Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria-phage system

Evolution

Volumn 70, Issue 5, 2016, Pages 969-978

  Betts, Alex ^a   Gifford, Danna R ^a   Maclean, R Craig ^a   King, Kayla C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Bacteria; Bacteriophage; Community; Experimental evolution; Host parasite

Indexed keywords

BACTERIOPHAGE; BACTERIUM; BIOLOGICAL CONTROL; COMMUNITY DYNAMICS; EVOLUTION; EXPERIMENTAL STUDY; HOST-PARASITE INTERACTION; HOST-PATHOGEN INTERACTION; MICROBIAL ACTIVITY; MONOCULTURE; MUTATION; PARASITE RESISTANCE; POPULATION DYNAMICS; SPECIES DIVERSITY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

BACTERIOPHAGE; GENETIC VARIATION; GENETICS; HOST PATHOGEN INTERACTION; MOLECULAR EVOLUTION; MUTATION; PATHOGENICITY; PSEUDOMONAS AERUGINOSA; VIROLOGY;

BACTERIOPHAGES; EVOLUTION, MOLECULAR; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; MUTATION; PSEUDOMONAS AERUGINOSA;

EID: 84964407285     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12909     Document Type: Article

References (83)

1. Abedon, S. T. 2011. Lysis from without. Bacteriophage 1:46-49.
2. Balmer, O., S. C. Stearns, A. Schötzau, and R. Brun . 2009. Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90:3367-3378.
3. Barbosa, C., P. Venail, A. V. Holguin, and M. J. Vives . 2013. Co-evolutionary dynamics of the bacteria Vibrio sp. CV1 and phages V1G, V1P1, and V1P2: implications for phage therapy. Microb. Ecol. 66:897-905.
4. Beeton, M. L., D. R. Alves, M. C. Enright, and A. T. A. Jenkins . 2015. Assessing phage therapy against Pseudomonas aeruginosa using a Galleria mellonella infection model. Int. J. Antimicrob. Agents 46:196-200.
5. Behrends, V., B. Ryall, J. E. A. Zlosnik, D. P. Speert, J. G. Bundy, and H. D. Williams . 2013. Metabolic adaptations of Pseudomonas aeruginosa during cystic fibrosis chronic lung infections. Environ. Microbiol. 15:398-408.
6. Bell, G., and J. M. Smith . 1987. Short-term selection for recombination among mutually antagonistic species. Nature 328:66-68.
7. Ben-Ami, F., L. Mouton, and D. Ebert . 2008. The effects of multiple infections on the expression and evolution of virulence in a Daphnia-endoparasite system. Evolution 62:1700-1711.
8. Bernard, C. S., C. Bordi, E. Termine, A. Filloux, and S. de Bentzmann . 2009. Organization and PprB-dependent control of the Pseudomonas aeruginosa tad Locus, involved in Flp pilus biology. J. Bacteriol. 191:1961-7193.
9. Berngruber, T. W., F. J. Weissing, and S. Gandon . 2010. Inhibition of superinfection and the evolution of viral latency. J. Virol. 84:10200-10208.
10. Best, A., A. White, and M. Boots . 2009. The implications of coevolutionary dynamics to host-parasite interactions. Am. Nat. 173:779-791.
11. Betts, A., O. Kaltz, and M. E. Hochberg . 2014. Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages. Proc. Natl. Acad. Sci. USA 111:11109-11114.
12. Betts, A., M. Vasse, O. Kaltz, and M. E. Hochberg . 2013. Back to the future: evolving bacteriophages to increase their effectiveness against the pathogen Pseudomonas aeruginosa PAO1. Evol. Appl. 6:1054-1063.
13. Bohannan, B. J. M., and R. E. Lenski . 2000. The relative importance of competition and predation varies with productivity in a model community. Am. Nat. 156:329-340.
14. Boucher, J. C., H. Yu, M. H. Mudd, and V. Deretic . 1997. Mucoid Pseudomonas aeruginosa in cystic fibrosis: characterization of muc mutations in clinical isolates and analysis of clearance in a mouse model of respiratory infection. Infect. Immun. 65:3838-3846.
15. Brockhurst, M. A., T. Chapman, K. C. King, J. E. Mank, S. Paterson, and G. D. D. Hurst . 2014. Running with the Red Queen: the role of biotic conflicts in evolution Darwin review. Proc. R. Soc. B Biol. Sci 281:20141382.
