Effects of actin-like proteins encoded by two Bacillus pumilus phages on unstable lysogeny, revealed by genomic analysis

Applied and Environmental Microbiology

Volumn 81, Issue 1, 2015, Pages 339-350

  Yuan, Yihui ^a   Peng, Qin ^a   Wu, Dandan ^a   Kou, Zheng ^a   Wu, Yan ^a   Liu, Pengming ^a   Gao, Meiying ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; BACTERIOPHAGES; DISEASE CONTROL; FOOD ADDITIVES; GENES; PROTEINS;

ATP-ASE ACTIVITY; BACILLUS PUMILUS; GENOMIC ANALYSIS; HIGHER FREQUENCIES; PLASMID SEGREGATION; PROTEOME ANALYSIS; PUTATIVE PROTEINS; STRUCTURAL PROTEINS;

C (PROGRAMMING LANGUAGE);

BIOASSAY; GENOME; PATHOGEN; PLASMID; PROTEIN; PROTEOMICS; RHIZOBACTERIUM; VIRUS;

BACILLUS PUMILUS; ZINGIBER OFFICINALE;

ACTIN; ADENOSINE TRIPHOSPHATASE; VIRUS PROTEIN;

BACILLUS; BACILLUS PHAGE; DNA SEQUENCE; GENETICS; GINGER; ISOLATION AND PURIFICATION; LYSOGENIZATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MYOVIRIDAE; PHYSIOLOGY; PLANT DISEASE; VIRAL PLAQUE ASSAY; VIROLOGY; VIRUS GENOME;

ACTINS; ADENOSINE TRIPHOSPHATASES; BACILLUS; BACILLUS PHAGES; GENOME, VIRAL; GINGER; LYSOGENY; MOLECULAR SEQUENCE DATA; MYOVIRIDAE; PLANT DISEASES; SEQUENCE ANALYSIS, DNA; VIRAL PLAQUE ASSAY; VIRAL PROTEINS;

EID: 84917708713     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02889-14     Document Type: Article

References (57)

