1887

Abstract

Aeromonas species are causative agents of a wide spectrum of diseases in animals and humans. Although these bacteria are commonly found in various environments, little is known about their phages. Thus far, only one temperate Aeromonas phage has been characterized. Whole-genome sequencing of an Aeromonas sp. strain ARM81 revealed the presence of two prophage clusters. One of them is integrated into the chromosome and the other was maintained as an extrachromosomal, linear plasmid-like prophage encoding a protelomerase. Both prophages were artificially and spontaneously inducible. We separately isolated both phages and compared their genomes with other known viruses. The novel phages show no similarity to the previously characterized Aeromonas phages and might represent new evolutionary lineages of viruses infecting Aeromonadaceae. Apart from the comparative genomic analyses of these phages, complemented with their structural and molecular characterization, a functional analysis of four DNA methyltransferases encoded by these viruses was conducted. One of the investigated N6-adenine-modifying enzymes shares sequence specificity with a Dam-like methyltransferase of its bacterial host, while another one is non-specific, as it catalyzes adenine methylation in various sequence contexts. The presented results shed new light on the diversity of Aeromonas temperate phages.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000504
2016-08-01
2019-09-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/8/2008.html?itemId=/content/journal/jgv/10.1099/jgv.0.000504&mimeType=html&fmt=ahah

References

  1. Alanis Villa A. , Kropinski A. M. , Abbasifar R. , Griffiths M. W. . ( 2012;). Complete genome sequence of Vibrio parahaemolyticus bacteriophage vB_VpaM_MAR. . J Virol 86: 13138–13139. [CrossRef] [PubMed]
    [Google Scholar]
  2. Altschul S. F. , Madden T. L. , Schäffer A. A. , Zhang J. , Zhang Z. , Miller W. , Lipman D. J. . ( 1997;). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. . Nucleic Acids Res 25: 3389–3402. [CrossRef] [PubMed]
    [Google Scholar]
  3. Apweiler R. , Bairoch A. , Wu C. H. , Barker W. C. , Boeckmann B. , Ferro S. , Gasteiger E. , Huang H. , Lopez R. et al. ( 2004;). UniProt: the Universal Protein knowledgebase. . Nucleic Acids Res 32: D115–119. [CrossRef] [PubMed]
    [Google Scholar]
  4. Aranda J. , Roca M. , Tuñón I. , PvuII. A. . ( 2012;). Substrate promiscuity in DNA methyltransferase M.PvuII. A mechanistic insight. . Org Biomol Chem 10: 5395–5400. [CrossRef] [PubMed]
    [Google Scholar]
  5. Beilstein F. , Dreiseikelmann B. . ( 2008;). Temperate bacteriophage PhiO18P from an Aeromonas media isolate: characterization and complete genome sequence. . Virology 373: 25–29. [CrossRef] [PubMed]
    [Google Scholar]
  6. Bujnicki J. M. , Radlinska M. , Zaleski P. , Piekarowicz A. . ( 2001;). Cloning of the Haemophilus influenzae Dam methyltransferase and analysis of its relationship to the Dam methyltransferase encoded by the HP1 phage. . Acta Biochim Pol 48: 969–983.[PubMed]
    [Google Scholar]