16. Brockhurst, M. A., A. D. Morgan, A. Fenton, and A. Buckling . 2007. Experimental coevolution with bacteria and phage The Pseudomonas fluorescens-Phi 2 model system. Infect. Genet. Evol. 7:547-552.
17. Buckling, A., R. Craig Maclean, M. A. Brockhurst, and N. Colegrave . 2009. The Beagle in a bottle. Nature 457:824-829.
18. Buckling, A., and P. Rainey . 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. B Biol. Sci. 269:931-936.
19. Ceyssens, P.-J., K. Miroshnikov, W. Mattheus, V. Krylov, J. Robben, J.-P. Noben, S. Vanderschraeghe, N. Sykilinda, A. M. Kropinski, G. Volckaert, et al. 2009a. Comparative analysis of the widespread and conserved PB1-like viruses infecting Pseudomonas aeruginosa. Environ. Microbiol. 11:2874-2883.
20. Ceyssens, P.-J., J.-P. Noben, H.-W. Ackermann, J. Verhaegen, D. De Vos, J.-P. Pirnay, M. Merabishvili, M. Vaneechoutte, A. Chibeu, G. Volckaert, et al. 2009b. Survey of Pseudomonas aeruginosa and its phages: de novo peptide sequencing as a novel tool to assess the diversity of worldwide collected viruses. Environ. Microbiol. 11:1303-1313.
21. Chan, B. K., S. T. Abedon, and C. Loc-Carrillo . 2013. Phage cocktails and the future of phage therapy. Future Microbiol. 8:769-783.
22. Chibani-Chennoufi, S., A. Bruttin, M. L. Dillmann, and H. Brussow . 2004. Phage-host interaction: an ecological perspective. J. Bacteriol. 186:3677-3686.
23. Chibeu, A., P.-J. Ceyssens, K. Hertveldt, G. Volckaert, P. Cornelis, S. Matthijs, and R. Lavigne . 2009. The adsorption of Pseudomonas aeruginosa bacteriophage phiKMV is dependent on expression regulation of type IV pili genes. FEMS Microbiol. Lett. 296:210-218.
24. D'Herelle, F. 1922. The bacteriophage its role in immunity. Williams & Wilkins, Baltimore, USA.
25. Decaestecker, E., H. De Gersem, Y. Michalakis, and J. Raeymaekers . 2013. Damped long-term host-parasite Red Queen coevolutionary dynamics: a reflection of dilution effects? Ecol. Lett. 16:1455-1462.
26. Duncan, A. B., A. Gonzalez, and O. Kaltz . 2013. Stochastic environmental fluctuations drive epidemiology in experimental host-parasite metapopulations. Proc. R. Soc. B Biol. Sci. 280:20131747.
27. Fischer, S., S. Kittler, G. Klein, and G. Glünder . 2013. Impact of a single phage and a phage cocktail application in broilers on reduction of Campylobacter jejuni and development of resistance. PLoS One 8:1-13.
28. Fischetti, V. A, D. Nelson, and R. Schuch . 2006. Reinventing phage therapy: are the parts greater than the sum? Nat. Biotechnol. 24:1508-1511.
29. Forde, S. E., J. N. Thompson, R. D. Holt, and B. J. M. Bohannan . 2008. Coevolution drives temporal changes in fitness and diversity across environments in a bacteria-bacteriophage interaction. Evolution 62:1830-1839.
30. Friman, V.-P., and A. Buckling . 2013. Effects of predation on real-time host-parasite coevolutionary dynamics. Ecol. Lett. 16:39-46.
31. Griffiths, E. C., A. B. Pedersen, A. Fenton, and O. L. Petchey . 2011. The nature and consequences of coinfection in humans. J. Infect. 63:200-206.
32. Gu, J., X. Liu, Y. Li, W. Han, L. Lei, Y. Yang, H. Zhao, Y. Gao, J. Song, R. Lu, C. Sun, and X. Feng . 2012. A method for generation phage cocktail with great therapeutic potential. PLoS One 7:e31698.
33. Haldane, J. B. S. 1949. Disease and evolution. Ric Sci Suppl. A 19:68-76.
34. Harcombe, W., and J. Bull . 2005. Impact of phages on two-species bacterial communities. Appl. Environ. Microbiol. 71:5254-5259.
35. Holloway, B. W. 1955. Genetic recombination in Pseudomonas aeruginosa. J. Gen. Microbiol. 13:572-581.
