Key Points
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The high prokaryotic mortality in pelagic habitats is caused by both viral lysis and predation by ciliated and flagellated protists. Viral lysis is thought to have the greatest effect on prokaryotic community diversity. By contrast, protistan predation might be most influential in limiting the total bacterial abundance and biomasses in the water column, but it also leaves its mark on microbial community composition. This article focuses on the role of protist predation.
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What does protistan predation contribute to the 'microbial loop' in pelagic habitats? According to the microbial loop concept, dissolved organic material that is produced during the flux of particulate matter towards larger organisms is reincorporated by heterotrophic bacteria and archaea. Bacterivorous nanoflagellates form a bridge between those planktonic organisms (the picoplankton) that consume dissolved organic matter and those that can only feed on cells >3–5 mm in diameter. Another point of entry for protists is herbivory, that is, direct feeding on bacterial primary producers, as well as feeding on detritus and competing with bacteria for dissolved organic material. Furthermore, grazing by protists is an important mechanism of nutrient regeneration.
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It is still unclear whether the biomass of prokaryotes in the water column is limited primarily by protistan predation ('top-down control') or by competition for organic carbon and nutrients ('bottom-up control'). However, empirical observations and theoretical models indicate that the mode of control might be influenced by the overall productivity in marine systems. In fresh water, the situation seems to be more complex.
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A significant proportion of microbial activity in pelagic habitats occurs on, or near, particles known as marine snow or lake snow. Bacteria on such aggregates cannot escape from protistan predation; in fact, protists are more efficient in collecting suspended bacteria if they are attached to a surface than if they are free-living.
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Not all members of the bacterioplankton are equal in the eyes of their protistan predators. The selective grazing pressure that protistan predators can exert on mixed bacterial assemblages at high particle concentrations is a function of both selective uptake and differential digestion (for example, it is more time-consuming to digest a Gram-positive cell than a Gram-negative cell). At low bacterial concentrations, feeding selectivity decreases.
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Owing to this selective foraging, protistan predation represents another mechanism (besides viral lysis) that can shape the structure of microbial communities in pelagic habitats.
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The grazing pressure exerted by protists has not 'gone unnoticed' by their microbial prey. Aquatic bacteria have evolved various anti-predator strategies, which include exopolymer secretion, filament formation, high-speed motility, cell miniaturization and toxin production. It is therefore conceivable that bacterivory by protists has shaped microbial evolution as profoundly as, for example, oxygenic photosynthesis.
Abstract
The oxic realms of freshwater and marine environments are zones of high prokaryotic mortality. Lysis by viruses and predation by ciliated and flagellated protists result in the consumption of microbial biomass at approximately the same rate as it is produced. Protist predation can favour or suppress particular bacterial species, and the successful microbial groups in the water column are those that survive this selective grazing pressure. In turn, aquatic bacteria have developed various antipredator strategies that range from simply 'outrunning' protists to the production of highly effective cytotoxins. This ancient predator–prey system can be regarded as an evolutionary precursor of many other interactions between prokaryotic and eukaryotic organisms.
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References
Schut, F., Prins, R. A. & Gottschal, J. C. Oligotrophy and pelagic marine bacteria: facts and fiction. Aquat. Microb. Ecol. 12, 177–202 (1997).
Morita, R. Y. in Bacteria in Oligotrophic Environments: Starvation-Survival Lifestyle, 529 (Chapman Hall, New York, 1997).
Thingstad, T. F. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45, 1320–1328 (2000). First systematic attempt to model the partitioning of bacterial production between protistan grazers and viruses.
Fuhrman, J. A. & Noble, R. T. Viruses and protists cause similar bacterial mortality in coastal seawaters. Limnol. Oceanogr. 40, 1236–1242 (1995).
Strom, S. L. in Microbial Ecology of the Oceans (ed. Kirchman, D. L.) 351–386 (J. Wiley & Son, New York, 2000).
Sommaruga, R., Obernosterer, I., Herndl, G. J. & Psenner, R. Inhibitory effect of solar radiation on thymidine and leucine incorporation by freshwater and marine bacterioplankton. Appl. Environ. Microbiol. 63, 4178–4184 (1997).
Bidle, K. D. & Falkowski, P. G. Cell death in planktonic, photosynthetic microorganisms. Nature Rev. Microbiol. 2, 643–655 (2004).