  7. Canchaya C. , Fournous G. , Brüssow H. . ( 2004;). The impact of prophages on bacterial chromosomes. . Mol Microbiol 53: 9–18. [CrossRef] [PubMed]
    [Google Scholar]
  8. Carver T. , Berriman M. , Tivey A. , Patel C. , Böhme U. , Barrell B. G. , Parkhill J. , Rajandream M. A. . ( 2008;). Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. . Bioinformatics 24: 2672–2676. [CrossRef] [PubMed]
    [Google Scholar]
  9. Casjens S. . ( 2003;). Prophages and bacterial genomics: what have we learned so far?. Mol Microbiol 49: 277–300.[PubMed] [CrossRef]
    [Google Scholar]
  10. Casjens S. R. , Gilcrease E. B. , Huang W. M. , Bunny K. L. , Pedulla M. L. , Ford M. E. , Houtz J. M. , Hatfull G. F. , Hendrix R. W. . ( 2004;). The pKO2 linear plasmid prophage of Klebsiella oxytoca . . J Bacteriol 186: 1818–1832.[PubMed] [CrossRef]
    [Google Scholar]
  11. Casjens S. R. , Gilcrease E. B. . ( 2009;). Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. . Methods Mol Biol 502: 91–111. [CrossRef] [PubMed]
    [Google Scholar]
  12. Catalano C. E. . ( 2000;). The terminase enzyme from bacteriophage lambda: a DNA-packaging machine. . Cell Mol Life Sci 57: 128–148. [CrossRef] [PubMed]
    [Google Scholar]
  13. Chan X. Y. , Chua K. H. , Yin W. F. , Puthucheary S. D. , Chan K. G. . ( 2014;). Whole-genome analysis of Aeromonas hydrophila strain 187, exhibiting quorum-sensing activity. . Genome Announc 2: e01360-14. [CrossRef] [PubMed]
    [Google Scholar]
  14. Clark T. A. , Murray I. A. , Morgan R. D. , Kislyuk A. O. , Spittle K. E. , Boitano M. , Fomenkov A. , Roberts R. J. , Korlach J. . ( 2012;). Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing. . Nucleic Acids Res 40: e29. [CrossRef] [PubMed]
    [Google Scholar]
  15. Coulby J. N. , Sternberg N. L. . ( 1988;). Characterization of the phage P1 dam gene. . Gene 74: 191. [CrossRef] [PubMed]
    [Google Scholar]
  16. Deppenmeier U. , Johann A. , Hartsch T. , Merkl R. , Schmitz R. A. , Martinez-Arias R. , Henne A. , Wiezer A. , Bäumer S. et al. ( 2002;). The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea. . J Mol Microbiol Biotechnol 4: 453–461.[PubMed]
    [Google Scholar]
  17. Dodd I. B. , Egan J. B. . ( 1990;). Improved detection of helix-turn-helix DNA-binding motifs in protein sequences. . Nucleic Acids Res 18: 5019–5026. [CrossRef] [PubMed]
    [Google Scholar]
  18. Drozdz M. , Piekarowicz A. , Bujnicki J. M. , Radlinska M. . ( 2012;). Novel non-specific DNA adenine methyltransferases. . Nucleic Acids Res 40: 2119–2130. [CrossRef] [PubMed]
    [Google Scholar]
  19. Dziewit L. , Czarnecki J. , Wibberg D. , Radlinska M. , Mrozek P. , Szymczak M. , Schlüter A. , Pühler A. , Bartosik D. . ( 2014a;). Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids. . BMC Genomics 15: 124. [CrossRef] [PubMed]
    [Google Scholar]
  20. Dziewit L. , Oscik K. , Bartosik D. , Radlinska M. . ( 2014b;). Molecular characterization of a novel temperate Sinorhizobium bacteriophage, ФLM21, encoding DNA methyltransferase with CcrM-like specificity. . J Virol 88: 13111–13124. [CrossRef]
    [Google Scholar]
