Long-term genomic coevolution of host-parasite interaction in the natural environment

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Laanto, Elina ^a   Hoikkala, Ville ^a   Ravantti, Janne ^b   Sundberg, Lotta Riina ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTAGONISM; ARMS RACE; BACTERIUM; GENETIC ANALYSIS; GENOMICS; HOST-PARASITOID INTERACTION; INFECTIVITY; MOLECULAR ANALYSIS;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; COEVOLUTION; COLUMNARIS DISEASE; FLAVOBACTERIUM; FLAVOBACTERIUM COLUMNARE; GENE LOCUS; GENOME SIZE; GENOMICS; HOST PARASITE INTERACTION; HOST RANGE; HOST RESISTANCE; NONHUMAN; ORGANISM COMMUNITY; SEQUENCE ALIGNMENT; BACTERIOPHAGE; ENVIRONMENTAL MICROBIOLOGY; GENETICS; MOLECULAR EVOLUTION; MUTATION; PHYSIOLOGY; TIME FACTOR; VIROLOGY; VIRUS GENOME;

BACTERIA (MICROORGANISMS); FLAVOBACTERIUM COLUMNARE;

BACTERIOPHAGES; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; ENVIRONMENTAL MICROBIOLOGY; EVOLUTION, MOLECULAR; FLAVOBACTERIUM; GENOME, BACTERIAL; GENOME, VIRAL; HOST-PARASITE INTERACTIONS; MUTATION; TIME FACTORS;

EID: 85026379203     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00158-7     Document Type: Article

References (77)