Weinbauer, M. G., Christaki, U., Nedoma, A. & Šimek, K. Comparing the effects of resource enrichment and grazing on viral production in a meso-eutrophic reservoir. Aquat. Microb. Ecol. 31, 137–144 (2003).
Weinbauer, M. G., Brettar, I. & Höfle, M. G. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol. Oceanogr. 48, 1457–1465 (2003).
Weinbauer, M. G. & Höfle, M. G. Size-specific mortality of lake bacterioplankton by natural virus communities. Aquat. Microb. Ecol. 15, 103–113 (1998).
Nagasaki, K., Ando, M., Imai, I., Itakura, S. & Ishida, Y. Virus-like particles in unicellular apochlorotic microorganisms in the coastal water of Japan. Fish. Sci. 61, 235–239 (1995).
Gowing, M. M. Large viruses and infected microeukaryotes in Ross Sea summer pack ice habitats. Mar. Biol. 142, 1029–1040 (2003).
Weinbauer, M. G. & Rassoulzadegan, F. Are viruses driving microbial diversification and diversity? Environ. Microbiol. 6, 1–11 (2004).
Verity, P. Feeding in planktonic protozoans, evidence for non-random acquisition of prey. J. Protozool. 38, 69–76 (1991).
Matz, C., Boenigk, J., Arndt, H. & Jürgens, K. Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquat. Microb. Ecol. 27, 137–148 (2002).
Beardsley, C., Pernthaler, J., Wosniok, W. & Amann, R. Are readily cultured bacteria in coastal North Sea waters suppressed by selective grazing mortality? Appl. Environ. Microbiol. 69, 2624–2630 (2003).
Gonzalez, J. M., Sherr, E. B. & Sherr, B. F. Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. Environ. Microbiol. 56, 583–589 (1990).
Šimek, K., Vrba, J. & Hartman, P. Size-selective feeding by Cyclidium sp. on bacterioplankton and various sizes of cultured bacteria. FEMS Microbiol. Ecol. 14, 157–167 (1994).
Sonntag, B., Posch, T. & Psenner, R. Comparison of three methods for determining flagellate abundance, cell size, and biovolume in cultures and natural freshwater samples. Arch. Hydrobiol. 149, 337–351 (2000).
Lim, E. L., Dennett, M. R. & Caron, D. A. The ecology of Paraphysomonas imperforata based on studies employing oligonucleotide probe identification in coastal water samples and enrichment cultures. Limnol. Oceanogr. 44, 37–51 (1999). Describes the population dynamics and growth of a marine protistan species identified by molecular biological techniques.
Cleven, E. J. & Weisse, T. Seasonal succession and taxon-specific bacterial grazing rates of heterotrophic nanoflagellates in Lake Constance. Aquat. Microb. Ecol. 23, 147–161 (2001).
Šimek, K. et al. Community structure, picoplankton grazing and zooplankton control of heterotrophic nanoflagellates in a eutrophic reservoir during the summer phytoplankton maximum. Aquat. Microb. Ecol. 12, 49–63 (1997).
Boenigk, J. & Arndt, H. Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Antonie Van Leeuwenhoek 81, 465–480 (2002).
Moon-van der Staay, S. Y., De Wachter, R. & Vaulot, D. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409, 607–610 (2001).
Massana, R., Guillou, L., Diez, B. & Pedros-Alio, C. Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl. Environ. Microbiol. 68, 4554–4558 (2002). Molecular identification of abundant uncultured marine flagellates and proof of their bacterivory in the field.
Šimek, K., Jurgens, K., Nedoma, J., Comerma, M. & Armengol, J. Ecological role and bacterial grazing of Halteria spp.: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. Aquat. Microb. Ecol. 22, 43–56 (2000).
Pierce, R. W. & Turner, J. T. Ecology of planktonic ciliates in marine food webs. Rev. Aquat. Sci. 6, 139–181 (1992).
Rappe, M. S. & Giovannoni, S. J. The uncultured microbial majority. Annu. Rev. Microbiol. 57, 369–394 (2003).
Zwart, G., Crump, B. C., Agterveld, M., Hagen, F. & Han, S. K. Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat. Microb. Ecol. 28, 141–155 (2002).
Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–810 (2002).
Karner, M., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–509 (2001).
Selje, N., Simon, M. & Brinkhoff, T. A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427, 445–448 (2004).
