AiM  Vol.3 No.3 , July 2013
Are Small Grazers and/or Viruses a Structuring Factor of the Free-Living Bacterial Community in Lake Geneva?
ABSTRACT

Two experiments were conducted to test whether viruses, small auto- and heterotrophic nanoflagellates were key factors regulating at relatively short-term (4 days) and nearby periods (April vs. May) the bacterial community in surface waters of Lake Geneva. 2.5 L containing polycarbonate bottles were incubated in situ with either <2 μm or <10 μm filtered water with additions of either virus-free water or a viral concentrate. Abundances of viruses, prokaryotes and small autotrophs were obtained each day using flow cytometry, while bacterial richness was assessed using 16S rDNA PCR-DGGE and auto- and heterotrophic flagellates counted with epifluorescence microscopy at t0 and t96. Transmission electron microscopy was also used to assess virus-induced bacterial mortality at the start and the end of the experiments. Cloning-sequencing was applied on PCR products obtained after excision of selected DGGE bands to highlight more specifically the identity of bacteria of interest in the context of the experiment. The autotrophs and grazer presence and/or the virus enrichment resulted in different effects on the structure of the bacterial community and the impact was also different with the period. In May, bacterial structure changes seemed to be related to the impact or influence of the eukaryotes (including nanoflagellate grazers), while viruses might have a higher impact on the bacterial community structure the month before. This study provides new persuasive evidence that the presence of viruses and small eukaryotes are likely to drive bacterial community composition and shifts on the short-term in lacustrine ecosystems. More interestingly, such effects seem to be different between viruses and grazers, the ones sustaining, the others reducing bacterial community composition.


Cite this paper
S. Jacquet, I. Domaizon, C. Chardon and S. Personnic, "Are Small Grazers and/or Viruses a Structuring Factor of the Free-Living Bacterial Community in Lake Geneva?," Advances in Microbiology, Vol. 3 No. 3, 2013, pp. 233-248. doi: 10.4236/aim.2013.33035.
References
[1]   S. Personnic, I. Domaizon, T. Sime-Ngando, et al., “Seasonal Variations of Microbial Abundances and Virus-Versus Flagellate-Induced Mortality of Picoplankton in Three Peri-Alpine Lakes,” Journal of Plant Research, Vol. 31, No. 10, 2009, pp. 1161-1177. doi:10.1093/plankt/fbp057

[2]   R. Bertoni, C. Callieri, G. Corno, et al., “Long-Term Trends of Epilimnetic and Hypolimnetic Bacteria and Organic Carbon in a Deep Holo-Oligomictic Lake,” Hydrobiology, Vol. 644, No. 1, 2010, pp. 279-287. doi:10.1007/s10750-010-0150-x

[3]   D. Kirchman, H. Ducklow and R. Mitchell, “Estimates of Bacterial Growth from Changes in Uptake Rates and Biomass,” Applied and Environmental Microbiology, Vol. 44, No. 6, 1982, pp. 1296-1307.

[4]   F. Azam, T. Fenchel, J. G. Field, et al., “The Ecological Role of Water-Column Microbes in the Sea,” Marine Ecology Progress Series, Vol. 10, 1983, pp. 257-263. doi:10.3354/meps010257

[5]   R. W. Sanders, K. G. Porter, S. J. Bennett, et al., “Seasonal Patterns of Bacterivory by Flagellates, Ciliates, Rotifers and Cladocerans in a Freshwater Planktonic Community,” Limnology and Oceanography, Vol. 34, No. 4, 1989, pp. 673-687. doi:10.4319/lo.1989.34.4.0673

[6]   T. Fenchel, “The Microbial Loop—25 Years Later,” Journal of Experimental Marine Biology and Ecology, Vol. 366, No. 1-2, 2008, pp. 99-103. doi:10.1016/j.jembe.2008.07.013

[7]   E. S. Lindsrtom, “Investigating Influential Factors on Bacterioplankton Community Composition: Results from a Field Study on Five Mesotrophic Lakes,” Microbial Ecology, Vol. 42, No. 4, 2001, pp. 598-605. doi:10.1007/s00248-001-0031-y