  21. Dziewit L. , Pyzik A. , Szuplewska M. , Matlakowska R. , Mielnicki S. , Wibberg D. , Schlüter A. , Pühler A. , Bartosik D. . ( 2015;). Diversity and role of plasmids in adaptation of bacteria inhabiting the Lubin copper mine in Poland, an environment rich in heavy metals. . Front Microbiol 6: 152. [CrossRef] [PubMed]
    [Google Scholar]
  22. Emond-Rheault J.-G. , Vincent A. T. , Trudel M. V. , Brochu F. , Boyle B. , Tanaka K. H. , Attéré S. A. , Jubinville É. , Loch T. P. et al. ( 2015a;). Variants of a genomic island in Aeromonas salmonicida subsp. salmonicida link isolates with their geographical origins. . Veterinary Microbiology 175: 68–76. [CrossRef]
    [Google Scholar]
  23. Emond-Rheault J.-G. , Vincent A. T. , Trudel M. , Frey J. , Frenette M. , Charette S. J. . ( 2015b;). AsaGEI2b : a new variant of a genomic island identified in the Aeromonas salmonicida subsp. salmonicida JF3224 strain isolated from a wild fish in Switzerland. . FEMS Microbiol Lett 362: fnv093. [CrossRef]
    [Google Scholar]
  24. Erova T. E. , Fadl A. A. , Sha J. , Khajanchi B. K. , Pillai L. L. , Kozlova E. V. , Chopra A. K. . ( 2006a;). Mutations within the catalytic motif of DNA adenine methyltransferase (Dam) of Aeromonas hydrophila cause the virulence of the Dam-overproducing strain to revert to that of the wild-type phenotype. . Infect Immun 74: 5763–5772. [CrossRef]
    [Google Scholar]
  25. Erova T. E. , Pillai L. , Fadl A. A. , Sha J. , Wang S. , Galindo C. L. , Chopra A. K. . ( 2006b;). DNA adenine methyltransferase influences the virulence of Aeromonas hydrophila . . Infect Immun 74: 410–424. [CrossRef]
    [Google Scholar]
  26. Erova T. E. , Kosykh V. G. , Sha J. , Chopra A. K. . ( 2012;). DNA adenine methyltransferase (Dam) controls the expression of the cytotoxic enterotoxin (act) gene of Aeromonas hydrophila via tRNA modifying enzyme-glucose-inhibited division protein (GidA). . Gene 498: 280–287. [CrossRef] [PubMed]
    [Google Scholar]
  27. Fang G. , Munera D. , Friedman D. I. , Mandlik A. , Chao M. C. , Banerjee O. , Feng Z. , Losic B. , Mahajan M. C. et al. ( 2012;). Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing. . Nat Biotechnol 30: 1232–1239. [CrossRef] [PubMed]
    [Google Scholar]
  28. Finn R. D. , Bateman A. , Clements J. , Coggill P. , Eberhardt R. Y. , Eddy S. R. , Heger A. , Hetherington K. , Holm L. et al. ( 2014;). Pfam: the protein families database. . Nucleic Acids Res 42: D222–230. [CrossRef] [PubMed]
    [Google Scholar]
  29. Fortier L. C. , Sekulovic O. . ( 2013;). Importance of prophages to evolution and virulence of bacterial pathogens. . Virulence 4: 354–365. [CrossRef] [PubMed]
    [Google Scholar]
  30. Gerdes K. , Møller-Jensen J. , Bugge Jensen R. . ( 2000;). Plasmid and chromosome partitioning: surprises from phylogeny. . Mol Microbiol 37: 455–466.[PubMed] [CrossRef]
    [Google Scholar]
  31. Goerke C. , Pantucek R. , Holtfreter S. , Schulte B. , Zink M. , Grumann D. , Bröker B. M. , Doskar J. , Wolz C. . ( 2009;). Diversity of prophages in dominant Staphylococcus aureus clonal lineages. . J Bacteriol 191: 3462–3468. [CrossRef] [PubMed]