Eilers, H. et al. Isolation of novel pelagic bacteria from the German Bight and their seasonal contribution to surface picoplankton. Appl. Environ. Microbiol. 67, 5134–5142 (2001).
Cottrell, M. T. & Kirchman, D. L. Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization. Appl. Environ. Microbiol. 66, 5116–5122 (2000).
Pernthaler, J., Zöllner, E., Warnecke, F. & Jürgens, K. Blooms of filamentous bacteria in a mesotrophic lake: Identity and potential controlling mechanisms. Appl. Environ. Microbiol. 70, 6272–6281 (2004). Molecular identification and population dynamics of grazing-resistant filamentous bacteria in a lake.
Burkert, U., Warnecke, F., Babenzien, D., Zwirnmann, E. & Pernthaler, J. Members of a readily enriched β-proteobacterial clade are common in the surface waters of a humic lake. Appl. Environ. Microbiol. 69, 6550–6559 (2003).
Šimek, K. et al. Changes in bacterial community composition, dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl. Environ. Microbiol. 67, 2723–2733 (2001). Experimental field study that describes the combined effect of protistan grazing and viruses on microbial community structure in a reservoir.
Sekar, R. et al. An improved protocol for the quantification of freshwater actinobacteria by fluorescence in situ hybridization. Appl. Environ. Microbiol. 69, 2928–2935 (2003).
Weisse, T. D in Advances in Microbial Ecology Vol. 13 (ed. Jones, J. G.) 327–370 (Plenum, New York, 1993).
Azam, F. et al. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263 (1983).
Jürgens, K., Wickham, S. A., Rothhaupt, K. O. & Santer, B. Feeding rates of macro- and microzooplankton on heterotrophic nanoflagellates. Limnol. Oceanogr. 41, 1833–1839 (1996).
Strom, S. L., Benner, R., Ziegler, S. & Dagg, M. J. Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol. Oceanogr. 42, 1364–1374 (1997).
Lampert, W. Release of dissolved organic carbon by grazing zooplankton. Limnol. Oceanogr. 23, 831–834 (1978).
Sherr, E. B. Direct use of high molecular-weight polysaccharide by heterotrophic flagellates. Nature 335, 348–351 (1988).
Posch, T. & Arndt, H. Uptake of sub-micrometre- and micrometre-sized detrital particles by bacterivorous and omnivorous ciliates. Aquat. Microb. Ecol. 10, 45–53 (1996).
González, J. M. & Suttle, C. A. Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar. Ecol. Prog. Ser. 94, 1–10 (1993).
Caron, D. A., Lim, E. L., Miceli, G., Waterbury, J. B. & Valois, F. W. Grazing and utilization of chroococcoid cyanobacteria and heterotrophic bacteria by protozoa in laboratory cultures and a coastal plankton community. Mar. Ecol. Prog. Ser. 76, 205–217 (1991).
Pernthaler, J. et al. Short-term changes of protozoan control on autotrophic picoplankton in an oligo-mesotrophic lake. J. Plankton Res. 18, 443–462 (1996).
Sherr, E. B., Sherr, B. F. & McDaniel, J. Clearance rates of less than 6 mm fluorescently labeled algae (FLA) by estuarine protozoa: Potential grazing impact of flagellates and ciliates. Mar. Ecol. Prog. Ser. 69, 81–92 (1991).
Sherr, E. B. & Sherr, B. F. Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek 81, 293–308 (2002).
Elser, J. J., Marzolf, E. R. & Goldman, C. R. Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: a review and critique of experimental enrichments. Can. J. Fish. Aquat. Sci. 47, 1468–1477 (1990).
Thingstad, T. F., Zweifel, U. L. & Rassoulzadegan, F. P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnol. Oceanogr. 43, 88–94 (1998).
Simon, M. & Azam, F. Protein content and protein synthesis rates of planktonic marine bacteria. Mar. Ecol. Prog. Ser. 51, 201–213 (1989).
Sherr, B. F., Sherr, E. B. & Berman, T. Grazing, growth, and ammonium excretion rates of a heterotrophic microflagellate fed with 4 species of bacteria. Appl. Environ. Microbiol. 45, 1196–1201 (1983).
Nagata, T. & Kirchman, D. L. Release of dissolved free and combined amino acids by bacterivorous marine flagellates. Limnol. Oceanogr. 36, 433–443 (1991).