1. Kim M, Ryu S. 2013. Antirepression system associated with the life cycle switch in the temperate Podoviridae phage SPC32H. J Virol 87:11775-11786. http://dx.doi.org/10.1128/JVI.02173-13.
2. Reichardt LF. 1975. Control of bacteriophage lambda-repressor synthesis: regulation of maintenance pathway by Cro and Ci products. J Mol Biol 93:289-309. http://dx.doi.org/10.1016/0022-2836(75)90133-3.
3. Sakaguchi Y, Hayashi T, Kurokawa K, Nakayama K, Oshima K, Fujinaga Y, Ohnishi M, Ohtsubo E, Hattori M, Oguma K. 2005. The genome sequence of Clostridium botulinum type C neurotoxinconverting phage and the molecular mechanisms of unstable lysogeny. Proc Natl Acad Sci U S A 102:17472-17477. http://dx.doi.org/10.1073/pnas.0505503102.
4. Oliva MA, Martin-Galiano AJ, Sakaguchi Y, Andreu JM. 2012. Tubulin homolog TubZ in a phage-encoded partition system. Proc Natl Acad Sci U S A 109:7711-7716. http://dx.doi.org/10.1073/pnas.1121546109.
5. Salje J, Gayathri P, Lowe J. 2010. The ParMRC system: molecular mechanisms of plasmid segregation by actin-like filaments. Nat Rev Microbiol 8:683-692. http://dx.doi.org/10.1038/nrmicro2425.
6. Kraemer JA, Erb ML, Waddling CA, Montabana EA, Zehr EA, Wang HN, Nguyen K, Pham DSL, Agard DA, Pogliano J. 2012. A phage tubulin assembles dynamic filaments by an atypical mechanism to center viral DNA within the host cell. Cell 149:1488-1499. http://dx.doi.org/10.1016/j.cell.2012.04.034.
7. Schumacher MA, Glover TC, Brzoska AJ, Jensen SO, Dunham TD, Skurray RA, Firth N. 2007. Segrosome structure revealed by a complex of ParR with centromere DNA. Nature 450:1268-U1215. http://dx.doi.org/10.1038/nature06392.
8. Fritze D. 2004. Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 94:1245-1248. http://dx.doi.org/10.1094/PHYTO.2004.94.11.1245.
9. Myresiotis CK, Karaoglanidis GS, Vryzas Z, Papadopoulou-Mourkidou E. 2012. Evaluation of plant-growth-promoting rhizobacteria, acibenzolar-S-methyl and hymexazol for integrated control of Fusarium crown and root rot on tomato. Pest Manag Sci 68:404-411. http://dx.doi.org/10.1002/ps.2277.
10. Logan NA. 2012. Bacillus and relatives in food-borne illness. J Appl Microbiol 112:417-429. http://dx.doi.org/10.1111/j.1365-2672.2011.05204.x.
11. Kimouli M, Vrioni G, Papadopoulou M, Koumaki V, Petropoulou D, Gounaris A, Friedrich AW, Tsakris A. 2012. Two cases of severe sepsis caused by Bacillus pumilus in neonatal infants. J Med Microbiol 61:596-599. http://dx.doi.org/10.1099/jmm.0.033175-0.
12. Galal AA, El-Bana AA, Janse J. 2006. Bacillus pumilus, a new pathogen on mango plants. Egypt J Phytopathol 34:17-29.
13. Li B, Qiu W, Tan Q, Su T, Fang Y, Xie G. 2009. Association of a Bacillus species with leaf and twig dieback of Asian pear (Pyrus pyrifolia) in China. J Plant Pathol 91:705-708.
14. Peng Q, Yuan Y, Gao M. 2013. Bacillus pumilus, a novel ginger rhizome rot pathogen in China. Plant Dis 97:1308-1315. http://dx.doi.org/10.1094/PDIS-12-12-1178-RE.
15. Bramucci MG, Keggins KM, Lovett PS. 1977. Bacteriophage conversion of spore-negative mutants to spore-positive in Bacillus pumilus. J Virol 22:194-202.
16. Barylski J, Nowicki G, Gozdzicka-Jozefiak A. 2014. The discovery of ϕAGATE, a novel phage infecting Bacillus pumilus, leads to new insights into the phylogeny of the subfamily Spounavirinae. PLoS One 9:e86632. http://dx.doi.org/10.1371/journal.pone.0086632.
17. Lorenz L, Lins B, Barrett J, Montgomery A, Trapani S, Schindler A, Christie GE, Cresawn SG, Temple L. 2013. Genomic characterization of six novel Bacillus pumilus bacteriophages. Virology 444:374-383. http://dx.doi.org/10.1016/j.virol.2013.07.004.
18. Mageeney C, Pope WH, Harrison M, Moran D, Cross T, Jacobs-Sera D, Hendrix RW, Dunbar D, Hatfull GF. 2012. Mycobacteriophage Marvin: a new singleton phage with an unusual genome organization. J Virol 86: 4762-4775. http://dx.doi.org/10.1128/JVI.00075-12.
