Global transcriptional response of Clostridium difficile carrying the ϕCD38-2 prophage

Applied and Environmental Microbiology

Volumn 81, Issue 4, 2015, Pages 1364-1374

  Sekulovic, Ognjen ^a   Fortier, Louis Charles ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM; CYTOLOGY; ENCODING (SYMBOLS); GENE ENCODING; METABOLISM; POLYMERASE CHAIN REACTION; PROTEINS; RNA;

CELL WALL PROTEINS; CLOSTRIDIUM DIFFICILE; DIFFERENTIALLY EXPRESSED GENE; HIGHER FREQUENCIES; HOSPITAL SETTINGS; PHOSPHOTRANSFERASE SYSTEM; TRANSCRIPTIONAL REGULATOR; TRANSCRIPTIONAL RESPONSE;

GENE EXPRESSION;

BACTERIOPHAGE; BACTERIUM; GENE EXPRESSION; GENETIC ANALYSIS; GENOME; HOSPITAL SECTOR; PROTEIN; RECOMBINATION;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM DIFFICILE;

BACTERIAL PROTEIN;

GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; LYSOGENIZATION; METABOLISM; PEPTOCLOSTRIDIUM DIFFICILE; PHYSIOLOGY; PROPHAGE; VIROLOGY;

BACTERIAL PROTEINS; CLOSTRIDIUM DIFFICILE; GENE EXPRESSION REGULATION, BACTERIAL; LYSOGENY; PROPHAGES; TRANSCRIPTION, GENETIC;

EID: 84922032068     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03656-14     Document Type: Article

References (69)