Caron, D. A., Goldman, J. C. & Dennett, M. R. Experimental demonstration of the roles of bacteria and bacterivorous protozoa in plankton nutrient cycles. Hydrobiologia 159, 27–40 (1988).
Kirchman, D. L. The uptake of inorganic nutrients by heterotrophic bacteria. Microb. Ecol. 28, 255–271 (1994).
Sanders, R. W., Caron, D. A. & Berninger, U. G. Relationship between bacteria and heterotrophic nanoplankton in marine and freshwaters: an inter-ecosystem comparison. Mar. Ecol. Prog. Ser. 86, 1–14 (1992).
Gasol, J. M. & Vaque, D. Lack of coupling between heterotrophic nanoflagellates and bacteria — a general phenomenon across aquatic systems. Limnol. Oceanogr. 38, 657–665 (1993).
Nakano, S., Ishii, N., Manage, P. M. & Kawabata, Z. Trophic roles of heterotrophic nanoflagellates and ciliates among planktonic organisms in a hypereutrophic pond. Aquat. Microb. Ecol. 16, 153–161 (1998).
Sherr, E. B. & Sherr, B. F. High rates of consumption of bacteria by pelagic ciliates. Nature 325, 710–711 (1987).
Hairston, N. G., Smith, F. E. & Slobodkin, L. B. Community structure, population control, and competition. Am. Nat. 94, 421–425 (1960). This paper does not deal with bacteria or protists, but rather explores the question of why “the world is green”.
Pace, M. L. & Cole, J. J. Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb. Ecol. 28, 181–193 (1994).
del Giorgio, P. A. et al. Bacterioplankton community structure: protists control net production and the proportion of active bacteria in a coastal marine community. Limnol. Oceanogr. 41, 1169–1179 (1996). An elegant experimental field study of how protists control the activity of bacterial communities.
Gasol, J. M., Pedros-Alio, C. & Vaqué, D. Regulation of bacterial assemblages in oligotrophic plankton systems: results from experimental and empirical approaches. Antonie Van Leeuwenhoek 81, 435–452 (2002).
Münster, U. Concentrations and fluxes of organic carbon substrates in the aquatic environment. Antonie Van Leeuwenhoek 63, 243–274 (1993).
Billett, D. S. M., Lampitt, R. S., Rice, A. L. & Mantoura, R. F. C. Seasonal sedimentation of phytoplankton to the deep sea benthos. Nature 302, 520–522 (1983).
Gasol, J. M. A framework for the assessment of top-down vs bottom-up control of heterotrophic nanoflagellate abundance. Mar. Ecol. Prog. Ser. 113, 291–300 (1994). A comprehensive compilation and analysis of field data, which indicates that the control of bacterial assemblages might be related to ecosystem productivity.
Thingstad, T. F. & Lignell, R. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13, 19–27 (1997).
Šimek, K. et al. Changes in the epilimnetic bacterial community composition, production, and protist-induced mortality along the longitudinal axis of a highly eutrophic reservoir. Microb. Ecol. 42, 359–371 (2001).
Jürgens, K. Impact of Daphnia on planktonic microbial food webs — a review. Mar. Microb. Food Webs 8, 295–324 (1994).
Alldredge, A. & Silver, M. Characteristics, dynamics and significance of marine snow. Prog. Oceanogr. 20, 41–82 (1988).
Grossart, H. P. & Simon, M. Limnetic macroscopic organic aggregates (lake snow): occurrence, characteristics, and microbial dynamics in Lake Constance. Limnol. Oceanogr. 38, 532–546 (1993).
Blackburn, N., Fenchel, T. & Mitchell, J. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science. 282, 2254–2256 (1998).
Caron, D. A. Grazing of attached bacteria by heterotrophic microflagellates. Microb. Ecol. 13, 203–218 (1987).
Caron, D. A. in The Biology of Free-living Heterotrophic Flagellates Vol. 45 (ed. Patterson, D. A.) 77–92 (Clarendon Press, Oxford, 1991).
Kiorboe, T., Tang, K., Grossart, H. P. & Ploug, H. Dynamics of microbial communities on marine snow aggregates: colonization, growth, detachment, and grazing mortality of attached bacteria. Appl. Environ. Microbiol. 69, 3036–3047 (2003).