    [Google Scholar]
  32. Grainge I. , Jayaram M. . ( 1999;). The integrase family of recombinase: organization and function of the active site. . Mol Microbiol 33: 449–456.[PubMed] [CrossRef]
    [Google Scholar]
  33. Gray M. D. , Lampel K. A. , Strockbine N. A. , Fernandez R. E. , Melton-Celsa A. R. , Maurelli A. T. . ( 2014;). Clinical isolates of Shiga toxin 1a-producing Shigella flexneri with an epidemiological link to recent travel to Hispañiola. . Emerg Infect Dis 20: 1669–1677. [CrossRef] [PubMed]
    [Google Scholar]
  34. Hammerl J. A. , Roschanski N. , Lurz R. , Johne R. , Lanka E. , Hertwig S. . ( 2015;). The molecular switch of telomere phages: high binding specificity of the PY54 Cro lytic repressor to a single operator site. . Viruses 7: 2771–2793. [CrossRef] [PubMed]
    [Google Scholar]
  35. Hattman S. , Newman L. , Murthy H. M. , Nagaraja V. . ( 1991;). Com, the phage Mu mom translational activator, is a zinc-binding protein that binds specifically to its cognate mRNA. . Proc Natl Acad Sci U S A 88: 10027–10031.[PubMed] [CrossRef]
    [Google Scholar]
  36. Hattman S. . ( 1999;). Unusual transcriptional and translational regulation of the bacteriophage Mu mom operon. . Pharmacol Ther 84: 367–388. [CrossRef] [PubMed]
    [Google Scholar]
  37. Heithoff D. M. , Sinsheimer R. L. , Low D. A. , Mahan M. J. . ( 1999;). An essential role for DNA adenine methylation in bacterial virulence. . Science 284: 967–970. [CrossRef] [PubMed]
    [Google Scholar]
  38. Hertwig S. , Klein I. , Lurz R. , Lanka E. , Appel B. . ( 2003;). PY54, a linear plasmid prophage of Yersinia enterocolitica with covalently closed ends. . Mol Microbiol 48: 989–1003.[PubMed] [CrossRef]
    [Google Scholar]
  39. Igbinosa I. H. , Okoh A. I. , Igumbor E. U. , Aghdasi F. , Tom M. . ( 2012;). Antibiotic susceptibility profile of Aeromonas species isolated from wastewater treatment plant. . Scientific World J 2012: 764563. [CrossRef] [PubMed]
    [Google Scholar]
  40. Julio S. M. , Heithoff D. M. , Provenzano D. , Klose K. E. , Sinsheimer R. L. , Low D. A. , Mahan M. J. . ( 2001;). DNA adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae . . Infect Immun 69: 7610–7615. [CrossRef] [PubMed]
    [Google Scholar]
  41. Kim J. H. , Son J. S. , Choresca C. H. , Shin S. P. , Han J. E. , Jun J. W. , Kang D. H. , Oh C. , Heo S. J. , Park S. C. . ( 2012;). Complete genome sequence of bacteriophage phiAS7, a T7-like virus that infects Aeromonas salmonicida subsp. salmonicida . . J Virol 86: 2894–2895. [CrossRef] [PubMed]
    [Google Scholar]
  42. Lan S. F. , Huang C. H. , Chang C. H. , Liao W. C. , Lin I. H. , Jian W. N. , Wu Y. G. , Chen S. Y. , Wong H. C. . ( 2009;). Characterization of a new plasmid-like prophage in a pandemic Vibrio parahaemolyticus O3:K6 strain. . Appl Environ Microbiol 75: 2659–2667. [CrossRef] [PubMed]
    [Google Scholar]
  43. Laslett D. , Canback B. . ( 2004;). ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. . Nucleic Acids Res 32: 11–16. [CrossRef] [PubMed]
    [Google Scholar]