1. Brüssow H, Hendrix RW. 2002. Phage genomics: small is beautiful. Cell 108:13-16. http://dx.doi.org/10.1016/S0092-8674(01)00637-7.
2. Guttman B, Raya R, Kutter E, Kutter E, Sulakvelidze A. 2005. Basic phage biology, p 29-66. In Kutter E, Sulakvelidze A (ed), Bacteriophages: biology and applications. CRC Press, Boca Raton, FL.
3. Ravin NV. 2011. N15: the linear phage-plasmid. Plasmid 65:102-109. http://dx.doi.org/10.1016/j.plasmid.2010.12.004.
4. 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.
5. Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S. 2005. Switches in bacteriophage lambda development. Annu Rev Genet 39:409-429. http://dx.doi.org/10.1146/annurev.genet.39.073003.113656.
6. Ventura M, Canchaya C, Bernini V, Altermann E, Barrangou R, McGrath S, Claesson M, Li Y, Leahy S, Walker C, Zink R, Neviani E, Steele J, Broadbent J, Klaenhammer T, Fitzgerald G, O'Toole P, van Sinderen D. 2006. Comparative genomics and transcriptional analysis of prophages identified in the genomes of Lactobacillus gasseri, Lactobacillus salivarius, and Lactobacillus casei. Appl Environ Microbiol 72:3130-3146. http://dx.doi.org/10.1128/AEM.72.5.3130-3146.2006.
7. Ventura M, Bruttin A, Canchaya C, Brussow H. 2002. Transcription analysis of Streptococcus thermophilus phages in the lysogenic state. Virology 302:21-32. http://dx.doi.org/10.1006/viro.2002.1571.
8. Ventura M, Canchaya C, Pridmore RD, Brussow H. 2004. The prophages of Lactobacillus johnsonii NCC 533: comparative genomics and transcription analysis. Virology 320:229-242. http://dx.doi.org/10.1016/j.virol.2003.11.034.
9. Ventura M, Lee J-H, Canchaya C, Zink R, Leahy S, Moreno-Munoz JA, O'Connell-Motherway M, Higgins D, Fitzgerald GF, O'Sullivan DJ, van Sinderen D. 2005. Prophage-like elements in bifidobacteria: insights from genomics, transcription, integration, distribution, and phylogenetic analysis. Appl Environ Microbiol 71:8692-8705. http://dx.doi.org/10.1128/AEM.71.12.8692-8705.2005.
10. Ventura M, Turroni F, Lima-Mendez G, Foroni E, Zomer A, Duranti S, Giubellini V, Bottacini F, Horvath P, Barrangou R, Sela DA, Mills DA, van Sinderen D. 2009. Comparative analyses of prophage-like elements present in bifidobacterial genomes. Appl Environ Microbiol 75:6929-6936. http://dx.doi.org/10.1128/AEM.01112-09.
11. Hendrix R, Lawrence J, Hatfull G, Casjens S. 2000. The origins and ongoing evolution of viruses. Trends Microbiol 8:504-508. http://dx.doi.org/10.1016/S0966-842X(00)01863-1.
12. Banks D, Beres S, Musser J. 2002. The fundamental contribution of phages to GAS evolution, genome diversification and strain emergence. Trends Microbiol 10:515-521. http://dx.doi.org/10.1016/S0966-842X(02)02461-7.
13. Brüssow H, Canchaya C, Hardt W-D. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560-602. http://dx.doi.org/10.1128/MMBR.68.3.560-602.2004.
14. Fortier L-C, Sekulovic O. 2013. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4:354-365. http://dx.doi.org/10.4161/viru.24498.
15. Barondess JJ, Beckwith J. 1990. A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature 346:871-874. http://dx.doi.org/10.1038/346871a0.
16. Barondess JJ, Beckwith J. 1995. bor gene of phage lambda, involved in serum resistance, encodes a widely conserved outer membrane lipoprotein. J Bacteriol 177:1247-1253.
17. Eklund MW, Poysky FT, Reed SM, Smith CA. 1971. Bacteriophage and the toxigenicity of Clostridium botulinum type C. Science 172:480-482.
18. Lu MJ, Stierhof YD, Henning U. 1993. Location and unusual membrane topology of the immunity protein of the Escherichia coli phage T4. J Virol 67:4905-4913.
19. Bebeacua C, Lorenzo Fajardo JC, Blangy S, Spinelli S, Bollmann S, Neve H, Cambillau C, Heller KJ. 2013. X-ray structure of a superinfection exclusion lipoprotein from phage TP-J34 and identification of the tape measure protein as its target. Mol Microbiol 89:152-165. http://dx.doi.org/10.1111/mmi.12267.