[8]   L. Jardillier, Y. Bettarel, M. Richardot, et al., “Effects of Viruses and Predators on Prokaryotic Community Composition,” Microbial Ecology, Vol. 50, No. 4, 2005, pp. 557-569. doi:10.1007/s00248-005-5030-y

[9]   I. Hewson and J. A. Fuhrman, “Viral Impacts upon Marine Bacterioplankton Assemblage Structure,” Journal of the Marine Biological Association of the United Kingdom, Vol. 86, No. 3, 2006, pp. 577-589. doi:10.1017/S002531540601349X

[10]   I. Hewson and J. A. Fuhrman, “Co-Variation of Viral Parameters with Bacterial Assemblage Richness and Diversity in the Water Column and Sediments,” Deep-Sea Research Part I, Vol. 54, No. 5, 2007, pp. 811-830. doi:10.1016/j.dsr.2007.02.003

[11]   L. Berdjeb, J. F. Ghiglione and S. Jacquet, “Bottom-Up vs. Top-Down Factors Regulating the Bacterial Community Structure in Two Peri-Alpine Lakes,” Applied and Environmental Microbiology, Vol. 77, No. 11, 2011, pp. 3591-3599. doi:10.1128/AEM.02739-10

[12]   M. G. Hofle, M. W. Hahn and E. R. Moore, “Bacterial Filament Formation, a Defense Mechanism against Flagellate Grazing, Is Growth Rate Controlled in Bacteria of Different Phyla,” Applied Environmental Microbiology, Vol. 65, No. 1, 1999, pp. 25-35.

[13]   K. van der Gucht, K. Sabbe, L. de Meester, et al., “Contrasting Bacterioplankton Community Composition and Seasonal Dynamics in Two Neighbouring Hypertrophic Freshwater Lakes,” Environmental Microbiology, Vol. 3, No. 11, 2001, pp. 680-690. doi:10.1046/j.1462-2920.2001.00242.x

[14]   A. C. Yannarell, A. D. Kent, G. H. Lauster, et al., “Temporal Patterns in Bacterial Communities in Three Temperate Lakes of Different Trophic Status,” Microbial Ecology, Vol. 46, No. 4, 2003, pp. 391-405. doi:10.1007/s00248-003-1008-9

[15]   A. Shade, A. D. Kent, S. E. Jones, et al., “Interannual Dynamics and Phenology of Bacterial Communities in a Eutrophic Lake,” Limnology and Oceanography, Vol. 52, No. 2, 2007, pp. 487-494. doi:10.4319/lo.2007.52.2.0487

[16]   M. Tijdens, H. L. Hoogveld, M. P. Kamst-van Agterveld, et al., “Population Dynamics and Diversity of Viruses, Bacteria and Phytoplankton in Shallow Eutrophic Lake,” Microbial Ecology, Vol. 56, No. 1, 2008, pp. 29-42. doi:10.1007/s00248-007-9321-3

[17]   E. S. Lindstrom, “Bacterioplankton Community Composition in a Boreal Forest Lake,” FEMS Microbiology Ecology, Vol. 27, No. 2, 1998, pp. 163-174. doi:10.1111/j.1574-6941.1998.tb00534.x

[18]   E. S. Lindsrtom, “Bacterioplankton Community Composition in Five Lakes Differing in Trophic Status and Humic Content,” Microbiology Ecology, Vol. 40, 2000, pp. 104-113.