36. Høyland-Kroghsbo, N., R. Mærkedahl, and S. Svenningsen . 2013. A quorum-sensing-induced bacteriophage defense mechanism. MBio 4(1):e00362-e00312.
37. Hughes, W. O. H., K. S. Petersen, L. V Ugelvig, D. Pedersen, L. Thomsen, M. Poulsen, and J. J. Boomsma . 2004. Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. BMC Evol. Biol. 4:45.
38. Hyman P., and S. T. Abedon . 2010. Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol. 70:217-248
39. Jones, R. 2010. Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clin. Infect. Dis. 51(Suppl 1):S81-S87.
40. Kiino, D. R., and L. B. Rothman-denes . 1989. Genetic analysis of bacteriophage N4 adsorption. J. Bacteriol. 171:4595-4602.
41. King, E., M. Ward, and D. Raney . 1954. 2 simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
42. King, K. C., L. F. Delph, J. Jokela, and C. M. Lively . 2009. The geographic mosaic of sex and the Red Queen. Curr. Biol. 19:1438-1441.
43. Koskella, B., D. M. Lin, A. Buckling, and J. N. Thompson . 2012. The costs of evolving resistance in heterogeneous parasite environments. Proc. R. Soc. B Biol. Sci. 279:1896-903.
44. Kouyos, R. D., M. Salathé, S. P. Otto, and S. Bonhoeffer . 2009. The role of epistasis on the evolution of recombination in host-parasite coevolution. Theor. Popul. Biol. 75:1-13.
45. Kropinski, A. M., L. Chan, K. Jarrell, and F. H. Milazzo . 1977. The nature of Pseudomonas aeruginosa strain PAO bacteriophage receptors. Can. J. Microbiol. 23:653-658.
46. Kwan, C., and J. D. Ernst . 2011. HIV and tuberculosis: a deadly human syndemic. Clin. Microbiol. Rev. 24:351-376.
47. Lammens, E., P.-J. Ceyssens, M. Voet, K. Hertveldt, R. Lavigne, and G. Volckaert . 2009. Representational difference analysis (RDA) of bacteriophage genomes. J. Microbiol. Methods 77:207-213.
48. Lavigne, R., E. Lecoutere, J. Wagemans, W. Cenens, A. Aertsen, L. Schoofs, B. Landuyt, J. Paeshuyse, M. Scheer, M. Schobert, et al. 2013. A multifaceted study of Pseudomonas aeruginosa shutdown by virulent podovirus LUZ19. MBio 4:1-8.
49. Lenski, R. E. 1988. Dynamics of interactions between bacteria and virulent bacteriophage. Adv. Microb. Ecol. 10:1-44.
50. Levin, B. R., and J. J. Bull . 2004. Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2:166-173.
51. Liu, J., R. Yan, Q. Zhong, S. Ngo, N. J. Bangayan, L. Nguyen, T. Lui, M. Liu, M. C. Erfe, N. Craft, et al. 2015. The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin. ISME J. 9:2078-2093.
52. Lu, T. K., and M. S. Koeris . 2011. The next generation of bacteriophage therapy. Curr. Opin. Microbiol. 14:524-531.
53. McPartland, J. A. 2008. The tail sheath of bacteriophage N4 is required for adsorption to the host. 1st ed. Proquest, Michigan, USA.
54. Merabishvili, M., J.-P. Pirnay, G. Verbeken, N. Chanishvili, M. Tediashvili, N. Lashkhi, T. Glonti, V. Krylov, J. Mast, L. Van Parys, et al. 2009. Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PLoS One 4:e4944.
55. Minot, S., and A. Bryson . 2013. Rapid evolution of the human gut virome. Proc. Natl. Acad. Sci. USA 110:12450-12455.
56. Mitchell-Olds, T., and J. Bergelson . 2000. Biotic interactions: genomics and coevolution. Curr. Opin. Plant Biol. 3:273-277.
57. Mizoguchi, K., M. Morita, C. R. Fischer, M. Yoichi, Y. Tanji, and H. Unno . 2003. Coevolution of bacteriophage PP01 and Escherichia coli O157: H7 in continuous culture. Appl. Environ. Microbiol. 69:170-176.
58. Mostowy, R., M. Salathe, R. D. Kouyos, and S. Bonhoeffer . 2010. On the evolution of sexual reproduction in hosts coevolving with mutliple parasites. Evolution 64:1644-1656.
59. Naidu, M., R. Robles-Sikisaka, S. R. Abeles, T. K. Boehm, and D. T. Pride . 2014. Characterization of bacteriophage communities and CRISPR profiles from dental plaque. BMC Microbiol. 14:175.
