Anti-phage islands force their target phage to directly mediate island excision and spread

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  McKitterick, Amelia C ^a   Seed, Kimberley D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHAN ZUCKERBERG BIOHUB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; PHAGE INDUCIBLE CHROMOSOMAL ISLAND LIKE ELEMENT 1; PROTEIN; RECOMBINASE; SERINE; UNCLASSIFIED DRUG; BACTERIAL DNA; VIRAL PROTEIN;

ARTICLE; BACTERIOPHAGE; CHOLERA; ECTOPIC EXPRESSION; EXCISION; GENE PRODUCT; GENOME ANALYSIS; IN VITRO STUDY; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; NONHUMAN; SEQUENCE ANALYSIS; VIBRIO CHOLERAE; BACTERIAL GENOME; CONSERVED SEQUENCE; CRISPR CAS SYSTEM; GENETIC RECOMBINATION; GENETICS; GENOMICS; INTERSPERSED REPEAT; METABOLISM; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PROTEIN DOMAIN; VIROLOGY;

BACTERIA (MICROORGANISMS); VIBRIO CHOLERAE;

BACTERIOPHAGES; CONSERVED SEQUENCE; CRISPR-CAS SYSTEMS; DNA, BACTERIAL; GENOME, BACTERIAL; GENOMICS; INTERSPERSED REPETITIVE SEQUENCES; OPEN READING FRAMES; POLYMERASE CHAIN REACTION; PROTEIN DOMAINS; RECOMBINATION, GENETIC; VIBRIO CHOLERAE; VIRAL PROTEINS;

EID: 85048718270     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-018-04786-5     Document Type: Article

References (43)