1. Buckling, A. & Rainey, P. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. B Biol. Sci. 269, 931-936 (2002).
2. Brockhurst, M. A. et al. Running with the Red Queen: the role of biotic conflicts in evolution. Proc. R. Soc. B Biol. Sci. 281, 20141382 (2014).
3. Bohannan, B. J. M. & Lenski, R. E. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol. Lett. 3, 362-377 (2000).
4. Brockhurst, M. A., Buckling, A. & Rainey, P. B. The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa. Proc. R. Soc. B Biol. Sci. 272, 1385-1391 (2005).
5. Paez-Espino, D. et al. CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus. MBio. 6, e00262-15 (2015).
6. Gómez, P. & Buckling, A. Bacteria-phage antagonistic coevolution in soil. Science 332, 106-109 (2011).
7. Koskella, B. Phage-mediated selection on microbiota of a long-lived host. Curr. Biol. 23, 1256-1260 (2013).
8. Paterson, S. et al. Antagonistic coevolution accelerates molecular evolution. Nature 464, 275-U154 (2010).
9. Scanlan, P. D., Hall, A. R., Lopez-Pascua, L. D. C. & Buckling, A. Genetic basis of infectivity evolution in a bacteriophage. Mol. Ecol. 20, 981-989 (2010).
10. Lenski, R. E. & Levin, B. R. Constraints on the coevolution of bacteria and virulent phage: a model, some experiments, and predictions for natural communities. Am. Nat. 125, 585-602 (1985).
11. Betts, A., Rafaluk, C. & King, K. C. Host and parasite evolution in a tangled bank. Trends Parasitol. 32, 863-873 (2016).
12. Parratt, S. R. & Laine, A.-L. The role of hyperparasitism in microbial pathogen ecology and evolution. ISME J. 10, 1815-1822 (2016).
13. Barrangou, R. et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709-1712 (2007).
14. Makarova, K. S. et al. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13, 722-736 (2015).
15. Leenay, R. T. et al. Identifying and visualizing functional PAM diversity across CRISPR-Cas systems. Mol. Cell 62, 137-147 (2016).
16. Abudayyeh, O. O. et al. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353, aaf5573 (2016).
17. Levin, B. R., Moineau, S., Bushman, M. & Barrangou, R. The population and evolutionary dynamics of phage and bacteria with CRISPR-mediated immunity. PLoS Genet. 9, e1003312 (2013).
18. Deveau, H. et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190, 1390-1400 (2008).
19. Bondy-Denomy, J., Pawluk, A., Maxwell, K. L. & Davidson, A. R. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493, 429-432 (2013).
20. Bondy-Denomy, J. et al. Multiple mechanisms for CRISPR-Cas inhibition by anti-CRISPR proteins. Nature 526, 136-139 (2015).
21. Pawluk, A. et al. Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat. Rev. Microbiol. 1, 16085 (2016).
22. Rauch, B. J. et al. Inhibition of CRISPR-Cas9 with bacteriophage proteins. Cell 168, 150-158.e10 (2017).
23. Decaestecker, E. et al. Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature 450, 870-873 (2007).
24. Andersson, A. F. & Banfield, J. F. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320, 1047-1050 (2008).
25. Tyson, G. W. & Banfield, J. F. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ. Microbiol. 10, 200-2007 (2007).
26. Weinberger, A. D. et al. Persisting viral sequences shape microbial CRISPR-based immunity. PLoS Comput. Biol. 8, e1002475 (2012).
27. Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317-327 (2010).
28. Samson, J. E., Magadán, A. H., Sabri, M. & Moineau, S. Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11, 675-687 (2013).
29. Hamilton, R., Siva-Jothy, M. & Boots, M. Two arms are better than one: parasite variation leads to combined inducible and constitutive innate immune responses. Proc. R. Soc. B Biol. Sci. 275, 937-945 (2008).
30. Westra, E. R. et al. Parasite exposure drives selective evolution of constitutive versus inducible defense. Curr. Biol. 25, 1043-1049 (2015).
31. van Houte, S., Buckling, A. & Westra, E. R. Evolutionary ecology of prokaryotic immune mechanisms. Microbiol. Mol. Biol. Rev. 80, 745-763 (2016).
32. Scanlan, P. D., Buckling, A. & Hall, A. R. Experimental evolution and bacterial resistance: (co)evolutionary costs and trade-offs as opportunities in phage therapy research. Bacteriophage 5, e1050153 (2015).
33. Food and Agriculture Organization of the United Nations. The state of world fisheries and aquaculture. Opportunities and Challenges (FAO, 2014).
34. Romero, J., Feijoo, C. G. & Navaterre, P. Health and Environment in Aquaculture, 159-198 (InTech Europe, 2014).
35. Richards, G. P. Bacteriophage remediation of bacterial pathogens in aquaculture: a review of the technology. Bacteriophage 4, e975540 (2014).
36. Declercq, A. M., Haesebrouck, F., Van den Broeck, W., Bossier, P. & Decostere, A. Columnaris disease in fish: a review with emphasis on bacterium-host interactions. Vet. Res. 44, 27 (2013).
37. Laanto, E., Sundberg, L.-R. & Bamford, J. K. H. Phage specificity of the freshwater fish pathogen Flavobacterium columnare. Appl. Environ. Microbiol. 77, 7868-7872 (2011).
38. Gaba, S. & Ebert, D. Time-shift experiments as a tool to study antagonistic coevolution. Trends Ecol. Evol. 24, 226-232 (2009).
39. Tekedar, H. C. et al. Genome sequence of the fish Pathogen Flavobacterium columnare ATCC 49512. J. Bacteriol. 194, 2763-2764 (2012).
40. Burstein, D. et al. Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems. Nat. Commun. 7, 10613 (2016).
41. Smargon, A. A. et al. Cas13b Is a type VI-B CRISPR-associated RNA-guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Mol. Cell 65, 618-630.e (2017).