[19]   D. Boucher, L. Jardillier and D. Debroas, “Succession of Bacterial Community Composition over Two Consecutive Years in Two Aquatic Systems: A Natural Lake and a Lake-Reservoir,” FEMS Microbiology Ecology, Vol. 55, No. 1, 2005, pp. 79-97. doi:10.1111/j.1574-6941.2005.00011.x

[20]   K. Simek, J. Pernthaller, M. G. Weinbauer, et al., “Changes in Bacterial Community Composition and Dynamics and Viral Mortality Rates Associated with Enhanced Flagellate Grazing in a Mesoeutrophic Reservoir,” Applied and Environmental Microbiology, Vol. 67, No. 6, 2001, pp. 2723-2733. doi:10.1128/AEM.67.6.2723-2733.2001

[21]   S. Jacquet, I. Domaizon, S. Personnic, et al., “Estimates of Protozoan and Virus-Mediated Mortality of Bacterioplankton in Lake Bourget (France),” Freshwater Biology, Vol. 50, No. 4, 2005, pp. 627-645. doi:10.1111/j.1365-2427.2005.01349.x

[22]   T. Bouvier and P. A. del Giorgio, “Key Role of Selective Viral-Induced Mortality in Determining Marine Bacterial Community Composition,” Environmental Microbiology, Vol. 9, No. 2, 2007, pp. 287-297. doi:10.1111/j.1462-2920.2006.01137.x

[23]   M. G. Weinbauer, J. Hornak, J. Nedoma, et al., “Synergistic and Antagonistic Effects of Viral Lysis and Protistan Grazing on Bacterial Biomass, Production and Diversity,” Environmental Microbiology, Vol. 9, No. 3, 2007, pp. 777-788. doi:10.1111/j.1462-2920.2006.01200.x

[24]   R. Zhang, M. G. Weinbauer and P. Y. Qian, “Viruses and Flagellates Sustain Apparent Richness and Reduce Biomass Accumulation of Bacterioplankton in Coastal Marine Waters,” Environmental Microbiology, Vol. 9, No. 12, 2007, pp. 2008-2018. doi:10.1111/j.1462-2920.2007.01410.x

[25]   O. Bonilla-Finji, G. J. Herndl, J. P. Gattuso, et al., “Viral and Flagellate Control of Prokaryotic Production and Community Structure in Offshore Mediterranean Waters,” Applied and Environmental Microbiology, Vol. 75, No. 14, 2009, pp. 4801-4812. doi:10.1128/AEM.01376-08

[26]   S. Personnic, I. Domaizon, U. Dorigo, et al., “Seasonal and Spatial Variability of Virio, Bacterio-, and Picophytoplanktonic Abundances in Three Peri-Alpine Lakes,” Hydrobiology, Vol. 627, No. 1, 2009, pp. 99-116. doi:10.1007/s10750-009-9718-8

[27]   R. Thomas, L. Berdjeb, T. Sime-Ngando and S. Jacquet, “Viral Abundance, Production, Decay Rates and Life Strategies (Lytic vs. Lysogeny) in Lake Bourget,” Environmental Microbiology, Vol. 13, 2011, pp. 616-630.

[28]   M. W. Hahn and M. G. Hofle, “Grazing of Protozoa and Its Effect on Populations of Aquatic Bacteria,” FEMS Microbiology Ecology, Vol. 35, No. 2, 2001, pp. 113-121. doi:10.1111/j.1574-6941.2001.tb00794.x

[29]   J. Comte, S. Jacquet, S. Viboud, et al., “Microbial Community Structure and Dynamics in the Largest Natural French Lake (Lake Bourget, February to July 2002),” Microbiology Ecology, Vol. 52 , No. 1, 2006, pp. 72-89. doi:10.1007/s00248-004-0230-4

[30]   M. G. Weinbauer, “Ecology of Prokaryotic Viruses,” FEMS Microbiology Reviews, Vol. 28, No. 2, 2004, pp. 127-181. doi:10.1016/j.femsre.2003.08.001

[31]   L. Berdjeb, T. Pollet, I. Domaizon, et al., “Effects of Grazers and Viruses on Bacterial Community Structure and Production in Two Contrasting Trophic Lakes,” BMC Microbiology, Vol. 11, 2011, p. 88. doi:10.1186/1471-2180-11-88