  44. Lavigne R. , Darius P. , Summer E. J. , Seto D. , Mahadevan P. , Nilsson A. S. , Ackermann H. W. , Kropinski A. M. . ( 2009;). Classification of Myoviridae bacteriophages using protein sequence similarity. . BMC Microbiol 9: 224. [CrossRef] [PubMed]
    [Google Scholar]
  45. Letunic I. , Doerks T. , Bork P. . ( 2012;). SMART 7: recent updates to the protein domain annotation resource. . Nucleic Acids Res 40: D302–305. [CrossRef] [PubMed]
    [Google Scholar]
  46. Lima-Mendez G. , Van Helden J. , Toussaint A. , Leplae R. . ( 2008;). Reticulate representation of evolutionary and functional relationships between phage genomes. . Mol Biol Evol 25: 762–777. [CrossRef] [PubMed]
    [Google Scholar]
  47. Mallory J. B. , Alfano C. , McMacken R. . ( 1990;). Host virus interactions in the initiation of bacteriophage lambda DNA replication. Recruitment of Escherichia coli DnaB helicase by lambda P replication protein. . J Biol Chem 265: 13297–13307.[PubMed]
    [Google Scholar]
  48. Marinus M. G. , Casadesus J. . ( 2009;). Roles of DNA adenine methylation in host-pathogen interactions: mismatch repair, transcriptional regulation, and more. . FEMS Microbiol Rev 33: 488–503. [CrossRef] [PubMed]
    [Google Scholar]
  49. Mobberley J. M. , Authement R. N. , Segall A. M. , Paul J. H. . ( 2008;). The temperate marine phage PhiHAP-1 of Halomonas aquamarina possesses a linear plasmid-like prophage genome. . J Virol 82: 6618–6630. [CrossRef] [PubMed]
    [Google Scholar]
  50. Moriel B. , Cruz L. M. , Dallagassa C. B. , Faoro H. , de Souza E. M. , Pedrosa F. O. , Rego F. G. , Picheth G. , Fadel-Picheth C. M. . ( 2015;). Draft genome sequence of Aeromonas caviae 8LM, isolated from stool culture of a child with diarrhea. . Genome Announc 3: e0052415. [CrossRef] [PubMed]
    [Google Scholar]
  51. Nettmann E. , Bergmann I. , Mundt K. , Linke B. , Klocke M. . ( 2008;). Archaea diversity within a commercial biogas plant utilizing herbal biomass determined by 16S rDNA and mcrA analysis. . J Appl Microbiol 105: 1835–1850. [CrossRef] [PubMed]
    [Google Scholar]
  52. Niu Y. D. , Cook S. R. , Wang J. , Klima C. L. , Hsu Y. H. , Kropinski A. M. , Turner D. , McAllister T. A. . ( 1975;). Comparative analysis of multiple inducible phages from Mannheimia haemolytica . . BMC Microbiol 15:.
    [Google Scholar]
  53. Oakey H. J. , Cullen B. R. , Owens L. . ( 2002;). The complete nucleotide sequence of the Vibrio harveyi bacteriophage VHML. . J Appl Microbiol 93: 1089–1098.[PubMed] [CrossRef]
    [Google Scholar]
  54. Oberto J. , Weisberg R. A. , Gottesman M. E. . ( 1989;). Structure and function of the nun gene and the immunity region of the lambdoid phage HK022. . J Mol Biol 207: 675–693.[PubMed] [CrossRef]
    [Google Scholar]
  55. Oliveira P. H. , Touchon M. , Rocha E. P. . ( 2014;). The interplay of restriction-modification systems with mobile genetic elements and their prokaryotic hosts. . Nucleic Acids Res 42: 10618–10631. [CrossRef] [PubMed]
    [Google Scholar]
  56. Page R. D. . ( 1996;). TreeView: an application to display phylogenetic trees on personal computers. . Comput Appl Biosci 12: 357–358.[PubMed]