19. Yuan YH, Gao MY, Wu DD, Liu PM, Wu Y. 2012. Genome characteristics of a novel phage from Bacillus thuringiensis showing high similarity with phage from Bacillus cereus. PLoS One 7:e37557. http://dx.doi.org/10.1371/journal.pone.0037557.
20. Thomas JA, Hardies SC, Rolando M, Hayes SJ, Lieman K, Carroll CA, Weintraub ST, Serwer P. 2007. Complete genomic sequence and mass spectrometric analysis of highly diverse, atypical Bacillus thuringiensis phage 0305 phi 8-36. Virology 368:405-421. http://dx.doi.org/10.1016/j.virol.2007.06.043.
21. Lynch KH, Stothard P, Dennis JJ. 2010. Genomic analysis and relatedness of P2-like phages of the Burkholderia cepacia complex. BMC Genomics 11:599. http://dx.doi.org/10.1186/1471-2164-11-599.
22. Catalao MJ, Gil F, Moniz-Pereira J, Pimentel M. 2010. The mycobacteriophage Ms6 encodes a chaperone-like protein involved in the endolysin delivery to the peptidoglycan. Mol Microbiol 77:672-686. http://dx.doi.org/10.1111/j.1365-2958.2010.07239.x.
23. Garcia P, Martinez B, Obeso JM, Lavigne R, Lurz R, Rodriguez A. 2009. Functional genomic analysis of two Staphylococcus aureus phages isolated from the dairy environment. Appl Environ Microbiol 75:7663-7673. http://dx.doi.org/10.1128/AEM.01864-09.
24. Marchler-Bauer A, Zheng CJ, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu SN, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang DC, Bryant SH. 2013. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41:D348-D352. http://dx.doi.org/10.1093/nar/gks1243.
25. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD. 2012. The Pfam protein families database. Nucleic Acids Res 40:D290-D301. http://dx.doi.org/10.1093/nar/gkr1065.
26. Soding J. 2005. Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951-960. http://dx.doi.org/10.1093/bioinformatics/bti125.
27. Stothard P, Wishart DS. 2005. Circular genome visualization and exploration using CGView. Bioinformatics 21:537-539. http://dx.doi.org/10.1093/bioinformatics/bti054.
28. Tatusov RL, Koonin EV, Lipman DJ. 1997. A genomic perspective on protein families. Science 278:631-637. http://dx.doi.org/10.1126/science.278.5338.631.
29. Schattner P, Brooks AN, Lowe TM. 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686-W689. http://dx.doi.org/10.1093/nar/gki366.
30. Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573-580. http://dx.doi.org/10.1093/nar/27.2.573.
31. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. 2006. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34:D32-D36. http://dx.doi.org/10.1093/nar/gkj014.
32. Krumsiek J, Arnold R, Rattei T. 2007. Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23:1026-1028. http://dx.doi.org/10.1093/bioinformatics/btm039.
33. Darling ACE, Mau B, Blattner FR, Perna NT. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394-1403. http://dx.doi.org/10.1101/gr.2289704.
34. Zafar N, Mazumder R, Seto D. 2002. CoreGenes: a computational tool for identifying and cataloging 'core' genes in a set of small genomes. BMC Bioinformatics 3:12. http://dx.doi.org/10.1186/1471-2105-3-12.
35. 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. http://dx.doi.org/10.1093/molbev/msr121.
36. Gao MY, Li RS, Dai SY, Wu Y, Yi D. 2008. Diversity of Bacillus thuringiensis strains from soil in China and their pesticidal activities. Biol Control 44:380-388. http://dx.doi.org/10.1016/j.biocontrol.2007.11.011.
37. Sambrook JFE, Maniatis T. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Popp D, Xu WJ, Narita A, Brzoska AJ, Skurray RA, Firth N, Goshdastider U, Maeda Y, Robinson RC, Schumacher MA. 2010. Structure and filament dynamics of the pSK41 actin-like ParM protein implications for plasmid DNA segregation. J Biol Chem 285:10130-10140. http://dx.doi.org/10.1074/jbc.M109.071613.
39. Hara F, Yamashiro K, Nemoto N, Ohta Y, Yokobori SI, Yasunaga T, Hisanaga SI, Yamagishi A. 2007. An actin homolog of the archaeon Thermoplasma acidophilum that retains the ancient characteristics of eukaryotic actin. J Bacteriol 189:2039-2045. http://dx.doi.org/10.1128/JB.01454-06.