[32]   T. Sime-Ngando and A. S. Pradeep Ram, “Grazer Effects on Prokaryotes and Viruses in a Freshwater Microcosm Experiment,” Aquatic Microbial Ecology, Vol. 41, No. 2, 2005, pp. 115-124. doi:10.3354/ame041115

[33]   T. Miki and S. Jacquet, “Complex Interactions in the Aquatic Microbial World: Under-Explored Relationships between Viruses, Bacteria and Heterotrophic Flagellates,” Aquatic Microbial Ecology, Vol. 51, No. 2, 2008, pp. 195-208. doi:10.3354/ame01190

[34]   R. Tadonléké, J. Lazzarotto, O. Anneville, et al., “Phytoplankton Productivity Increased in Lake Geneva despite Phosphorus Loading Reduction,” Journal of Plankton Research, Vol. 31, No. 10, 2009, pp. 1179-1194. doi:10.1093/plankt/fbp063

[35]   S. Jacquet, O. Anneville and O. Domaizon, “Long-Term Trend of Physico-Chemical and Biological Indicators of Water-Quality and Functioning of Large Peri-Alpine Lakes (Lakes Geneva, Annecy and Bourget): A Comparative Study of Ecosystem Trajectories during Re-Oligotrophication,” Archives des Science, Vol. 65, 2012, pp. 191-208.

[36]   C. Leboulanger, U. Dorigo, S. Jacquet, et al., “Application of a Submersible Spectrofluorometer for Rapid Monitoring of Freshwater Cyanobacterial Blooms: A Case Study,” Aquatic Microbial Ecology, Vol. 30, No. 1, 2002, pp. 83-89. doi:10.3354/ame030083

[37]   R. T. Noble, M. Middelboe and J. A. Fuhrman, “Effects of Viral Enrichment on the Mortality and Growth of Heterotrophic Bacterioplankton,” Aquatic Microbial Ecology, Vol. 18, No. 1, 1999, pp. 1-13. doi:10.3354/ame018001

[38]   S. Duhamel, I. Domaizon, S. Personnic, et al., “Assessing the Microbial Community Dynamics and the Role of Bacteriophages in Bacterial Mortality in Lake Geneva,” Journal of Water Science, Vol. 19, No. 2, 2006, pp. 115-126.

[39]   D, Vaulot, “CYTOPC: Processing Software for Flow Cytometric Data,” Signal Noise, Vol. 2, 1989, p. 8.

[40]   D. A. Caron, “Technique for Enumeration of Heterotrophic and Phototrophic Nanoplankton, Using Epifluorescence Microscopy, and Comparison with Other Procedure,” Applied and Environmental Microbiology, Vol. 46, No. 2, 1983, pp. 249-268.

[41]   M. G. Weinbauer and P. Peduzzi, “Frequency, Size and Distribution of Bacteriophages in Different Marine Bacterial Morphotypes,” Marine Ecology Progress Series, Vol. 108, 1994, pp. 11-20.

[42]   M. G. Weinbauer, C. Winter and M. G. Hofle, “Reconsidering Transmission Electron Microscopy Based Estimates of Viral Infection of Bacterioplankton Using Conversion Factors Derived from Natural Communities. Aquatic Microbial Ecology, Vol. 27, No. 2, 2002, pp. 103-110. doi:10.3354/ame027103

[43]   B. J. Binder, “Reconsidering the Relationship between Virally-Induced Bacterial Mortality and Frequency of Infected Cells,” Aquatic Microbial Ecology, Vol. 18, No. 3, 1999, pp. 207-215. doi:10.3354/ame018207

[44]   C. A. Suttle, “The Significance of Viruses to Mortality in Aquatic Microbial Communities,” Microbial Ecology, Vol. 28, No. 2, 1994, pp. 237-243. doi:10.1007/BF00166813

[45]   M. G. Weinbauer and M. G. Hofle, “Significance of Viral Lysis and Flagellate Grazing as Factors Controlling Bacterioplankton Production in a Eutrophic Lake,” Applied and Environmental Microbiology, Vol. 64, No. 2, 1998, pp. 431-438.