    [Google Scholar]
  57. Pang M. , Jiang J. , Xie X. , Wu Y. , Dong Y. , Kwok A. H. , Zhang W. , Yao H. , Lu C. et al. ( 2015;). Novel insights into the pathogenicity of epidemic Aeromonas hydrophila ST251 clones from comparative genomics. . Sci Rep 5: 9833. [CrossRef] [PubMed]
    [Google Scholar]
  58. Piekarowicz A. , Bujnicki J. . ( 1999;). Cloning of the Dam methyltransferase gene from Haemophilus influenzae bacteriophage HP1. . Acta Microbiol Pol 48: 123–129.[PubMed]
    [Google Scholar]
  59. Radlinska M. , Bujnicki J. M. . ( 2001;). Cloning of enterohemorrhagic Escherichia coli phage VT-2 dam methyltransferase. . Acta Microbiol Pol 50: 161–167.[PubMed]
    [Google Scholar]
  60. Rasko D. A. , Webster D. R. , Sahl J. W. , Bashir A. , Boisen N. , Scheutz F. , Paxinos E. E. , Sebra R. , Chin C. S. et al. ( 2011;). Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. . N Engl J Med 365: 709–717. [CrossRef] [PubMed]
    [Google Scholar]
  61. Ravin N. V. . ( 2003;). Mechanisms of replication and telomere resolution of the linear plasmid prophage N15. . FEMS Microbiol Lett 221: 1–6. [CrossRef] [PubMed]
    [Google Scholar]
  62. Ravin N. V. . ( 2015;). Replication and maintenance of linear phage-plasmid N15. . Microbiol Spectr 3: 0032–2014. [CrossRef]
    [Google Scholar]
  63. Refardt D. . ( 2011;). Within-host competition determines reproductive success of temperate bacteriophages. . ISME J 5: 1451–1460. [CrossRef] [PubMed]
    [Google Scholar]
  64. Refardt D. , Bergmiller T. , Kümmerli R. . ( 2013;). Altruism can evolve when relatedness is low: evidence from bacteria committing suicide upon phage infection. . Proc Biol Sci 280: 20123035. [CrossRef] [PubMed]
    [Google Scholar]
  65. Tekedar H. C. , Karsi A. , Akgul A. , Kalindamar S. , Waldbieser G. C. , Sonstegard T. , Schroeder S. G. , Lawrence M. L. . ( 2015;). Complete genome sequence of an Edwardsiella piscicida-like species, recovered from Tilapia in the United States. . Genome Announc 3: e0100401015. [CrossRef] [PubMed]
    [Google Scholar]
  66. Reisenauer A. , Kahng L. S. , McCollum S. , Shapiro L. . ( 1999;). Bacterial DNA methylation: a cell cycle regulator?. J Bacteriol 181: 5135–5139.[PubMed]
    [Google Scholar]
  67. Rigden D. J. , Jedrzejas M. J. , Galperin M. Y. . ( 2003;). Amidase domains from bacterial and phage autolysins define a family of gamma-D,L-glutamate-specific amidohydrolases. . Trends Biochem Sci 28: 230–234. [CrossRef] [PubMed]
    [Google Scholar]
  68. Roberts R. J. , Vincze T. , Posfai J. , Macelis D. . ( 2015;). REBASE--a database for DNA restriction and modification: enzymes, genes and genomes. . Nucleic Acids Res 43: D298–299. [CrossRef] [PubMed]
    [Google Scholar]
  69. Robinson V. L. , Oyston P. C. , Titball R. W. . ( 2005;). A dam mutant of Yersinia pestis is attenuated and induces protection against plague. . FEMS Microbiol Lett 252: 251–256. [CrossRef] [PubMed]
    [Google Scholar]
  70. Sambrook J. , Russell D. W. . ( 2001;). Cold Spring Harbor. . Molecular Cloning: A Laboratory Manual. N. Y:: Cold Spring Harbor Laboratory Press;.
