The phage growth limitation system in Streptomyces coelicolor A(3)2 is a toxin/antitoxin system, comprising enzymes with DNA methyltransferase, protein kinase and ATPase activity

Virology

Volumn 477, Issue , 2015, Pages 100-109

  Hoskisson, Paul A ^a,c   Sumby, Paul ^b,d   Smith, Margaret C M ^a,e  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Bacteriophage; Defence; Immunity; Modification; Restriction; Streptomyces

Indexed keywords

ADENOSINE TRIPHOSPHATASE; APRAMYCIN; DNA METHYLTRANSFERASE; KANAMYCIN; PROTEIN KINASE; BACTERIAL TOXIN; RESTRICTION ENDONUCLEASE; VIRUS DNA;

ACTINOMYCETALES INFECTION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL VIABILITY; BACTERIOPHAGE; BIOINFORMATICS; CONTROLLED STUDY; ENZYME ACTIVITY; NONHUMAN; PGL GENE; PGLX GENE; PGLY GENE; PGLZ GENE; PHAGE GROWTH LIMITATION SYSTEM; PRIORITY JOURNAL; PROTEIN FUNCTION; STREPTOMYCES COELICOLOR; STREPTOMYCES COELICOLOR INFECTION; TOXIN ANTITOXIN SYSTEM; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; METABOLISM; SIGNAL TRANSDUCTION; VIROLOGY;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

ADENOSINE TRIPHOSPHATASES; BACTERIAL TOXINS; BACTERIOPHAGES; DNA RESTRICTION ENZYMES; DNA, VIRAL; HOST-PARASITE INTERACTIONS; PROTEIN KINASES; SIGNAL TRANSDUCTION; STREPTOMYCES COELICOLOR;

EID: 84939543888     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.12.036     Document Type: Article

References (40)