Fenchel, T. & Blackburn, N. Motile chemosensory behaviour of phagotrophic protists: mechanisms for and efficiency in congregating at food patches. Protist 150, 325–336 (1999).
Jonsson, P. R., Johansson, M. & Pierce, R. W. Attachment to suspended particles may improve foraging and reduce predation risk for tintinnid ciliates. Limnol. Oceanogr. 49, 1907–1914 (2004).
Šimek, K., Jezbera, J., Hornak, K., Vrba, J. & Sed'a, J. Role of diatom-attached choanoflagellates of the genus Salpingoeca as pelagic bacterivores. Aquat. Microb. Ecol. 36, 257–269 (2004).
Fenchel, T. Protozoan filter feeding. Progr. Protistol. 1, 65–113 (1986).
Boenigk, J. Variability of ingestion rates with stage in cell cycle of a heterotrophic nanoflagellate (Spumella sp.) measured by an individual-based approach. Eur. J. Protistol. 38, 299–306 (2002). Observations on the feeding behaviour of a heterotrophic flagellate during the cell cycle using means of video microscopy.
Jürgens, K. & Matz, C. Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek 81, 413–434 (2002).
Shimeta, J. Diffusional encounter of submicrometer particles and small cells by suspension feeders. Limnol. Oceanogr. 38, 456–465 (1993).
González, J. M., Sherr, E. B. & Sherr, B. F. Size selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. Environ. Microbiol. 56, 583–589 (1990). Laboratory experiments describing size-selective prey uptake by heterotrophic flagellates.
Monger, B. C. & Landry, M. R. Prey size dependency of grazing by freeliving marine flagellates. Mar. Ecol. Prog. Ser. 74, 239–248 (1991).
Boenigk, J., Stadler, P., Wiedlroither, A. & Hahn, M. W. Strain-specific differences in the grazing sensitivities of closely related ultramicrobacteria affiliated with the Polynucleobacter cluster. Appl. Environ. Microbiol. 70, 5787–5793 (2004).
Wu, O. L. L., Boenigk, J. & Hahn, M. W. Successful predation of filamentous bacteria by a nanoflagellate challenges current models of flagellate bacterivory. Appl. Environ. Microbiol. 70, 332–339 (2004).
Sherr, B. F., Sherr, E. B. & Rassoulzadegan, F. Rates of digestion of bacteria by marine phagotrophic protozoa: temperature dependence. Appl. Environ. Microbiol. 54, 1091–1095 (1988).
González, J. M., Iriberri, J., Egea, L. & Barcina, I. Differential rates of digestion of bacteria by freshwater and marine phagotrophic protozoa. Appl. Environ. Microbiol. 56, 1851–1857 (1990).
Boenigk, J., Matz, C., Jürgens, K. & Arndt, H. Food concentration-dependent regulation of food selectivity of interception-feeding bacterivorous nanoflagellates. Aquat. Microb. Ecol. 27, 195–202 (2002).
Hansen, P. J., Bjornsen, P. K. & Hansen, B. W. Zooplankton grazing and growth: scaling within the 2–2,000-mm body size range. Limnol. Oceanogr. 42, 687–704 (1997).
Šimek, K., Macek, M., Pernthaler, J., Straskrabova, V. & Psenner, R. Can freshwater planktonic ciliates survive on a diet of picoplankton? J. Plankton Res. 18, 597–613 (1996).
Jürgens, K. & DeMott, W. D. Behavioural flexibility in prey detection by bacterivorous flagellates. Limnol. Oceanogr. 40, 1503–1507 (1995).
Boenigk, J. & Novarino, G. Effect of suspended clay on the feeding and growth of bacterivorous flagellates and ciliates. Aquat. Microb. Ecol. 34, 181–192 (2004).
Weisse, T. The significance of inter- and intraspecific variation in bacterivorous and herbivorous protists. Antonie Van Leeuwenhoek 81, 327–341 (2002).
Sanders, R. W. Mixotrophic protists in marine and freshwater ecosystems. J. Protozool. 38, 76–81 (1991).
Raven, J. A. Phagotrophy in phototrophs. Limnol. Oceanogr. 42, 198–205 (1997).
Nygaard, K. & Tobiesen, A. Bacterivory in algae: a survival strategy during nutrient limitation. Limnol. Oceanogr. 38, 273–279 (1993).