1. Dy, R. L., Richter, C., Salmond, G. P. C. & Fineran, P. C. Remarkable mechanisms in microbes to resist phage infections. Annu. Rev. Virol. 1, 307-331 (2014).
2. Samson, J. E., Magadan, A. H., Sabri, M. & Moineau, S. Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11, 675-687 (2013).
3. Koskella, B. & Brockhurst, M. A. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38, 916-931 (2014).
4. Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317-327 (2010).
5. Penades, J. R. & Christie, G. E. The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. Annu. Rev. Virol. 2, 181-201 (2015).
6. Ram, G. et al. Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism. Proc. Natl. Acad. Sci. 109, 16300-16305 (2012).
7. Lindsay, Ja, Ruzin, A., Ross, H. F., Kurepina, N. & Novick, R. P. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol. Microbiol. 29, 527-543 (1998).
8. Ubeda, C. et al. SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage. Mol. Microbiol. 67, 493-503 (2008).
9. Tormo-Mas, M. A. et al. Moonlighting bacteriophage proteins derepress staphylococcal pathogenicity islands. Nature 465, 779-782 (2010).
10. Poliakov, A. et al. Capsid size determination by Staphylococcus aureus pathogenicity island SaPI1 involves specific incorporation of SaPI1 proteins into procapsids. J. Mol. Biol. 380, 465-475 (2008).
11. Ubeda, C. et al. Specificity of staphylococcal phage and SaPI DNA packaging as revealed by integrase and terminase mutations. Mol. Microbiol. 72, 98-108 (2009).
12. Ram, G., Chen, J., Ross, H. F. & Novick, R. P. Precisely modulated pathogenicity island interference with late phage gene transcription. Proc. Natl. Acad. Sci. U. S. A. 111, 14536-14541 (2014).
13. Seed, K. D. et al. Evolutionary consequences of intra-patient phage predation on microbial populations. eLife 3, e03497 (2014).
14. Nelson, E. J., Harris, J. B., Morris, J. G., Calderwood, S. B. & Camilli, A. Cholera transmission: the host, pathogen and bacteriophage dynamic. Nat. Rev. Microbiol. 7, 693-702 (2009).
15. D'Herelle, F. & Malone, R. H. A Preliminary report of work carried out by the cholera bacteriophage enquiry. Ind. Med. Gaz. 62, 614-616 (1927).
16. Faruque, S. M. et al. Self-limiting nature of seasonal cholera epidemics: Role of host-mediated amplification of phage. Proc. Natl. Acad. Sci. U. S. A 102, 6119-6124 (2005).
17. Seed, K. D. et al. Evidence of a dominant lineage of Vibrio cholerae-Specific lytic bacteriophages shed by cholera patiens over a 10-year period in Dhaka, Bangladesh. mBio 2, e00334-10 (2011).
18. Seed, K. D., Lazinski, D. W., Calderwood, S. B. & Camilli, A. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494, 489-491 (2013).
19. Naser, I. Bin, Hoque, M. M., Nahid, M. A., Rocky, M. K. & Faruque, S. M. Analysis of the CRISPR-Cas system in bacteriophages active on epidemic strains of Vibrio cholerae in Bangladesh. Sci. Rep. 7, 14880 (2017).
20. O'Hara, B. J., Barth, Z. K., McKitterick, A. C. & Seed, K. D. A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome. PLoS. Genet. 13, e1006838 (2017).
21. Smith, M. C. M. Phage-encoded serine integrases and other large serine recombinases. Micro. Biol. Spec. 3, 253-272 (2015).
22. Thorpe, H. M. & Smith, M. C. In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc. Natl. Acad. Sci. U. S. A. 95, 5505-5510 (1998).
23. Kuhstoss, S. & Rao, R. N. Analysis of the integration function of the streptomycete bacteriophage φC31. J. Mol. Biol. 222, 897-908 (1991).
24. Bibb, L. A., Hancox, M. I. & Hatfull, G. F. Integration and excision by the large serine recombinase φ Rv1 integrase. Mol. Microbiol. 55, 1896-1910 (2005).
25. Khaleel, T., Younger, E., Mcewan, A. R., Varghese, A. S. & Smith, M. C. A phage protein that binds φ C31 integrase to switch its directionality. Mol. Microbiol. 80, 1450-1463 (2011).
26. Savinov, A., Pan, J., Ghosh, P. & Hatfull, G. F. The Bxb1 gp47 recombination directionality factor is required not only for prophage excision, but also for phage DNA replication. Gene. 495, 42-48 (2012).
27. Fogg, P. C., Colloms, S., Rosser, S., Stark, M. & Smith, M. C. New applications for phage integrases. J. Mol. Biol. 426, 2703-2716 (2014).
28. Ghosh, P., Wasil, L. R. & Hatfull, G. F. Control of phage Bxb1 excision by a novel recombination directionality factor. PLoS Biol. 4, e186 (2006).
29. Bowring, J. et al. Pirating conserved phage mechanisms promotes promiscuous staphylococcal pathogenicity island transfer. eLife 6, e26487 (2017).
30. Frigols, B. et al. Virus satellites drive viral evolution and ecology. PLoS. Genet. 11, e1005609 (2015).
31. Misiura, A. et al. Roles of two large serine recombinases in mobilizing the methicillin-resistance cassette SCCmec. Mol. Microbiol. 88, 1218-1229 (2013).
32. Yen, M., Cairns, L. S. & Camilli, A. A cocktail of three virulent bacteriophages prevents Vibrio cholerae infection in animal models. Nat. Commun. 8, 14187 (2017).
33. Clokie, M. R. J. & Kropinski, A. M. (eds) Bacteriophages: Methods and Protocols. Methods in Molecular Biology (Humana Press, New York, 2009).
34. Dalia, A. B., Lazinski, D. W. & Camilli, A. Identification of a membrane-bound transcriptional regulator that links chitin and natural competence in Vibrio cholerae. mBio 5, e01028-13 (2014).
35. Furste, J. P. et al. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene. 48, 119-131 (1986).
36. Topp, S. et al. Synthetic riboswitches that induce gene expression in diverse bacterial species. Appl. Environ. Microbiol. 76, 7881-7884 (2010).
37. Box, A. M., McGuffie, M. J., O'Hara, B. J. & Seed, K. D. Functional analysis of bacteriophage immunity through a type I-E CRISPR-Cas system in Vibrio cholerae and its application in bacteriophage genome engineering. J. Bacteriol. 198, 578-590 (2015).
38. Ouellette, S. P., Karimova, G., Davi, M. & Ladant, D. Analysis of membrane protein interactions with a bacterial adenylate cyclase-based two-hybrid (bACTH) technique. Curr. Protoc. Mol. Biol. 118, 20. 12. 1-20. 12. 24 (2017).
39. Marchler-Bauer, A. et al. CDD/SPARCLE: Functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 45, D200-D203 (2017).
40. Alva, V., Nam, S.-Z., Soding, J. & Lupas, A. N. The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis. Nucleic Acids Res. 44, W410-W415 (2016).
41. Crooks, G., Hon, G., Chandonia, J. & Brenner, S. WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190 (2004).
42. Bawono, P. & Heringa, J. PRALINE: a versatile multiple sequence alignment toolkit. Methods Mol. Bio 1079, 245-262 (2014).
43. Li, W. et al. The EMBL-EBI bioinformatics web and programmatic tools framework. Nucl. Acids Res. 43, W580-W584 (2015).