20. Labrie SJ, Samson JE, Moineau S. 2010. Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317-327. http://dx.doi.org/10.1038/nrmicro2315.
21. Wagemans J, Lavigne R. 2012. Phages and their hosts, a web of interactions- applications to drug design, p 119-133. In Hyman P, Abedon ST (ed), Bacteriophages in health and disease. CABI Press, Wallingford, United Kingdom.
22. Liu B, Shadrin A, Sheppard C, Mekler V, Xu Y, Severinov K, Matthews S, Wigneshweraraj S. 2014. The sabotage of the bacterial transcription machinery by a small bacteriophage protein. Bacteriophage 4:e28520. http://dx.doi.org/10.4161/bact.28520.
23. Roucourt B, Lavigne R. 2009. The role of interactions between phage and bacterial proteins within the infected cell: a diverse and puzzling interactome. Environ Microbiol 11:2789-2805. http://dx.doi.org/10.1111/j.1462-2920.2009.02029.x.
24. Fallico V, Ross RP, Fitzgerald GF, McAuliffe O. 2011. Genetic response to bacteriophage infection in Lactococcus lactis reveals a four-strand approach involving induction of membrane stress proteins, D-alanylation of the cell wall, maintenance of proton motive force, and energy conservation. J Virol 85:12032-12042. http://dx.doi.org/10.1128/JVI.00275-11.
25. Ainsworth S, Zomer A, Mahony J, van Sinderen D. 2013. Lytic infection of Lactococcus lactis by bacteriophages Tuc2009 and c2 triggers alternative transcriptional host responses. Appl Environ Microbiol 79:4786-4798. http://dx.doi.org/10.1128/AEM.01197-13.
26. Cenens W, Makumi A, Mebrhatu MT, Lavigne R, Aertsen A. 2013. Phage-host interactions during pseudolysogeny: lessons from the Pid/dgo interaction. Bacteriophage 3:e25029. http://dx.doi.org/10.4161/bact.25029.
27. Chen Y, Golding I, Sawai S, Guo L, Cox EC. 2005. Population fitness and the regulation of Escherichia coli genes by bacterial viruses. PLoS Biol 3:e229. http://dx.doi.org/10.1371/journal.pbio.0030229.
28. Schuch R, Fischetti VA. 2009. The secret life of the anthrax agent Bacillus anthracis: bacteriophage-mediated ecological adaptations. PLoS One 4:e6532. http://dx.doi.org/10.1371/journal.pone.0006532.
29. Barbut F, Jones G, Eckert C. 2011. Epidemiology and control of Clostridium difficile infections in healthcare settings: an update. Curr Opin Infect Dis 24:370-376. http://dx.doi.org/10.1097/QCO.0b013e32834748e5.
30. Rupnik M, Wilcox MH, Gerding DN. 2009. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 7:526-536. http://dx.doi.org/10.1038/nrmicro2164.
31. Goh S, Riley TV, Chang BJ. 2005. Isolation and characterization of temperate bacteriophages of Clostridium difficile. Appl Environ Microbiol 71:1079-1083. http://dx.doi.org/10.1128/AEM.71.2.1079-1083.2005.
32. Fortier L-C, Moineau S. 2007. Morphological and genetic diversity of temperate phages in Clostridium difficile. Appl Environ Microbiol 73:7358-7366. http://dx.doi.org/10.1128/AEM.00582-07.
33. Nale JY, Shan J, Hickenbotham PT, Fawley WN, Wilcox MH, Clokie MRJ. 2012. Diverse temperate bacteriophage carriage in Clostridium difficile 027 strains. PLoS One 7:e37263. http://dx.doi.org/10.1371/journal.pone.0037263.
34. Shan J, Patel KV, Hickenbotham PT, Nale JY, Hargreaves KR, Clokie MRJ. 2012. Prophage carriage and diversity within clinically relevant strains of Clostridium difficile. Appl Environ Microbiol 78:6027-6034. http://dx.doi.org/10.1128/AEM.01311-12.
35. Hargreaves KR, Colvin HV, Patel KV, Clokie JJP, Clokie MRJ. 2013. Genetically diverse Clostridium difficile strains harboring abundant prophages in an estuarine environment. Appl Environ Microbiol 79:6236-6243. http://dx.doi.org/10.1128/AEM.01849-13.
36. Nagy E, Foldes J. 1991. Electron microscopic investigation of lysogeny of Clostridium difficile strains isolated from antibiotic-associated diarrhea cases and from healthy carriers. APMIS 99:321-326. http://dx.doi.org/10.1111/j.1699-0463.1991.tb05156.x.
