Top-down effects of a lytic bacteriophage and protozoa on bacteria in aqueous and biofilm phases

Ecology and Evolution

Volumn 4, Issue 23, 2014, Pages 4444-4453

  Zhang, Ji ^a,b   Örmälä Odegrip, Anni Maria ^a,b   Mappes, Johanna ^a   Laakso, Jouni ^a,b  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Tetrahymena thermophila; Acanthamoeba castellanii; Aquatic bacteria; Defense evolution; Lytic bacteriophage; Microcosm; Semad11; Serratia marcescens db11; Top down regulation

Indexed keywords

ACANTHAMOEBA CASTELLANII; BACTERIA (MICROORGANISMS); CILIOPHORA; PROTOZOA; SERRATIA MARCESCENS; TETRAHYMENA THERMOPHILA;

EID: 84919464022     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1302     Document Type: Article

References (62)

1. Abedon, S. T. 2008. Bacteriophage ecology: Population growth, evolution, and impact of bacterial viruses. Cambridge University Press, New York.
2. Ali, T., and D. Saleh. 2013. A simplified experimental model for clearance of some pathogenic bacteria using common bacterivorous ciliated spp. in Tigris river. Appl. Environ. Microbiol. 4:63-71.
3. Bettarel, Y., T. Sime-Ngando, C. Amblard, and J. Dolan. 2004. Viral activity in two contrasting lake ecosystems. Appl. Environ. Microbiol. 70:2941-2951.
4. Bohannan, B. J. M., and R. E. Lenski. 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol. Lett. 3:362-377.
5. Bowers, B. 1977. Comparison of pinocytosis and phagocytosis in Acanthamoeba castellanii. Exp. Cell Res. 110:409-417.
6. Brussaard, C. P., D. Marie, and G. Bratbak. 2000. Flow cytometric detection of viruses. J. Virol. Methods 85:175-182.
7. Buckling, A., and P. B. Rainey. 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. Biol. Sci. 269:931-936.
8. Bull, J. J., C. S. Vegge, M. Schmerer, W. N. Chaudhry, and B. R. Levin. 2014. Phenotypic resistance and the dynamics of bacterial escape from phage control. PLoS ONE 9:e94690.
9. Chan, B. K., S. T. Abedon, and C. Loc-Carrillo. 2013. Phage cocktails and the future of phage therapy. Future Microbiol. 8:769-783.
10. Christaki, U., J. R. Dolan, S. Pelegri, and F. Rassoulzadegan. 1998. Consumption of picoplankton-size particles by marine ciliates: effects of physiological state of the ciliate and particle quality. Limnol. Oceanogr. 43:458-464.
11. Dawkins, R., and J. R. Krebs. 1979. Arms races between and within species. Proc. Biol. Sci. 205:489-511.
12. Declercq, A. M., F. Haesebrouck, W. Van den Broeck, P. Bossier, and A. Decostere. 2013. Columnaris disease in fish: a review with emphasis on bacterium-host interactions. Vet. Res. 44:27.
13. Dopheide, A., G. Lear, R. Stott, and G. Lewis. 2011. Preferential feeding by the ciliates Chilodonella and Tetrahymena spp. and effects of these protozoa on bacterial biofilm structure and composition. Appl. Environ. Microbiol. 77:4564-4572.
14. Eisenmann, H., H. Harms, R. Meckenstock, E. I. Meyer, and A. J. Zehnder. 1998. Grazing of Tetrahymena sp. on adhered bacteria in percolated columns monitored by in situ hybridization with fluorescent oligonucleotide probes. Appl. Environ. Microbiol. 64:1264-1269.
15. Elena, S. F., and R. E. Lenski. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4:457-469.
16. Fenchel, T. 1980. Suspension feeding in ciliated protozoa: functional response and particle size selection. Microb. Ecol. 6:1-11.
17. Flyg, C., K. Kenne, and H. G. Boman. 1980. Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J. Gen. Microbiol. 120:173-181.
