of grazingresistant bacteria in a hypertrophic Lake. Appl. Environ. Microbiol. 61: 3457–3459.PubMedGoogle Scholar
  141. Sterner RW (1989) The role of grazers in phytoplankton succession. In: Sommer U (Ed) Plankton Ecology - Succession in Plankton Communities (pp 107–169). Springer, Berlin.Google Scholar
  142. Stoderegger KE & Herndl GJ (2001) Visualization of the exopolysaccharide bacterial capsule and its distribution in oceanic environments. Aquat. Microb. Ecol. 26: 195–199.Google Scholar
  143. Stoecker DK & Capuzzo JM (1990) Predation on protozoa: its importance to zooplankton. J. Plankton Res. 12: 891–908.Google Scholar
  144. Stoecker DK, Cucci TL, Hulburt EM & Yentsch cm (1986) Selective feeding by Balanion sp. (Ciliata, Balanionidae) on phytoplankton that best support its growth. J. Exp. Mar. Biol. Ecol. 95: 113–130.CrossRefGoogle Scholar
  145. Strom SL (2000) Bacterivory: interactions between bacteria and their grazers. In: Kirchman DL (Ed) Microbial Ecology of the Oceans (pp 351–386). Wiley-Liss, New York.Google Scholar
  146. Sutherland IW (1977) Bacterial exopolysaccharides - their nature and production. In: Sutherland IW (Ed) Surface Carbohydrates of the Procaryotic Cell (pp 27–96). Academic Press, New York.Google Scholar
  147. Suzuki MT (1999) Effect of protistan bacterivory on coastal bacterioplankton diversity. Aquat. Microb. Ecol. 20: 261–272.Google Scholar
  148. Taniguchi A & Takeda Y (1988) Feeding rate and behavior of the tintinnid ciliate Favella taraikaensis observed with a high speed VTR system. Mar. Microb. Food Webs 3: 21–34.Google Scholar
  149. Thingstad T (2000) Control of bacterial growth in idealized food webs. In: Kirchman D (Ed) Microbial Ecology of the Oceans (pp 229–261). Wiley-Liss, New York.Google Scholar
  150. Thingstad TF & Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13: 19–27.Google Scholar
  151. Tollrian R & Harvell C (1999). The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton.Google Scholar
  152. van Donk E, Lürling M & Lampert W (1998) Consumer-induced changes in phytoplankton: Inducibility, costs, benefits, and the impact on grazers. In: Tollrian R & Harvell C (Eds) The Ecology and Evolution of Inducible Defenses (pp 89–103). Princeton University Press, Princeton.Google Scholar
  153. Van Hannen EJ, Veninga M, Bloem J, Gons HJ & Laanbroek HJ (1999) Genetic changes in the bacterial community structure associated with protistan grazers. Arch. Hydrobiol. 145: 25–38.Google Scholar
  154. Verhagen FJM, Duyts H & Laanbroek HJ (1993) Effects of grazing by flagellates on competition for ammonium between nitrifying and heterotrophic bacteria in soil columns. Appl. Environ. Microbiol. 59: 2099–2106.PubMedGoogle Scholar
  155. Verity PG (1991) Feeding in planktonic protozoans: Evidence for non-random acquisition of prey. J. Protozool. 38: 69–76.Google Scholar
  156. Wagner M, Amann R, Kämpfer P, Assmus B, Hartmann A, Hutzler P, Springer N & Schleifer KH (1994) Identification and in situ detection of gram-negative filamentous bacteria in activated sludge. Syst. Appl. Microbiol. 17: 405–417.Google Scholar
  157. Weinbauer MG & Höfle MG (1998) Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Appl. Environ. Microbiol. 64: 431–438.PubMedGoogle Scholar
  158. Wickham SA (1995) Trophic relations between cyclopoid copepods and ciliated protists: Complex interactions link the microbial and classic food webs. Limnol. Oceanogr. 40: 1173–1181.Google Scholar
  159. Wolfe GV (2000) The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts. Biol. Bull. 198: 225–244.PubMedGoogle Scholar
  160. Yamada T, Muramatsu N & Kondo T (1993) Phagocytosis of monosaccharide-binding latex particles by guinea-pig polymorphonuclear leucocytes. J. Biomat. Sci. Polymer Ed. 4: 347–355.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Klaus Jürgens
    • 1
  • Carsten Matz
    • 1
  1. 1.Max Planck Institute for LimnologyPlönGermany

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