37. Govind R, Fralick J, Rolfe R. 2006. Genomic organization and molecular characterization of Clostridium difficile bacteriophage ϕCD119. J Bacteriol 188:2568-2577. http://dx.doi.org/10.1128/JB.188.7.2568-2577.2006.
38. Mayer MJ, Narbad A, Gasson MJ. 2008. Molecular characterization of a Clostridium difficile bacteriophage and its cloned biologically active endolysin. J Bacteriol 190:6734-6740. http://dx.doi.org/10.1128/JB.00686-08.
39. Sekulovic O, Meessen-Pinard M, Fortier L-C. 2011. Prophagestimulated toxin production in Clostridium difficile NAP1/027 lysogens. J Bacteriol 193:2726-2734. http://dx.doi.org/10.1128/JB.00787-10.
40. Horgan M, O'Sullivan O, Coffey Aidan Fitzgerald GF, van Sinderen D, McAuliffe O, Ross RP. 2010. Genome analysis of the Clostridium difficile phage PhiCD6356, a temperate phage of the Siphoviridae family. Gene 462:34-43. http://dx.doi.org/10.1016/j.gene.2010.04.010.
41. Hargreaves KR, Kropinski AM, Clokie MRJ. 2014. What does the talking?: quorum sensing signalling genes discovered in a bacteriophage genome. PLoS One 9:e85131. http://dx.doi.org/10.1371/journal.pone.0085131.
42. Hargreaves KR, Flores CO, Lawley TD, Clokie MRJ. 2014. Abundant and diverse clustered regularly interspaced short palindromic repeat spacers in Clostridium difficile strains and prophages target multiple phage types within this pathogen. mBio 5:e01045-13. http://dx.doi.org/10.1128/mBio.01045-13.
43. Meessen-Pinard M, Sekulovic O, Fortier L-C. 2012. Evidence of in vivo prophage induction during Clostridium difficile infection. Appl Environ Microbiol 78:7662-7670. http://dx.doi.org/10.1128/AEM.02275-12.
44. Goh S, Ong PF, Song KP, Riley TV, Chang BJ. 2007. The complete genome sequence of Clostridium difficile phage phiC2 and comparisons to phiCD119 and inducible prophages of CD630. Microbiology 153:676-685. http://dx.doi.org/10.1099/mic.0.2006/002436-0.
45. Govind R, Vediyappan G, Rolfe RD, Dupuy B, Fralick JA. 2009. Bacteriophage-mediated toxin gene regulation in Clostridium difficile. J Virol 83:12037-12045. http://dx.doi.org/10.1128/JVI.01256-09.
46. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-359. http://dx.doi.org/10.1038/nmeth.1923.
47. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079.
48. Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. 2012. Artemis: an integrated platform for visualization and analysis of highthroughput sequence-based experimental data. Bioinformatics 28:464- 469. http://dx.doi.org/10.1093/bioinformatics/btr703.
49. Anders S, Pyl PT, Huber W. 20 February 2014. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics http://dx.doi.org/10.1093/bioinformatics/btu638.
50. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11:R106. http://dx.doi.org/10.1186/gb-2010-11-10-r106.
51. Brosseau J-P, Lucier J-F, Lapointe E, Durand M, Gendron D, Gervais-Bird J, Tremblay K, Perreault J-P, Elela SA. 2010. High-throughput quantification of splicing isoforms. RNA 16:442-449. http://dx.doi.org/10.1261/rna.1877010.
52. Lingohr E, Frost S, Johnson RP. 2009. Determination of bacteriophage genome size by pulsed-field gel electrophoresis. Methods Mol Biol 502: 19-25. http://dx.doi.org/10.1007/978-1-60327-565-1_3.
53. Sambrook J, Russell D. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
54. Calabi E, Ward S, Wren B, Paxton T, Panico M, Morris H, Dell A, Dougan G, Fairweather N. 2001. Molecular characterization of the surface layer proteins from Clostridium difficile. Mol Microbiol 40:1187-1199. http://dx.doi.org/10.1046/j.1365-2958.2001.02461.x.
55. Reynolds CB, Emerson JE, La Riva de L, Fagan RP, Fairweather NF. 2011. The Clostridium difficile cell wall protein CwpV is antigenically variable between strains, but exhibits conserved aggregation-promoting function. PLoS Pathog 7:e1002024. http://dx.doi.org/10.1371/journal.ppat.1002024.