42. Hall, A. R., Scanlan, P. D. & Buckling, A. Bacteria-phage coevolution and the emergence of generalist pathogens. Am. Nat. 177, 44-53 (2011).
43. Yasmin, A. et al. Comparative genomics and transduction potential of Enterococcus faecalis temperate bacteriophages. J. Bacteriol. 192, 1122-1130 (2010).
44. Leggett, H. C., Buckling, A., Long, G. H. & Boots, M. Generalism and the evolution of parasite virulence. Trends Ecol. Evol. 28, 592-596 (2013).
45. Leckenby, A. & Hall, N. Genomic changes during evolution of animal parasitism in eukaryotes. Curr. Opin. Genet. Dev. 35, 86-92 (2015).
46. Johnson, C. M. & Grossman, A. D. Integrative and conjugative elements (ICEs): what they do and how they work. Annu. Rev. Genet. 49, 577-601 (2015).
47. Amitai, G. & Sorek, R. CRISPR-Cas adaptation: insights into the mechanism of action. Nat. Rev. Microbiol. 14, 67-76 (2016).
48. Savitskaya, E. et al. Dynamics of Escherichia coli type I-E CRISPR spacers over 42,000 years. Mol. Ecol. 26, 2019-2026 (2016).
49. Castillo, D., Christiansen, R. H., Dalsgaard, I., Madsen, L. & Middelboe, M. Bacteriophage resistance mechanisms in the fish pathogen Flavobacterium psychrophilum: linking genomic mutations to changes in bacterial virulence factors. Appl. Environ. Microbiol. 81, 1157-1167 (2015).
50. Lopatina, A. et al. Metagenomic analysis of bacterial communities of antarctic surface snow. Front. Microbiol. 7, 255 (2016).
51. Sun, C. L. et al. Phage mutations in response to CRISPR diversification in a bacterial population. Environ. Microbiol. 15, 463-470 (2013).
52. Sternberg, S. H., Richter, H., Charpentier, E. & Qimron, U. Adaptation in CRISPR-cas systems. Mol. Cell 61, 797-808 (2016).
53. Modell, J. W., Jiang, W. & Marraffini, L. A. CRISPR-Cas systems exploit viral DNA injection to establish and maintain adaptive immunity. Nature 544, 101-104 (2017).
54. Molineux, I. J. & Panja, D. Popping the cork: mechanisms of phage genome ejection. Nature 11, 194-204 (2013).
55. McGinn, J. & Marraffini, L. A. CRISPR-cas systems optimize their immune response by specifying the site of spacer integration. Mol. Cell 64, 616-623 (2016).
56. Vale, P. F. et al. Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus. Proc. R. Soc. B Biol. Sci. 282, 20151270 (2015).
57. van Houte, S. et al. The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 532, 385-388 (2016).
58. Vale, P. F. & Little, T. J. CRISPR-mediated phage resistance and the ghost of coevolution past. Proc. R. Soc. B Biol. Sci. 277, 2097-2103 (2010).
59. Sundberg, L.-R. et al. Intensive aquaculture selects for increased virulence and interference competition in bacteria. Proc. R. Soc. B Biol. Sci. 283, 20153069 (2016).
60. Laanto, E., Bamford, J. K. H., Laakso, J. & Sundberg, L.-R. Phage-driven loss of virulence in a fish pathogenic bacterium. PLoS ONE 7, e53157 (2012).
61. Laanto, E., Bamford, J. K. H., Ravantti, J. J. & Sundberg, L.-R. The use of phage FCL-2 as an alternative to chemotherapy against columnaris disease in aquaculture. Front. Microbiol. 6, 829 (2015).
62. Zhang, J. et al. Association of colony morphotypes with virulence, growth and resistance against protozoan predation in the fish pathogen Flavobacterium columnare. FEMS Microbiol. Ecol. 89, 553-562 (2014).
63. Song, Y. L., Fryer, J. L. & Rohovec, J. S. Comparison of six media for the cultivation of Flexibacter columnaris. Fish Pathol. 23, 81-94 (1988).
64. Decostere, A., Haesebrouck, F. & Devriese, L. Shieh medium supplemented with tobramycin for selective isolation of Flavobacterium columnare (Flexibacter columnaris) from diseased fish. J. Clin. Microbiol. 35, 322-324 (1997).
65. Kunttu, H. M. T., Sundberg, L.-R., Pulkkinen, K. & Valtonen, E. T. Environment may be the source of Flavobacterium columnare outbreaks at fish farms. Environ. Microbiol. Rep. 4, 398-402 (2012).
66. Ashrafi, R., Pulkkinen, K., Sundberg, L.-R., Pekkala, N. & Ketola, T. A multilocus sequence analysis scheme for characterization of Flavobacterium columnare isolates. BMC Microbiol. 15, 243-10 (2015).
67. Kunttu, H. M. T., Suomalainen, L.-R., Jokinen, E. I. & Valtonen, E. T. Flavobacterium columnare colony types: connection to adhesion and virulence? Microb. Pathog. 46, 21-27 (2009).
68. Kropinski, A. M. Measurement of the rate of attachment of bacteriophage to cells. Methods Mol. Biol. 501, 151-155 (2009).
69. Santos, M. A. An improved method for the small scale preparation of bacteriophage DNA based on phage precipitation by zinc chloride. Nucleic Acids Res. 19, 5442 (1991).
70. Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008).
71. Besemer, J., Lomsadze, A. & Borodovsky, M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 29, 2607-2618 (2001).
72. Delcher, A. L., Bratke, K. A., Powers, E. C. & Salzberg, S. L. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23, 673-679 (2007).
73. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845-858 (2015).
74. Biswas, A., Staals, R. H. J., Morales, S. E., Fineran, P. C. & Brown, C. M. CRISPRDetect: a flexible algorithm to define CRISPR arrays. BMC Genomics 17, 356 (2016).
75. Zhang, Y. et al. Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol. Cell 50, 488-503 (2013).
76. Leenay, R. T. & Beisel, C. L. Deciphering, communicating, and engineering the CRISPR PAM. J. Mol. Biol. 429, 177-191 (2016).
77. Li, M., Wang, R., Zhao, D. & Xiang, H. Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process. Nucleic Acids Res. 42, 2483-2492 (2014).