Coaggregation in a microbial predator-prey system affects competition and trophic transfer efficiency

Ecology

Volumn 94, Issue 4, 2013, Pages 870-881

  Corno, Gianluca ^a,b   Villiger, Jörg ^a   Pernthaler, Jakob ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b CNR Institute of Ecosystem Study   (Italy)

Author keywords

Arthrobacter agilis; Brevundimonas; community ecology; cooperation; microbial coaggregation; Poterioochromonas; prey predator interactions; system efficiency.

Indexed keywords

ANIMAL; BACTERIUM; COEXISTENCE; COMMUNITY ECOLOGY; DISSOLVED ORGANIC MATTER; INTRASPECIFIC COMPETITION; MICROBIAL ECOLOGY; PLANT; PREDATOR; PREDATOR-PREY INTERACTION; PRODUCTIVITY; TROPHIC LEVEL;

ANIMALIA; ARTHROBACTER; ARTHROBACTER AGILIS; BACTERIA (MICROORGANISMS); BREVUNDIMONAS; POTERIOOCHROMONAS; PROTISTA;

EID: 84876760716     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/12-1652.1     Document Type: Article

References (66)

1. Alldredge, A., and M. Silver. 1988. Characteristics, dynamics and significance of marine snow. Progress in Oceanography 20:41-82.
2. Arndt, H., K. Schmidt-Denter, B. Auer, and M. Weitere. 2003. Protozoans and biofilms. Pages 173-189 in W. E. Krumbein, D. M. Paterson, and G. A. Zavarzin, editors. Fossil and recent biofilms, mats and networks. Kluwer Academic Publishers, Dordrecht, The Netherlands.
3. Azam, F., and F. Malfatti. 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology 5:782-791.
4. Blom, J. F., K. Hornak, K. Simek, and J. Pernthaler. 2010a. Aggregate formation in a freshwater bacterial strain induced by growth state and conspecific chemical cues. Environmental Microbiology 12:2486-2495.
5. Blom, J. F., and J. Pernthaler. 2010. Antibiotic effects of three strains of chrysophytes (Ochromonas, Poterioochromonas) on freshwater bacterial isolates. FEMS Microbiology Ecology 71:281-290.
6. Blom, J. F., Y. S. Zimmermann, T. Ammann, and J. Pernthaler. 2010b. Scent of danger: floc formation by a freshwater bacterium is induced by supernatants from a predator-prey coculture. Applied and Environmental Microbiology 76:6156-6163.
7. Boenigk, J., C. Matz, K. Jurgens, and H. Arndt. 2002. Food concentration-dependent regulation of food selectivity of interception-feeding bacterivorous nanoflagellates. Aquatic Microbial Ecology 27:195-202.
8. Bohannan, B. J. M., and R. E. Lenski. 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecology Letters 3:362-377.
9. Buswell, C. M., Y. M. Herlihy, P. D. Marsh, C. W. Keevil, and S. A. Leach. 1997. Coaggregation amongst aquatic biofilm bacteria. Journal of Applied Microbiology 83:477-484.
10. Chase, Z., and N. Price. 1997. Metabolic consequences of iron deficiency in heterotrophic marine protozoa. Limnology and Oceanography 42:1673-1684.
11. Christensen-Dalsgaard, K. K., and T. Fenchel. 2003. Increased filtration efficiency of attached compared to free-swimming flagellates. Aquatic Microbial Ecology 33:77-86.
12. Corno, G., E. Caravati, C. Callieri, and R. Bertoni. 2008. Effects of predation pressure on bacterial abundance, diversity, and size-structure distribution in an oligotrophic system. Journal of Limnology 67:107-119.
13. Corno, G., and K. Jurgens. 2006. Direct and indirect effects of protist predation on population size structure of a bacterial strain with high phenotypic plasticity. Applied and Environmental Microbiology 72:78-86.
14. Corno, G., and K. Jurgens. 2008. Structural and functional patterns of bacterial communities in response to protist predation along an experimental productivity gradient. Environmental Microbiology 10:2857-2871.
15. Coustau, C., C. Chevillon, and R. French-Constant. 2000. Resistance to xenobiotics and parasites: can we count the costTrends in Ecology and Evolution 15:378-383.
16. Drake, J. A., G. R. Huxel, and C. L. Hewitt. 1996. Microcosms as models for generating and testing community theory. Ecology 77:670-677.
17. Fenchel, T. 1982. Biology of heterotrophic microflagellates. 2: Bioenergetics and growth. Marine Ecology Progress Series 8:225-231.
18. Fenchel, T. 1986. Protozoan filter feeding. Progress in Protistology 1:65-113.
19. Glockner, F. O., H.-D. Babenzien, and R. Amann. 1998. Phylogeny and identification in situ of Nevskia ramosa. Applied and Environmental Microbiology 64:1895-1901.