Caron, D. A., Porter, K. G. & Sanders, R. W. Carbon, nitrogen, and phosphorus budgets for the mixotrophic phytoflagellate Poterioochromonas malhamensis (Chrysophyceae) during bacterial ingestion. Limnol. Oceanogr. 35, 433–443 (1990). Laboratory study that explores the ecological consequences of protistan mixotrophy.
Thingstad, T. F., Havskum, H., Garde, K. & Riemann, B. On the strategy of 'eating your competitor': a mathematical analysis of algal mixotrophy. Ecology 77, 2108–2118 (1996).
Medina-Sanchez, J. M., Villar-Argaiz, M. & Carrillo, P. Neither with nor without you: a complex algal control on bacterioplankton in a high mountain lake. Limnol. Oceanogr. 49, 1722–1733 (2004).
Hahn, M. W., Moore, E. R. B. & Höfle, M. G. Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Appl. Environ. Microbiol. 65, 25–35 (1999).
Matz, C. & Jürgens, K. High motility reduces grazing mortality of planktonic bacteria. Appl. Environ. Microbiol. 71, 921–929 (2005).
Matz, C. et al. Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates. Appl. Environ. Microbiol. 70, 1593–1599 (2004). Describes bacteria that kill their predators with toxins that are specifically induced by quorum sensing.
Rappe, M. S., Connon, S. A., Vergin, K. L. & Giovannoni, S. J. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418, 630–633 (2002).
Hahn, M. W. et al. Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Appl. Environ. Microbiol. 69, 1442–1451 (2003).
Jiang, X. P. & Chai, T. J. Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Appl. Environ. Microbiol. 62, 1300–1305 (1996).
Schauer, M. & Hahn, M. Diversity and phylogenetic affiliations of morphologically conspicuous large filamentous bacteria occurring in the pelagic zones of a broad spectrum of freshwater habitats. Appl. Environ. Microbiol. 71, 1931–1940 (2005).
Shikano, S., Luckinbill, L. S. & Kurihara, Y. Changes of traits in a bacterial population associated with protozoal predation. Microb. Ecol. 20, 75–84 (1990).
Hahn, M. W. & Höfle, M. G. 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 (1998). Co-culture study of two bacteria showing that flagellate predation specifically favoured the growth of the filament-forming species.
Flemming, H. C. & Wingender, J. Relevance of microbial extracellular polymeric substances (EPSs) — Part I: Structural and ecological aspects. Water Sci. Technol. 43, 1–8 (2001).
Matz, C., Bergfeld, T., Rice, S. A. & Kjelleberg, S. Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ. Microbiol. 6, 218–226 (2004).
Hahn, M. W., Lunsdorf, H. & Janke, L. Exopolymer production and microcolony formation by planktonic freshwater bacteria: defence against protistan grazing. Aquat. Microb. Ecol. 35, 297–308 (2004).
Iriberri, J., Azua, I., Labirua-Iturburu, A., Artolozaga, I. & Barcina, I. Differential elimination of enteric bacteria by protists in a freshwater system. J. Appl. Bacteriol. 77, 476–483 (1994).
Jezbera, J., Hornak, K. & Simek, K. Food selection by bacterivorous protists: insight from the analysis of the food vacuole content by means of fluorescence in situ hybridization. FEMS Microbiol. Ecol. (in the press).
Matz, C. & Jürgens, K. Effects of hydrophobic and electrostatic cell surface properties of bacteria on feeding rates of heterotrophic nanoflagellates. Appl. Environ. Microbiol. 67, 814–820 (2001).
Monger, B. C., Landry, M. R. & Brown, S. L. Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey. Limnol. Oceanogr. 44, 1917–1927 (1999).
Absolom, D. R. The role of bacterial hydrophobicity in infection: bacterial adhesion and phagocytic ingestion. Can. J. Microbiol. 34, 287–298 (1988).
González, J. M., Sherr, E. B. & Sherr, B. F. Differential feeding by marine flagellates on growing versus starving, and on motile versus nonmotile, bacterial prey. Mar. Ecol. Prog. Ser. 102, 257–267 (1993).
Güde, H. Direct and indirect influences of crustacean zooplankton on bacterioplankton of Lake Constance. Hydrobiologia 159, 63–73 (1988).
Jürgens, K. & Güde, H. The potential importance of grazing-resistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112, 169–188 (1994). Compilation of ecological observations about aquatic bacteria that resist protistan grazing.