[46]   I, Domaizon, S. Viboud and D. Fontvieille, “Taxon-Specific and Seasonal Variations in Flagellates Grazing on Heterotrophic Bacteria in the Oligotrohic Lake Annecy—Importance of Mixotrophy,” FEMS Microbiology Ecology, Vol. 46, No. 3, 2003, pp. 317-329. doi:10.1016/S0168-6496(03)00248-4

[47]   U. Dorigo, D. Fontvieille and J. F. Humbert, “Spatial Variability in the Abundance and Composition of the Free-Living Bacterioplankton Community in the Pelagic Zone of Lake Bourget (France),” FEMS Microbiology Ecology, Vol. 58, No. 1, 2006, pp. 109-119. doi:10.1111/j.1574-6941.2006.00139.x

[48]   G. Muyzer, E. C. de Waad and A. G. Uitterlinden, “Profiling of Complex Microbial Populations by Denaturing Gel Electrophoresis Analysis of Polymerase Chain Reaction-Amplified Genes Coding for 16S rRNA,” Applied and Environmental Microbiology, Vol. 59, No. 3, 1993, pp. 695-700.

[49]   M. Schauer, V. Balagué, C. Pedrós-Alió, et al., “Seasonal Changes in the Taxonomic Composition of Bacterio-plankton in Coastal Oligotrophic System,” Aquatic Microbial Ecology, Vol. 31, No. 2, 2003, pp. 163-174. doi:10.3354/ame031163

[50]   N. Fromin, J. Hamelin, S. Tarnawski, et al., “Statistical Analysis of Denaturing Gel Electrophoresis (DGE) Fingerprinting Patterns,” Environmental Microbiology, Vol. 4, No. 11, 2002, pp. 634-643. doi:10.1046/j.1462-2920.2002.00358.x

[51]   T. Huber, G. Faulkner and P. Hugenholtz, “Bellerophon: A Program to Detect Chimeric Sequences in Multiple Sequence Alignments,” Bioinformatics, Vol. 20, No. 14, 2004, pp. 2317-2319.

[52]   J. R. Cole, B. Chai, R. J. Farris, et al., “The Ribosomal Database Project (RDP-II): Sequences and Tools for High-Throughput rRNA Analysis,” Nucleic Acids Research, Vol. 33, Suppl. 1, 2005, pp. D294-D296. doi:10.1093/nar/gki038

[53]   R. Massana and K. Jürgens, “Composition and Population Dynamics of Planktonic Bacteria and Bacterivorous Flagellates in Seawater Chemostat Cultures,” Aquatic Microbial Ecology, Vol. 32, No. 1, 2003, pp. 11-22. doi:10.3354/ame032011

[54]   S. Jacquet, T. Miki, R. Noble, et al., “Viruses in Aquatic Ecosystems: Important Advancements of the Last 20 Years and Prospects for the Future in Microbial Oceanography and Limnology,” Advances in Oceanography and Limnology, Vol. 1, No. 1, 2010, pp. 71-101.

[55]   K. Hornak, M. Masin, J. Jezbera, et al., “Effects of Decreased Resource Availability, Protozoan Grazing and Viral Impact on a Structure of Bacterioplankton Assemblage in a Canyon-Shaped Reservoir,” FEMS Microbiology Ecology, Vol. 52, No. 3, 2005, pp. 315-327. doi:10.1016/j.femsec.2004.11.013

[56]   S. Jacquet, I. Domaizon, S. Personnic, et al., “Do Small Grazers Influence Viral-Induced Bacterial Mortality in Lake Bourget?” Fundamental and Applied Limnology, Vol. 170, No. 2, 2007, pp. 125-132. doi:10.1127/1863-9135/2007/0170-0125

[57]   A. S. Pradeep Ram and T. Sime-Ngando, “Functional Responses of Prokaryotes and Viruses to Grazer Effects and Nutrient Additions in Freshwater Microcosms,” The ISME Journal, Vol. 2, 2008, pp. 498-509. doi:10.1038/ismej.2008.15