18. Friman, V. P., and A. Buckling. 2013. Effects of predation on real-time host-parasite coevolutionary dynamics. Ecol. Lett. 16:39-46.
19. Friman, V. P., and J. Laakso. 2011. Pulsed-resource dynamics constrain the evolution of predator-prey interactions. Am. Nat. 177:334-345.
20. Friman, V. P., T. Hiltunen, J. Laakso, and V. Kaitala. 2008. Availability of prey resources drives evolution of predator-prey interaction. Proc. Biol. Sci. 275:1625-1633.
21. Friman, V. P., J. Laakso, M. Koivu-Orava, and T. Hiltunen. 2011. Pulsed-resource dynamics increase the asymmetry of antagonistic coevolution between a predatory protist and a prey bacterium. J. Evol. Biol. 24:2563-2573.
22. Fuhrman, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548.
23. Gomez, P., and A. Buckling. 2011. Bacteria-phage antagonistic coevolution in soil. Science 332:106-109.
24. Gonzalez, J. M., E. B. Sherr, and B. F. Sherr. 1990. Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. Environ. Microbiol. 56:583-589.
25. Goodridge, L. D., and B. Bisha. 2011. Phage-based biocontrol strategies to reduce foodborne pathogens in foods. Bacteriophage 1:130-137.
26. Greub, G., and D. Raoult. 2004. Microorganisms resistant to free-living amoebae. Clin. Microbiol. Rev. 17:413-433.
27. Grimont, P. A., and F. Grimont. 1978. The genus Serratia. Ann. Rev. Microbiol. 32:221-248.
28. Gu, J., X. Liu, Y. Li, W. Han, L. Lei, Y. Yang, et al. 2012. A method for generation phage cocktail with great therapeutic potential. PLoS ONE 7:e31698.
29. Hanlon, G. W., S. P. Denyer, C. J. Olliff, and L. J. Ibrahim. 2001. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 67:2746-2753.
30. Jürgens, K., and C. Matz. 2002. Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Leeuwenhoek 81:413-434.
31. Kennedy, G. M., J. H. Morisaki, and P. A. Champion. 2012. Conserved mechanisms of Mycobacterium marinum pathogenesis within the environmental amoeba Acanthamoeba castellanii. Appl. Environ. Microbiol. 78:2049-2052.
32. Kiy, T., and A. Tiedtke. 1992. Mass cultivation of Tetrahymena-Thermophila yielding high cell densities and short generation times. Appl. Microbiol. Biotechnol. 37:576-579.
33. Koskella, B., D. M. Lin, A. Buckling, and J. N. Thompson. 2012. The costs of evolving resistance in heterogeneous parasite environments. Proc. Biological Sci. 279:1896-1903.
34. La Scola, B., L. Mezi, P. J. Weiller, and D. Raoult. 2001. Isolation of Legionella anisa using an amoebic coculture procedure. J. Clin. Microbiol. 39:365-366.
35. Laakso, J., K. Löytynoja, and V. Kaitala. 2003. Environmental noise and population dynamics of the ciliated protozoa Tetrahymena thermophila in aquatic microcosms. Oikos 102:663-671.
36. Labrie, S. J., J. E. Samson, and S. Moineau. 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317-327.
37. Lennon, J. T., S. A. M. Khatana, M. F. Marston, and J. B. H. Martiny. 2007. Is there a cost of virus resistance in marine cyanobacteria? ISME J. 1:300-312.
38. Levin, B. R., and J. J. Bull. 2004. Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2:166-173.
39. Lopez-Pascua, L. D. C., and A. Buckling. 2008. Increasing productivity accelerates host-parasite coevolution. J. Evol. Biol. 21:853-860.
40. Mahlen, S. D. 2011. Serratia infections: from military experiments to current practice. Clin. Microbiol. Rev. 24:755-791.
41. Mathias, C. B., A. Kirschner, and B. Velimirov. 1995. Seasonal variations of virus abundance and viral control of the bacterial production in a backwater system of the Danube river. Appl. Environ. Microbiol. 61:3734-3740.