    [Google Scholar]
  71. Sauer R. T. , Pan J. , Hopper P. , Hehir K. , Brown J. , Poteete A. R. . ( 1981;). Primary structure of the phage P22 repressor and its gene c2 . . Biochemistry 20: 3591–3598. [CrossRef] [PubMed]
    [Google Scholar]
  72. Schattner P. , Brooks A. N. , Lowe T. M. . ( 2005;). The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. . Nucleic Acids Res 33: W686–689. [CrossRef] [PubMed]
    [Google Scholar]
  73. Scherzer E. , Auer B. , Schweiger M. . ( 1987;). Identification, purification, and characterization of Escherichia coli virus T1 DNA methyltransferase. . J Biol Chem 262: 15225–15231.[PubMed]
    [Google Scholar]
  74. Schubert R. A. , Dodd I. B. , Egan J. B. , Shearwin K. E. . ( 2007;). Cro's role in the CI-Cro bistable switch is critical for λ's transition from lysogeny to lytic development. . Genes Dev. 21: 2461–2472. [CrossRef] [PubMed]
    [Google Scholar]
  75. Seed K. D. . ( 2015;). Battling phages: how bacteria defend against viral attack. . PLoS Pathog 11: e1004847. [CrossRef] [PubMed]
    [Google Scholar]
  76. Siguier P. , Perochon J. , Lestrade L. , Mahillon J. , Chandler M. . ( 2006;). ISfinder: the reference centre for bacterial insertion sequences. . Nucleic Acids Res 34: D32–36. [CrossRef] [PubMed]
    [Google Scholar]
  77. Smeesters P. R. , Drèze P. A. , Bousbata S. , Parikka K. J. , Timmery S. , Hu X. , Perez-Morga D. , Deghorain M. , Toussaint A. et al. ( 2011;). Characterization of a novel temperate phage originating from a cereulide-producing Bacillus cereus strain. . Res Microbiol 162: 446–459. [CrossRef] [PubMed]
    [Google Scholar]
  78. Snyder L. . ( 1995;). Phage-exclusion enzymes: a bonanza of biochemical and cell biology reagents?. Mol Microbiol 15: 415–420.[PubMed] [CrossRef]
    [Google Scholar]
  79. Sullivan M. J. , Petty N. K. , Beatson S. A. . ( 2011;). Easyfig: a genome comparison visualizer. . Bioinformatics 27: 1009–1010. [CrossRef] [PubMed]
    [Google Scholar]
  80. Svenningsen S. L. , Costantino N. , Court D. L. , Adhya S. . ( 2005;). On the role of Cro in lambda prophage induction. . Proc Natl Acad Sci U S A 102: 4465–4469. [CrossRef] [PubMed]
    [Google Scholar]
  81. Tamura K. , Peterson D. , Peterson N. , Stecher G. , Nei M. , Kumar S. . ( 2011;). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28: 2731–2739. [CrossRef] [PubMed]
    [Google Scholar]
  82. Toro N. , Jiménez-Zurdo J. I. , García-Rodríguez F. M. . ( 2007;). Bacterial group II introns: not just splicing. . FEMS Microbiol Rev 31: 342–358. [CrossRef] [PubMed]
    [Google Scholar]
  83. Weinbauer M. G. . ( 2004;). Ecology of prokaryotic viruses. . FEMS Microbiol Rev 28: 127–181. [CrossRef] [PubMed]
    [Google Scholar]
  84. Witkowski R. T. , Hattman S. , Newman L. , Clark K. , Tierney D. L. , Penner-Hahn J. , McLendon G. . ( 1995;). The zinc coordination site of the bacteriophage Mu translational activator protein, Com. . J Mol Biol 247: 753–764. [CrossRef] [PubMed]
    [Google Scholar]
  85. Wu Z. , Gumport R. I. , Gardner J. F. . ( 1998;). Defining the structural and functional roles of the carboxyl region of the bacteriophage lambda excisionase (Xis) protein. . J Mol Biol 281: 651–661. [CrossRef] [PubMed]
    [Google Scholar]
  86. Wulczyn F. G. , Bölker M. , Kahmann R. . ( 1989;). Translation of the bacteriophage Mu mom gene is positively regulated by the phage com gene product. . Cell 57: 1201–1210. [CrossRef] [PubMed]
    [Google Scholar]
  87. Zabala B. , Hammerl J. A. , Espejo R. T. , Hertwig S. . ( 2009;). The linear plasmid prophage Vp58.5 of Vibrio parahaemolyticus is closely related to the integrating phage VHML and constitutes a new incompatibility group of telomere phages. . J Virol 83: 9313–9320. [CrossRef] [PubMed]
    [Google Scholar]
  88. Zhou Y. , Liang Y. , Lynch K. H. , Dennis J. J. , Wishart D. S. . ( 2011;). PHAST: a fast phage search tool. . Nucleic Acids Res 39: W347–352. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000504
Loading
/content/journal/jgv/10.1099/jgv.0.000504
Loading

Data & Media loading...

Supplementary File 1



PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error