[58]   F. Hammes, M. Vital and T. Egli, “Critical Evaluation of the Volumetric ‘Bottle Effect’ on Microbial Batch Growth,”. Applied and Environmental Microbiology, Vol. 76, No. 4, 2010, pp. 1278-1281. doi:10.1128/AEM.01914-09

[59]   T. F. Thingstad, “Elements of a Theory for the Mechanisms Controlling Abundance, Diversity, and Biogeochemical Role of Lytic Bacterial Viruses in Aquatic Systems,” Limnology and Oceanography, Vol. 45, No. 6, 2000, pp. 1320-1328. doi:10.4319/lo.2000.45.6.1320

[60]   T. F. Thingstad and R. Lignell, “Theoretical Models for the Control of Bacterial Growth Rate, Abundance, Diversity and Carbon Demand,” Aquatic Microbial Ecology, Vol. 13, No. 1, 1997, pp. 19-27. doi:10.3354/ame013019

[61]   N. H. Mann, A. Cook, A. Millard, et al., “Bacterial Photosynthesis Genes in a Virus,” Nature, Vol. 424, 2003, p. 741.

[62]   J. A. Fuhrman and M. S. Schwalbach, “Viral Influence on Aquatic Bacterial Communities,” Biological Bulletin, Vol. 204, No. 2, 2003, pp. 192-195. doi:10.2307/1543557

[63]   M. G. Weinbauer and F. Rassoulzadegan, “Are Viruses Driving Microbial Diversification and Diversity,” Environmental Microbiology, Vol. 6, No. 1, 2004, pp. 1-11. doi:10.1046/j.1462-2920.2003.00539.x

[64]   R. T. Noble and J. A. Fuhrman, “Virus Decay and Its Causes in Coastal Waters,” Applied and Environmental Microbiology, Vol. 63, No. 1, 1997, pp. 77-83.

[65]   S. W. Wilhelm, M. G. Weinbauer, C. A. Suttle, et al., “Measurements of DNA Damage and Photoreactivation Imply that Most Viruses in Marine Surface Waters Are Infective,” Aquatic Microbial Ecology, Vol. 14, No. 3, 1998, pp. 215-222. doi:10.3354/ame014215

[66]   W. H. Jeffrey, J. P. Kase and S. W. Wilhelm, “Ultraviolet Radiation Effects on Bacterioplankton and Viruses in Marine Ecosystems,” In: S. J. de Mora, et al., Eds., Effects of UV Radiation on Marine Ecosystems, Cambridge University Press, Cambridge, 2000, pp. 206-236. doi:10.1017/CBO9780511535444.009

[67]   C. A. Suttle and F. Chen, “Mechanisms and Rates of Decay of Marine Viruses in Seawater,” Applied and Environmental Microbiology, Vol. 58, No. 11, 1992, pp. 3721-3729.

[68]   J. M. Gonzales and C. A. Suttle, “Grazing by Marine Nanoflagellates on Viruses and Virus-Size Particles: Ingestion and Digestion,” Marine Ecology Progress Series, Vol. 94, 1993, pp. 1-10.

[69]   Y. Bettarel, T. Sime-Ngando, M. Bouvy, et al., “Low Consumption of Virus-Sized Particles by Heterotrophic Nanoflagellates in Two Lakes of the French Massif Central,” Aquatic Microbial Ecology, Vol. 39, No. 2, 2005, pp. 205-209. doi:10.3354/ame039205

[70]   S. C. Jiang and J. H. Paul, “Significance of Lysogeny in the Marine Environments: Studies with Isolates and a Model of Lysogenic Phage Production,” Microbial Ecology, Vol. 35, No. 3-4, 1998, pp. 235-243. doi:10.1007/s002489900079

[71]   M. G. Weinbauer and C. A. Suttle, “Lysogeny and Prophage Induction in Coastal and Offshore Bacterial Communities,” Aquatic Microbial Ecology, Vol. 18, No. 3, 1999, pp. 217-225. doi:10.3354/ame018217