56. Heap JT, Pennington OJ, Cartman ST, Carter GP, Minton NP. 2007. The ClosTron: a universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70:452-464. http://dx.doi.org/10.1016/j.mimet.2007.05.021.
57. Stabler RA, He M, Dawson L, Martin M, Valiente E, Corton C, Lawley TD, Sebaihia M, Quail MA, Rose G, Gerding DN, Gibert M, Popoff MR, Parkhill J, Dougan G, Wren BW. 2009. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol 10:R102. http://dx.doi.org/10.1186/gb-2009-10-9-r102.
58. He M, Miyajima F, Roberts P, Ellison L, Pickard DJ, Martin MJ, Connor TR, Harris SR, Fairley D, Bamford KB, D'Arc S, Brazier J, Brown D, Coia JE, Douce G, Gerding D, Kim HJ, Koh TH, Kato H, Senoh M, Louie T, Michell S, Butt E, Peacock SJ, Brown NM, Riley T, Songer G, Wilcox M, Pirmohamed M, Kuijper E, Hawkey P, Wren BW, Dougan G, Parkhill J, Lawley TD. 2013. Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nat Genet 45:109-113. http://dx.doi.org/10.1038/ng.2478.
59. Emerson JE, Reynolds CB, Fagan RP, Shaw HA, Goulding D, Fairweather NF. 2009. A novel genetic switch controls phase variable expression of CwpV, a Clostridium difficile cell wall protein. Mol Microbiol 74: 541-556. http://dx.doi.org/10.1111/j.1365-2958.2009.06812.x.
60. Seegers JFML, McGrath S, O'Connell-Motherway M, Arendt EK, de Guchte van M, Creaven M, Fitzgerald GF, van Sinderen D. 2004. Molecular and transcriptional analysis of the temperate lactococcal bacteriophage Tuc2009. Virology 329:40-52. http://dx.doi.org/10.1016/j.virol.2004.07.003.
61. Husson-Kao C, Mengaud J, Cesselin B, van Sinderen D, Benbadis L, Chapot-Chartier MP. 2000. The Streptococcus thermophilus autolytic phenotype results from a leaky prophage. Appl Environ Microbiol 66:558-565. http://dx.doi.org/10.1128/AEM.66.2.558-565.2000.
62. Carrolo M, Frias MJ, Pinto FR, Melo-Cristino J, Ramirez M. 2010. Prophage spontaneous activation promotes DNA release enhancing biofilm formation in Streptococcus pneumoniae. PLoS One 5:e15678. http://dx.doi.org/10.1371/journal.pone.0015678.
63. Baugher JL, Durmaz E, Klaenhammer TR. 2014. Spontaneously induced prophages in Lactobacillus gasseri contribute to horizontal gene transfer. Appl Environ Microbiol 80:3508-3517. http://dx.doi.org/10.1128/AEM.04092-13.
64. Pratto F, Cicek A, Weihofen WA, Lurz R, Saenger W, Alonso JC. 2008. Streptococcus pyogenes pSM19035 requires dynamic assembly of ATPbound ParA and ParB on parS DNA during plasmid segregation. Nucleic Acids Res 36:3676-3689. http://dx.doi.org/10.1093/nar/gkn170.
65. McGrath S, Fitzgerald GF, van Sinderen D. 2002. Identification and characterization of phage-resistance genes in temperate lactococcal bacteriophages. Mol Microbiol 43:509-520. http://dx.doi.org/10.1046/j.1365-2958.2002.02763.x.
66. Sun X, Gohler A, Heller KJ, Neve H. 2006. The ltp gene of temperate Streptococcus thermophilus phage TP-J34 confers superinfection exclusion to Streptococcus thermophilus and Lactococcus lactis. Virology 350:146-157. http://dx.doi.org/10.1016/j.virol.2006.03.001.
67. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeño-Tárraga AM, Wang H, Holden MTG, Wright A, Churcher C, Quail MA, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J. 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38:779-786. http://dx.doi.org/10.1038/ng1830.
68. Soutourina OA, Monot M, Boudry P, Saujet L, Pichon C, Sismeiro O, Semenova E, Severinov K, Le Bouguenec C, Coppée J-Y, Dupuy B, Martin-Verstraete I. 2013. Genome-wide identification of regulatory RNAs in the human pathogen Clostridium difficile. PLoS Genet 9:e1003493. http://dx.doi.org/10.1371/journal.pgen.1003493.
69. Groth AC, Calos MP. 2004. Phage integrases: biology and applications. J Mol Biol 335:667-678. http://dx.doi.org/10.1016/j.jmb.2003.09.082.