Pernthaler, J., Sattler, B., Šimek, K., Schwarzenbacher, A. & Psenner, R. Top-down effects on the size-biomass distribution of a freshwater bacterioplankton community. Aquat. Microb. Ecol. 10, 255–263 (1996).
Vrba, J. et al. Massive occurrence of heterotrophic filaments in acidified lakes: seasonal dynamics and composition. FEMS Microbiol. Ecol. 46, 281–294 (2003).
Jürgens, K., Arndt, H. & Zimmermann, H. Impact of metazoan and protozoan grazers on bacterial biomass distribution in microcosm experiments. Aquat. Microb. Ecol. 12, 131–138 (1997).
Posch, T. et al. Predator-induced changes of bacterial size-structure and productivity studied on an experimental microbial community. Aquat. Microb. Ecol. 18, 235–246 (1999).
Šimek, K. et al. Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Appl. Environ. Microbiol. 63, 587–595 (1997).
Sherr, B. F., Sherr, E. B. & McDaniel, J. Effect of protistan grazing on the frequency of dividing cells in bacterioplankton assemblages. Appl. Environ. Microbiol. 58, 4371–4378 (1992).
Vaque, D., Casamayor, E. O. & Gasol, J. M. Dynamics of whole community bacterial production and grazing losses in seawater incubations as related to the changes in the proportions of bacteria with different DNA content. Aquat. Microb. Ecol. 25, 163–177 (2001).
Šimek, K. et al. Comparing the effects of resource enrichment and grazing on a bacterioplankton community of a meso-eutrophic reservoir. Aquat. Microb. Ecol. 31, 123–135 (2003).
Matz, C. & Jürgens, K. Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb. Ecol. 45, 384–398 (2003).
Tansley, A. G. & Adamson, R. S. Studies of the vegetation of the English chalk III: The chalk grasslands of Hampshire–Sussex border. J. Ecol. 13, 177–223 (1925).
Pernthaler, J. et al. Predator-specific enrichment of actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture. Appl. Environ. Microbiol. 67, 2145–2155 (2001).
Hahn, M. W. & Höfle, M. G. 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 (1999).
Suzuki, M. T. Effect of protistan bacterivory on coastal bacterioplankton diversity. Aquat. Microb. Ecol. 20, 261–272 (1999).
Jürgens, K., Pernthaler, J., Schalla, S. & Amann, R. Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl. Environ. Microbiol. 65, 1241–1250 (1999).
Macek, M., Carlos, G., Memije, P. & Ramirez, P. Ciliate Vibrio cholerae interactions within a microbial loop: an experimental study. Aquat. Microb. Ecol. 13, 257–266 (1997).
Arndt, H. et al. in The Flagellates (eds Leadbeater, B. S. C. & Green, J. C.) 240–268 (Taylor & Francis, London, 2000).
Massana, R. & Jürgens, K. Composition and population dynamics of planktonic bacteria and bacterivorous flagellates in seawater chemostat cultures. Aquat. Microb. Ecol. 32, 11–22 (2003).
Šimek, K., Nedoma, J., Pernthaler, J., Posch, T. & Dolan, J. R. Altering the balance between bacterial production and protistan bacterivory triggers shifts in freshwater bacterial community composition. Antonie Van Leeuwenhoek 81, 453–463 (2002).
Caron, D. A., Gast, R. J., Lim, E. L. & Dennett, M. R. Protistan community structure: molecular approaches for answering ecological questions. Hydrobiologia 401, 215–227 (1999).
Cottrell, M. T. & Kirchman, D. L. 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 (2000).
Zubkov, M. V. et al. Linking the composition of bacterioplankton to rapid turnover of dissolved dimethylsulfoniopropionate in an algal bloom in the North Sea. Environ. Microbiol. 3, 304–311 (2001).
Cavalier-Smith, T. The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int. J. Syst. Evol. Microbiol. 52, 297–354 (2002).
Bhattacharya, D. & Medlin, L. The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. J. Phycol. 31, 489–498 (1995).
Molmeret, M., Horn, M., Wagner, M., Santic, M. & Abu Kwaik, Y. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 71, 20–28 (2005).
Wright, R. T. & Coffin, R. B. Measuring microzooplankton grazing on planktonic marine bacteria by its impact on bacterial production. Microb. Ecol. 10, 137–149 (1984).