[72]   S. J. Williamson, L. A. Houchin, L. McDaniel, et al., “Seasonal Variation in Lysogeny as Depicted by Prophage Induction in Tampa Bay, Florida,” Applied and Environmental Microbiology, Vol. 68, No. 9, 2002, pp. 4307-4314. doi:10.1128/AEM.68.9.4307-4314.2002

[73]   K. Jurgens, J. Pernthaler, S. Schalla, et al., “Morphological and Compositional Changes in a Planktonic Bacterial Community in Response to Enhanced Protozoan Grazing,” Applied and Environmental Microbiology, Vol. 65, No. 3, 1999, pp. 1241-1250.

[74]   S. Langenheder and K. Jurgens, “Regulation of Bacterial Biomass and Community Structure by Metazoan and Protozoan Predaton,” Limnology and Oceanography, Vol. 46, No. 1, 2001, pp. 121-134. doi:10.4319/lo.2001.46.1.0121

[75]   K. Simek, P. Kojecka, J. Nedoma, et al., “Shifts in Bacterial Community Composition Associated with Different Microzooplankton Size Fractions in a Eutrophic Reservoir,” Limnology and Oceanography, Vol. 20, 1999, pp. 1634-1644.

[76]   J. Gasol, M. Comerma, J. Carlos-Garcia, et al., “A Transplant Experiment to Identify the Factors Controlling Bacterial Abundance, Activity, Production and Community Composition in a Eutrophic Canyon-Shaped Reservoir,” Limnology and Oceanography, Vol. 47, No. 1, 2002, pp. 62-77. doi:10.4319/lo.2002.47.1.0062

[77]   J. Pernthaler, “Predation on Procaryotes in the Water Column and Its Ecological Implications,” Nature Reviews, Vol. 3, No. 7, 2005, pp. 537-546.

[78]   B. C. Monger and M. R. Landry, “Prey-Size Dependancy of Grazing by Free-Living Marine Flagellates,” Marine Ecology Progress Series, Vol. 74, 1991, pp. 239-248. doi:10.3354/meps074239

[79]   K. Simek and T. H. Chrzanowski, “Direct and Indirect Evidence of Size-Selective Grazing on Pelagic Bacteria by Freshwater Nanoflagellates,” Applied and Environmental Microbiology, Vol. 58, No. 11, 1992, pp. 3715-3720.

[80]   U. Christaki, J. Dolan, S. Pelegri, et al., “Consumption of Picoplankton-Size Particles by Marine Ciliates: Effects of Physiological State of the Ciliate and Particle Quality,” Limnology and Oceanography, Vol. 43, No. 3, 1998, pp. 458-464. doi:10.4319/lo.1998.43.3.0458

[81]   T. Posch, J. Jezbera, J. Vrba, et al., “Size Selective Feeding in Cyclidium glaucoma (Ciliophora, Scuticociliatida) and Its Effects on Bacterial Community Structure: A Study from a Continuous Cultivation System,” Microbial Ecology, Vol. 42, No. 3, 2001, pp. 217-227. doi:10.1007/s002480000114

[82]   C. Matz and K. Jurgens, “Interaction of Nutrient Limitation and Protozoan Grazing Determines the Phenotypic Structure of a Bacterial Community,” Microbial Ecology, Vol. 45, No. 4, 2003, pp. 384-398. doi:10.1007/s00248-003-2000-0

[83]   C. Matz, J. Boenigk, H. Arndt, et al., “Role of Bacterial Phenotypic Traits in Selective Feeding of the Heterotrophic Nanoflagellate Spunella sp,” Aquatic Microbial Ecology, Vol. 27, No. 2, 2002, pp. 137-148. doi:10.3354/ame027137

[84]   P. Lebaron, P. Servais, M. Troussellier, et al., “Changes in Bacterial Community Structure in Seawater Mesocosms Differing in Their Nutrient Status,” Aquatic Microbial Ecology, Vol. 19, No. 3, 1999, pp. 255-267. doi:10.3354/ame019255

 
 
Top