1. Apweiler R., Attwood T.K., Bairoch A., Bateman A., Birney E., Biswas M., Bucher P., Cerutti L., Corpet F., Croning M.D., Durbin R., Falquet L., Fleischmann W., Gouzy J., Hermjakob H., Hulo N., Jonassen I., Kahn D., Kanapin A., Karavidopoulou Y., Lopez R., Marx B., Mulder N.J., Oinn T.M., Pagni M., Servant F., Sigrist C.J., Zdobnov E.M. InterPro-an integrated documentation resource for protein families, domains and functional sites. Bioinformatics 2000, 16:1145-1150.
2. Bayliss C.D., Callaghan M.J., Moxon E.R. High allelic diversity in the methyltransferase gene of a phase variable type III restriction-modification system has implications for the fitness of Haemophilus influenzae. Nucleic Acids Res. 2006, 34:4046-4059.
3. Bedford D.J., Laity C., Buttner M.J. Two genes involved in the phase-variable phi C31 resistance mechanism of Streptomyces coelicolor A3(2). J. Bacteriol. 1995, 177:4681-4689.
4. Bentley S.D., Chater K.F., Cerdeno-Tarraga A.M., Challis G.L., Thomson N.R., James K.D., Harris D.E., Quail M.A., Kieser H., Harper D., Bateman A., Brown S., Chandra G., Chen C.W., Collins M., Cronin A., Fraser A., Goble A., Hidalgo J., Hornsby T., Howarth S., Huang C.H., Kieser T., Larke L., Murphy L., Oliver K., O'Neil S., Rabbinowitsch E., Rajandream M.A., Rutherford K., Rutter S., Seeger K., Saunders D., Sharp S., Squares R., Squares S., Taylor K., Warren T., Wietzorrek A., Woodward J., Barrell B.G., Parkhill J., Hopwood D.A. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 2002, 417:141-147.
5. Bierman M., Logan R., O'Brien K., Seno E.T., Rao R.N., Schoner B.E. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 1992, 116:43-49.
6. Chinenova T.A., Mkrtumian N.M., Lomovskaia N.D. Genetic characteristics of a new phage resistance trait in Streptomyces coelicolor A3(2). Genetika 1982, 18:1945-1952.
7. Dryden D.T., Murray N.E., Rao D.N. Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Res. 2001, 29:3728-3741.
8. Finn R.D., Mistry J., Tate J., Coggill P., Heger A., Pollington J.E., Gavin O.L., Gunasekaran P., Ceric G., Forslund K., Holm L., Sonnhammer E.L., Eddy S.R., Bateman A. The Pfam protein families database. Nucleic Acids Res. 2010, 38:D211-D222.
9. Goldfarb T., Sberro H., Weinstock E., Cohen O., Doron S., Charpak-Amikam Y., Afik S., Ofir G., Sorek R. BREX is a novel phage resistance system widespread in microbial genomes. EMBO J 2014, pii: e201489455. [Epub ahead of print].
10. Gonzalez-Ceron G., Miranda-Olivares O.J., Servin-Gonzalez L. Characterization of the methyl-specific restriction system of Streptomyces coelicolor A3(2) and of the role played by laterally acquired nucleases. FEMS Microbiol. Lett. 2009, 301:35-43.
11. Gust B., Challis G.L., Fowler K., Kieser T., Chater K.F. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:1541-1546.
12. Hanks S.K., Hunter T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 1995, 9:576-596.
13. Hanks S.K., Quinn A.M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 1988, 241:42-52.
14. Hesketh A.R., Chandra G., Shaw A.D., Rowland J.J., Kell D.B., Bibb M.J., Chater K.F. Primary and secondary metabolism, and post-translational protein modifications, as portrayed by proteomic analysis of Streptomyces coelicolor. Mol. Microbiol. 2002, 46:917-932.
15. Hobbs G., Fraser C.M., Gardner D.J.C., Cullum J.A., Oliver S.G. Dispersed Growth of Streptomyces in liquid culture. Appl. Microbiol. Biotechnol. 1989, 31:272-277.
16. Hoskisson P.A., Smith M.C.M. Hypervariation and phase variation in the bacteriophage 'resistome'. Curr. Opin. Microbiol. 2007, 10:396-400.
17. Huang J., Shi J., Molle V., Sohlberg B., Weaver D., Bibb M.J. Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol. Microbiol. 2005, 58:1276-1287.
18. Hulo N., Bairoch A., Bulliard V., Cerutti L., Cuche B.A., de Castro E., Lachaize C., Langendijk-Genevaux P.S., Sigrist C.J. The 20 years of PROSITE. Nucleic Acids Res. 2008, 36:D245-D249.
19. Karata K., Inagawa T., Wilkinson A.J., Tatsuta T., Ogura T. Dissecting the role of a conserved motif (the second region of homology) in the AAA family of ATPases. Site-directed mutagenesis of the ATP-dependent protease FtsH. J. Biol. Chem. 1999, 274:26225-26232.
20. Khodakaramian G., Lissenden S., Gust B., Moir L., Hoskisson P.A., Chater K.F., Smith M.C. Expression of Cre recombinase during transient phage infection permits efficient marker removal in Streptomyces. Nucleic Acids Res. 2006, 34:e20.
21. Kieser T., Bibb M.J., Buttner M.J., Chater K.F., Hopwood D.A. Practical Streptomyces Genetics 2000, The John Innes Foundation, Norwich.
22. Laity C., Chater K.F., Lewis C.G., Buttner M.J. Genetic analysis of the phic31-specific phage growth limitation (Pgl) system of Streptomyces coelicolor A3(2). Mol. Microbiol. 1993, 7:329-336.
23. Lomovskaya N.D., Chater K.F., Mkrtumian N.M. Genetics and molecular biology of Streptomyces bacteriophages. Microbiol. Rev. 1980, 44:206-229.
24. MacNeil D.J. Characterization of a unique methyl-specific restriction system in Streptomyces avermitilis. J. Bacteriol. 1988, 170:5607-5612.
25. Makarova K.S., Wolf Y.I., Koonin E.V. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res. 2013, 41:4360-4377.
26. McGlynn P., Mahdi A.A., Lloyd R.G. Characterisation of the catalytically active form of RecG helicase. Nucleic Acids Res. 2000, 28:2324-2332.
27. Molle V., Girard-Blanc C., Kremer L., Doublet P., Cozzone A.J., Prost J.F. Protein PknE, a novel transmembrane eukaryotic-like serine/threonine kinase from Mycobacterium tuberculosis. Biochem. Biophys. Res. Commun. 2003, 308:820-825.
28. Murray N.E. Immigration control of DNA in bacteria: self versus non-self. Microbiology 2002, 148:3-20.
29. Parke D. Construction of mobilizable vectors derived from plasmids RP4, pUC18 and pUC19. Gene 1990, 93:135-137.
30. Pingoud A., Fuxreiter M., Pingoud V., Wende W. Type II restriction endonucleases: structure and mechanism. Cell. Mol. Life Sci. 2005, 62:685-707.
31. Quevillon E., Silventoinen V., Pillai S., Harte N., Mulder N., Apweiler R., Lopez R. InterProScan: protein domains identifier. Nucleic Acids Res. 2005, 33:W116-W120.
32. Ramakrishnan C., Dani V.S., Ramasarma T. A conformational analysis of Walker motif A [GXXXXGKT (S)] in nucleotide-binding and other proteins. Protein Eng. 2002, 15:783-798.
33. Redenbach M., Kieser H.M., Denapaite D., Eichner A., Cullum J., Kinashi H., Hopwood D.A. A set of ordered cosmids and a detailed genetic and physical map for the 8Mb Streptomyces coelicolor A3(2) chromosome. Mol. Microbiol. 1996, 21:77-96.
34. 6-methyltransferase. J. Biol. Chem. 1998, 273:17333-17342.
35. Scavetta R.D., Thomas C.B., Walsh M.A., Szegedi S., Joachimiak A., Gumport R.I., Churchill M.E. Structure of RsrI methyltransferase, a member of the N6-adenine beta class of DNA methyltransferases. Nucleic Acids Res. 2000, 28:3950-3961.
36. Sumby P., Smith M.C.M. Genetics of the phage growth limitation (Pgl) system of Streptomyces coelicolor A3(2). Mol. Microbiol. 2002, 44:489-500.
37. Sumby P., Smith M.C.M. Phase variation in the phage growth limitation system of Streptomyces coelicolor A3(2). J. Bacteriol. 2003, 185:4558-4563.
38. Tabor S., Richardson C.C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:1074-1078.
39. Weinbauer M.G., Rassoulzadegan F. Are viruses driving microbial diversification and diversity?. Environ. Microbiol. 2004, 6:1-11.
40. Young T.A., Delagoutte B., Endrizzi J.A., Falick A.M., Alber T. Structure of Mycobacterium tuberculosis PknB supports a universal activation mechanism for Ser/Thr protein kinases. Nat. Struct. Biol. 2003, 10:168-174.