42. Mcmanus, G. B., and J. A. Fuhrman. 1986. Bacterivory in seawater studied with the use of inert fluorescent particles. Limnol. Oceanogr. 31:420-426.
43. Meyer, J. R., and R. Kassen. 2007. The effects of competition and predation on diversification in a model adaptive radiation. Nature 446:432-435.
44. Molmeret, M., M. Horn, M. Wagner, M. Santic, and Y. Abu Kwaik. 2005. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 71:20-28.
45. Morgan, A. D., R. C. Maclean, and A. Buckling. 2009. Effects of antagonistic coevolution on parasite-mediated host coexistence. J. Evol. Biol. 22:287-292.
46. Nygaard, K., and D. O. Hessen. 1990. Use of C-14 protein-labeled bacteria for estimating clearance rates by heterotrophic and mixotrophic flagellates. Mar. Ecol. Prog. Ser. 68:7-14.
47. O'toole, G. A., and R. Kolter. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
48. Pace, M. L., and J. J. Cole. 1994. Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb. Ecol. 28:181-193.
49. Page, F. C. 1976. An illustrated key to freshwater and soil amoebae: With notes on cultivation and ecology. Freshwater Biological Association, Cumbria.
50. Page, F. C. 1988. A new key to freshwater and soil Gymnamoebae with instructions for culture. Freshwater Biological Association, Cumbria.
51. Palsson, E., K. J. Lee, R. E. Goldstein, J. Franke, R. H. Kessin, and E. C. Cox. 1997. Selection for spiral waves in the social amoebae Dictyostelium. Proc. Natl Acad. Sci. USA 94:13719-13723.
52. Parry, J. D., A. K. Holmes, M. E. Unwin, and J. Laybourn-Parry. 2007. The use of ultrasonic imaging to evaluate the effect of protozoan grazing and movement on the topography of bacterial biofilms. Lett. Appl. Microbiol. 45:364-370.
53. Rodriguez-Zaragoza, S. 1994. Ecology of free-living amoebae. Crit. Rev. Microbiol. 20:225-241.
54. Sherr, B. F., E. B. Sherr, T. L. Andrew, R. D. Fallon, and S. Y. Newell. 1986. Trophic interactions between heterotrophic protozoa and bacterioplankton in estuarine water analyzed with selective metabolic-inhibitors. Mar. Ecol. Prog. Ser. 32:169-179.
55. Stern, A., and R. Sorek. 2011. The phage-host arms race: shaping the evolution of microbes. BioEssays 33:43-51.
56. Sutherland, I. W., K. A. Hughes, L. C. Skillman, and K. Tait. 2004. The interaction of phage and biofilms. FEMS Microbiol. Lett. 232:1-6.
57. Sutherland, K. P., J. W. Porter, J. W. Turner, B. J. Thomas, E. E. Looney, T. P. Luna, et al. 2010. Human sewage identified as likely source of white pox disease of the threatened Caribbean elkhorn coral, Acropora palmata. Environ. Microbiol. 12:1122-1131.
58. Suttle, C. A. 2005. Viruses in the sea. Nature 437:356-361.
59. Van Valen, L. 1973. A new evolutionary law. Evolution. Theor. 1:1-33.
60. Vogel, G., L. Thilo, H. Schwarz, and R. Steinhart. 1980. Mechanism of phagocytosis in Dictyostelium discoideum: phagocytosis is mediated by different recognition sites as disclosed by mutants with altered phagocytotic properties. J. Cell Biol. 86:456-465.
61. Weitere, M., T. Bergfeld, S. A. Rice, C. Matz, and S. Kjelleberg. 2005. Grazing resistance of Pseudomonas aeruginosa biofilms depends on type of protective mechanism, developmental stage and protozoan feeding mode. Environ. Microbiol. 7:1593-1601.
62. Wommack, K. E., R. T. Hill, T. A. Muller, and R. R. Colwell. 1996. Effects of sunlight on bacteriophage viability and structure. Appl. Environ. Microbiol. 62:1336-1341.