60. Nilsson, A. S. 2014. Phage therapy-constraints and possibilities. Ups. J. Med. Sci. 119:192-198.
61. Örmälä-Odegrip, A.-M., V. Ojala, T. Hiltunen, J. Zhang, J. K. Bamford, and J. Laakso . 2015. Protist predation can select for bacteria with lowered susceptibility to infection by lytic phages. BMC Evol. Biol. 15:1-7.
62. Paul, J. H., M. B. Sullivan, A. M. Segall, and F. Rohwer . 2002. Marine phage genomics. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 133:463-476.
63. Pedruzzi, I., J. P. Rosenbusch, and K. P. Locher . 1998. Inactivation in vitro of the Escherichia coli outer membrane protein FhuA by a phage T5-encoded lipoprotein. FEMS Microbiol. Lett. 168:119-125.
64. Poullain, V., S. Gandon, M. A. Brockhurst, A. Buckling, and M. E. Hochberg . 2008. The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution 62:1-11.
65. R Core Team (2013). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/
66. Refardt, D. 2011. Within-host competition determines reproductive success of temperate bacteriophages. ISME J. 5:1451-1460.
67. Samson, J. E., A. H. Magadán, M. Sabri, and S. Moineau . 2013. Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11:675-687.
68. SAS Institute Inc. 2012. New Features in JMP 10. Cary, NC.
69. Scanlan, P. D., A. R. Hall, P. Burlinson, G. Preston, and A. Buckling . 2013. No effect of host-parasite co-evolution on host range expansion. J. Evol. Biol. 26:205-209.
70. Schmerer, M., I. J. Molineux, and J. J. Bull . 2014. Synergy as a rationale for phage therapy using phage cocktails. PeerJ 2:e590.
71. Schrag, S. J., and J. E. Mittler . 1996. Host-parasite coexistence: the role of spatial refuges in stabilizing bacteria-phage interactions. Am. Nat. 148:348-377.
72. Schulte, R. D., C. Makus, B. Hasert, N. K. Michiels, and H. Schulenburg . 2010. Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc. Natl. Acad. Sci. USA 107:7359-7364.
73. Skurnik, M., and E. Strauch . 2006. Phage therapy: facts and fiction. Int. J. Med. Microbiol. 296:5-14.
74. Sulakvelidze, A., Z. Alavidze, and J. Morris . 2001. Bacteriophage therapy. Antimicrob. Agents Chemother. 45, 649-659.
75. Tazzyman, S. J., and A. R. Hall . 2014. Lytic phages obscure the cost of antibiotic resistance in Escherichia coli. ISME J. 9:809-820.
76. Telfer, S., X. Lambin, R. Birtles, P. Beldomenico, S. Burthe, S. Paterson, and M. Begon . 2010. Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243-246.
77. Thrall, P. H., M. E. Hochberg, J. J. Burdon, and J. D. Bever . 2007. Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol. Evol. 22:120-126.
78. Thrall, P. H., A.-L. Laine, M. Ravensdale, A. Nemri, P. N. Dodds, L. G. Barrett, and J. J. Burdon . 2012. Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol. Lett. 15:425-435.
79. Turki, Y., H. Ouzari, I. Mehri, A. Ben Ammar, and A. Hassen . 2012. Evaluation of a cocktail of three bacteriophages for the biocontrol of Salmonella of wastewater. Food Res. Int. 45:1099-1105.
80. Ulrich, Y., and P. Schmid-Hempel . 2012. Host modulation of parasite competition in multiple infections. Proc. R. Soc. B Biol. Sci. 279:2982-2989.
81. Vogwill, T., A. Fenton, and M. A. Brockhurst . 2011. Coevolving parasites enhance the diversity-decreasing effect of dispersal. Biol. Lett. 7:578-580.
82. Wichman, H. A., J. Millstein, and J. J. Bull . 2005. Adaptive molecular evolution for 13, 000 phage generations: a possible arms race. Genetics 170:19-31.
83. Williamson, K. E., M. Radosevich, and K. E. Wommack . 2005. Abundance and diversity of viruses in six Delaware soils. Appl. Environ. Microbiol. 71:3119-3125.