20. Goldman, J. C., and D. A. Caron. 1985. Experimental studies on an omnivorous microflagellate -implications for grazing and nutrient regeneration in the marine microbial foodchain. Deep-Sea Research Part I, Oceanographic Research Papers 32:899-915.
21. Gram, L., H. P. Grossart, A. Schlingloff, and T. Kiorboe. 2002. Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Applied and Environmental Microbiology 68:4111-4116.
22. Grossart, H. P., C. Dziallas, F. Leunert, and K. W. Tang. 2010. Bacteria dispersal by hitchhiking on zooplankton. Proceedings of the National Academy of Sciences USA 107:11959-11964.
23. Grossart, H. P., and M. Simon. 1993. Limnetic macroscopic organic aggregates (lake snow) -occurrence, characteristics, and microbial dynamics in Lake Constance. Limnology and Oceanography 38:532-546.
24. Hagstrom, A., F. Azam, A. Andersson, J. Wikner, and F. Rassoulzadegan. 1988. Microbial loop in an oligotrophic pelagic marine ecosystem: possible roles of cyanobacteria and nanoflagellates in the organic fluxes. Marine Ecology Progress Series 49:171-178.
25. Hahn, M. W., H. Lunsdorf, and L. Janke. 2004. Exopolymer production and microcolony formation by planktonic freshwater bacteria: defence against protistan grazing. Aquatic Microbial Ecology 35:297-308.
26. Hamilton, W. D. 1971. Geometry for the selfish herd. Journal of Theoretical Biology 31:295-311.
27. Hervás, A., L. Camarero, I. Reche, and E. O. Casamayor. 2009. Viability and potential for immigration of airborne bacteria from Africa that reach high mountain lakes in Europe. Environmental Microbiology 11:1612-1623.
28. Hoppe, H. G., K. Gocke, R. Koppe, and C. Begler. 2002. Bacterial growth and primary production along a northsouth transect of the Atlantic Ocean. Nature 416:168-171.
29. Hutchinson, G. E. 1961. The paradox of the plankton. American Naturalist 95:137-145.
30. Iriberri, J., I. Azua, A. Labirua-Iturburu, I. Artolozaga, and I. Barcina. 1994. Differential elimination of enteric bacteria by protists in a freshwater system. Journal of Applied Bacteriology 77:476-483.
31. Jaspers, E., and J. Overmann. 2004. Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Applied and Environmental Microbiology 70:4831-4839.
32. Jessup, C. M., S. E. Forde, and B. J. M. Bohannan. 2005. Microbial experimental systems in ecology. Advances in Ecological Research 37:273-307.
33. Jurgens, K., and H. Gude. 1994. The potential importance of grazing-resistant bacteria in planktonic systems. Marine Ecology Progress Series 112:169-188.
34. Jurgens, K., and C. Matz. 2002. Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 81:413-434.
35. Kepner, R. L., and J. R. Pratt. 1994. Use of fluorochromes for direct enumeration of total bacteria in environmental samples -past and present. Microbiological Reviews 58:603-615.
36. Kiboe, T., H. P. Grossart, H. Ploug, and K. Tang. 2002. Mechanisms and rates of bacterial colonization of sinking aggregates. Applied and Environmental Microbiology 68:3996-4006.
37. Kiboe, T., H. P. Grossart, H. Ploug, K. Tang, and B. Auer. 2004. Particle-associated flagellates: swimming patterns, colonization rates, and grazing on attached bacteria. Aquatic Microbial Ecology 35:141-152.
38. Koch, A. L. 1996. What size should a bacterium beA question of scale. Annual Review of Microbiology 50:317-348.
39. Kolenbrander, P. E. 1989. Surface recognition among oral bacteria: multigeneric coaggregations and their mediators. Critical Reviews in Microbiology 17:137-158.
40. Lawton, J. H. 1995. Ecological experiments with model systems. Science 269:328-331.
41. Loferer-Krossbacher, M., J. Klima, and R. Psenner. 1998. Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Applied and Environmental Microbiology 64:688-694.
42. Malik, A., M. Sakamoto, S. Hanazaki, M. Osawa, T. Suzuki, M. Tochigi, and K. Kakii. 2003. Coaggregation among nonflocculating bacteria isolated from activated sludge. Applied and Environmental Microbiology 69:6056-6063.
43. Matz, C., P. Deines, J. Boenigk, H. Arndt, L. Eberl, S. Kjelleberg, and K. Jurgens. 2004. Impact of violaceinproducing bacteria on survival and feeding of bacterivorous nanoflagellates. Applied and Environmental Microbiology 70:1593-1599.