Acknowledgements
I thank my students and colleagues for the inspiring discussions and bitter controversies that have helped to shape my understanding of aquatic microbial food webs. Valuable suggestions by three reviewers have greatly improved the text. This work was supported by the European Union and by the Max-Planck Society.
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Glossary
- PELAGIC HABITAT
-
The parts of a lake, river and ocean that make up the water column.
- OLIGOTROPHIC
-
An aquatic environment that has low levels of nutrient and algal photosynthetic production (for example, high mountain lakes).
- PHAGOTROPHY
-
The uptake of particles by eukaryotic cells.
- BACTERIOPLANKTON
-
Bacteria that inhabit the water column of lakes and oceans, either freely suspended or attached to particles.
- OMNIVORY
-
Ability of animals to feed on different types of prey.
- HETEROTROPHY
-
The acquisition of metabolic energy by consumption of particulate or dissolved organic matter.
- BACTERIVOROUS NANOFLAGELLATES
-
Small, flagellated protists that range in size from 3 to 15 mm and that can feed on bacteria.
- PICOPLANKTON
-
Organisms suspended in the water column that are less than 2 mm in size.
- DETRITAL PARTICLES
-
Dead organic material suspended in the water column.
- PRIMARY PRODUCERS
-
Organisms that are the original source of organic material in an ecosystem — plants, algae or chemosynthetic microorganisms.
- AUTOTROPHY
-
The acquisition of metabolic energy from the fixation of inorganic carbon, for example, by photo- or chemosynthesis.
- EUPHOTIC ZONE
-
Upper realms of the oceans that are penetrated by sufficient amounts of light for the growth of photosynthetic organisms.
- HERBIVORY
-
The consumption of plants.
- NUTRIENT REGENERATION
-
Processes by which nutrients that are bound in organismic biomass are retransformed into their inorganic form.
- TOP-DOWN CONTROL
-
Ecological scenario in which the abundance or biomass of organisms is mainly determined by mortality owing to predation.
- BOTTOM-UP CONTROL
-
Ecological scenario in which the abundance or biomass of organisms is mainly determined by a lack of resources and mortality owing to starvation.
- EUTROPHIC
-
Aquatic systems with high availability of dissolved organic matter from photosynthetic production or other sources. Examples include shallow lowland lakes and coastal estuaries.
- CHEMOSPHERE
-
Zone of elevated concentration of organic molecules that diffuse from the surface of a suspended particle.
- CHEMOTAXIS
-
Ability of microorganisms to follow a chemical gradient.
- FILTER FEEDING
-
Feeding mode that filters particles from the water by means of a sieving structure. Usually the prey is very small compared with the predator.
- INTERCEPTION FEEDING
-
The capture of individual bacteria or particles by direct random contact with a protistan cell. Usually the sizes of the predator and prey are similar.
- PHOTOTROPHS
-
Organisms that fix inorganic carbon using light energy.
- MIXOTROPHS
-
Organisms that are part autotrophic and part heterotrophic, for example, carnivorous plants.
- ULTRAMICROBACTERIA
-
Bacteria that maintain cell volumes of <0.1 mm3 even during exponential growth on rich media.
- QUORUM SENSING
-
Bacterial communication system based on the secretion and detection of a quorum, which is a substance that increases with population density and that induces expression of specific genes in the population above a threshold concentration.
- APOPTOTIC RESPONSE
-
Phenotypic changes that occur during programmed cell death in eukaryotic cells, for example, cell shrinkage.
- SPECIES RICHNESS
-
Number of species that are present in a community.
- COMMUNITY EVENNESS
-
Balance of the respective number of individuals in each species of a community.
- FEAST OR FAMINE
-
Growth strategy of microorganisms that rapidly proliferate if conditions are optimal and that can survive extended periods of starvation.
- ECOPHYSIOLOGICAL APPROACHES
-
Determination of protistan physiological properties under field conditions, for example, of feeding rates through uptake of surrogate particles.
- MOLECULAR BIOLOGICAL APPROACHES
-
Cultivation-independent identification of protists in environmental samples by sequencing of rRNA genes and fluorescence in situ hybridization with rRNA-targeted probes.
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Pernthaler, J. Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3, 537–546 (2005). https://doi.org/10.1038/nrmicro1180
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DOI: https://doi.org/10.1038/nrmicro1180
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