40. Lindner P, Bauer K, Kremmer E, Krebber C, Honegger A, Klinger B, Mocikat R, Pluckthun A. 1997. Specific detection of his-tagged proteins with recombinant anti-His tag scFv-phosphatase or scFv-phage fusions. Biotechniques 22:140-149.
41. Moak M, Molineux IJ. 2004. Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169-1183. http://dx.doi.org/10.1046/j.1365-2958.2003.03894.x.
42. Lavigne R, Noben JP, Hertveldt K, Ceyssens PJ, Briers Y, Dumont D, Roucourt B, Krylov VN, Mesyanzhinov VV, Robben J, Volckaert G. 2006. The structural proteome of Pseudomonas aeruginosa bacteriophage phi KMV. Microbiology 152:529-534. http://dx.doi.org/10.1099/mic.0.28431-0.
43. Siew N, Azaria Y, Fischer D. 2004. The ORFanage: an ORFan database. Nucleic Acids Res 32:D281-D283. http://dx.doi.org/10.1093/nar/gkh116.
44. Handtke S, Schroeter R, Jurgen B, Methling K, Schluter R, Albrecht D, van Hijum SAFT, Bongaerts J, Maurer KH, Lalk M, Schweder T, Hecker M, Voigt B. 2014. Bacillus pumilus reveals a remarkably high resistance to hydrogen peroxide provoked oxidative stress. PLoS One 9:e85625. http://dx.doi.org/10.1371/journal.pone.0085625.
45. Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B. 2010. Ahierarchical classification of polysaccharide lyases for glycogenomics. Biochem J 432:437-444. http://dx.doi.org/10.1042/BJ20101185.
46. Thompson JE, Pourhossein M, Waterhouse A, Hudson T, Goldrick M, Derrick JP, Roberts IS. 2010. The K5 lyase KflA combines a viral tail spike structure with a bacterial polysaccharide lyase mechanism. J Biol Chem 285:23963-23969. http://dx.doi.org/10.1074/jbc.M110.127571.
47. Catalao MJ, Gil F, Moniz-Pereira J, Sao-Jose C, Pimentel M. 2013. Diversity in bacterial lysis systems: bacteriophages show the way. FEMS Microbiol Rev 37:554-571. http://dx.doi.org/10.1111/1574-6976.12006.
48. Vandersteegen K, Kropinski AM, Nash JHE, Noben JP, Hermans K, Lavigne R. 2013. Romulus and Remus, two phage isolates representing a distinct clade within the Twortlikevirus genus, display suitable properties for phage therapy applications. J Virol 87:3237-3247. http://dx.doi.org/10.1128/JVI.02763-12.
49. Fujimoto Z, Kimura K. 2012. Crystal structure of bacteriophage Phi NIT1 zinc peptidase PghP that hydrolyzes gamma-glutamyl linkage of bacterial poly-gamma-glutamate. Proteins 80:722-732. http://dx.doi.org/10.1002/prot.23229.
50. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM. 2005. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 29:231-262. http://dx.doi.org/10.1016/j.femsre.2004.12.008.
51. Ebersbach G, Gerdes K. 2005. Plasmid segregation mechanisms. Annu Rev Genet 39:453-479. http://dx.doi.org/10.1146/annurev.genet.38.072902.091252.
52. Kristensen DM, Cai XX, Mushegian A. 2011. Evolutionarily conserved orthologous families in phages are relatively rare in their prokaryotic hosts. J Bacteriol 193:1806-1814. http://dx.doi.org/10.1128/JB.01311-10.
53. Stella EJ, Franceschelli JJ, Tasselli SE, Morbidoni HR. 2013. Analysis of novel mycobacteriophages indicates the existence of different strategies for phage inheritance in mycobacteria. PLoS One 8:e56384. http://dx.doi.org/10.1371/journal.pone.0056384.
54. Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R. 2013. Expanding the marine virosphere using metagenomics. PLoS Genet. 9:e1003987. http://dx.doi.org/10.1371/journal.pgen.1003987.
55. Lee JH, Shin H, Son B, Ryu S. 2012. Complete genome sequence of Bacillus cereus bacteriophage BCP78. J Virol 86:637-638. http://dx.doi.org/10.1128/JVI.06520-11.
56. Bandara N, Jo J, Ryu S, Kim KP. 2012. Bacteriophages BCP1-1 and BCP8-2 require divalent cations for efficient control of Bacillus cereus in fermented foods. Food Microbiol 31:9-16. http://dx.doi.org/10.1016/j.fm.2012.02.003.
57. Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H. 2005. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci U S A 102:16919-16926. http://dx.doi.org/10.1073/pnas.0507029102.