44. Matz, C., and K. Jurgens. 2005. High motility reduces grazing mortality of planktonic bacteria. Applied and Environmental Microbiology 71:921-929.
45. Menden-Deuer, S., E. J. Lessard, and J. Satterberg. 2001. Effect of preservation on dinoflagellate and diatom cell volume and consequences for carbon biomass predictions. Marine Ecology Progress Series 222:41-50.
46. Miyazaki, T., K. Tainaka, T. Togashi, T. Suzuki, and J. Yoshimura. 2006. Spatial coexistence of phytoplankton species in ecological timescale. Population Ecology 48:107-112.
47. Nagata, T., and D. L. Kirchman. 1992. Release of macromolecular organic complexes by heterotrophic marine flagellates. Marine Ecology Progress Series 83:233-240.
48. Newton, R. J., S. E. Jones, A. Eiler, K. D. McMahon, and S. Bertilsson. 2011. A guide to the natural history of freshwater lake bacteria. Microbiology and Molecular Biology Reviews 75:14-49.
49. Pelegri, S. P., U. Christaki, J. Dolan, and F. Rassoulzadegan. 1999. Particulate and dissolved organic carbon production by the heterotrophic nanoflagellate Pteridomonas danica. Microbial Ecology 37:276-284.
50. Pernthaler, A., J. Pernthaler, H. Eilers, and R. Amann. 2001. Growth patterns of two marine isolates: adaptations to substrate patchinessApplied and Environmental Microbiology 67:4077-4083.
51. Pernthaler, J. 2005. Predation on prokaryotes in the water column and its ecological implications. Nature Reviews Microbiology 3:537-546.
52. Rayor, L. S., and G. W. Uetz. 1993. Ontogenic shifts within the selfish herd -predation risk and foraging trade-offs change with age in colonial web-building spiders. Oecologia 95:1-8.
53. Rickard, A. H., S. A. Leach, L. S. Hall, C. M. Buswell, N. J. High, and P. S. Handley. 2002. Phylogenetic relationships and coaggregation ability of freshwater biofilm bacteria. Applied and Environmental Microbiology 68:3644-3650.
54. Roller, C., M. Wagner, R. Amann, W. Ludwig, and K.-H. Schleifer. 1994. In situ probing of Gram-positive bacteria with high DNA GC content using 23S rRNA-targeted oligonucleotides. Microbiology 140:2849-2858.
55. Rothhaupt, K. O. 1997. Nutrient turnover by freshwater bacterivorous flagellates: differences between a heterotrophic and a mixotrophic chrysophyte. Aquatic Microbial Ecology 12:65-70.
56. Sekar, R., A. Pernthaler, J. Pernthaler, F. Warnecke, T. Posch, and R. Amann. 2003. An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Applied and Environmental Microbiology 69:2928-2935.
57. Sherr, E. B., B. F. Sherr, and L. J. Albright. 1987. Bacteria -link or sinkScience 235:88-88.
58. Shikano, S., L. S. Luckinbill, and Y. Kurihara. 1990. Changes of traits in a bacterial population associated with protozoal predation. Microbial Ecology 20:75-84.
59. Simek, K., J. Vrba, J. Pernthaler, T. Posch, P. Hartman, J. Nedoma, and R. Psenner. 1997. Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Applied and Environmental Microbiology 63:587-595.
60. Simon, M., H. P. Grossart, B. Schweitzer, and H. Ploug. 2002. Microbial ecology of organic aggregates in aquatic ecosystems. Aquatic Microbial Ecology 28:175-211.
61. van Gremberghe, I., P. Vanormelingen, B. Vanelslander, K. Van der Gucht, S. D'Hondt, L. De Meester, and W. Vyverman. 2009. Genotype-dependent interactions among sympatric Microcystis strains mediated by Daphnia grazing. Oikos 118:1647-1658.
62. Wey, J. K., A. Scherwass, H. Norf, H. Arndt, and M. Weitere. 2008. Effects of protozoan grazing within river biofilms under semi-natural conditions. Aquatic Microbial Ecology 52:283-296.
63. Wiggert, J. D., A. G. E. Haskell, G. A. Paffenhofer, E. E. Hofmann, and J. M. Klinck. 2005. The role of feeding behavior in sustaining copepod populations in the tropical ocean. Journal of Plankton Research 27:1013-1031.
64. Wilson, D. S. 1974. Prey capture and competition in the ant lion. Biotropica 6:187-193.
65. Wimpenny, J., and R. Colasanti. 2004. A simple automaton model for coaggregation. Biofilms 1:369-375.
66. Zotina, T., O. Koster, and F. Juttner. 2003. Photoheterotrophy and light-dependent uptake of organic and organic nitrogenous compounds by Planktothrix rubescens under low irradiance. Freshwater Biology 48:1859-1872.