A sporulation factor is involved in the morphological change of Clostridium perfringens biofilms in response to temperature

Journal of Bacteriology

Volumn 196, Issue 8, 2014, Pages 1540-1550

  Obana, Nozomu ^a   Nakamura, Kouji ^a   Nomura, Nobuhiko ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ARTICLE; BACTERIUM ADHERENCE; BIOFILM; CELL ADHESION; CLOSTRIDIUM PERFRINGENS; EXTRACELLULAR MATRIX; GENE EXPRESSION; LOW TEMPERATURE; MICROBIAL MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; SPOROGENESIS; SURFACE PROPERTY; THERMOREGULATION; TRANSCRIPTION REGULATION;

BIOFILMS; CLOSTRIDIUM PERFRINGENS; GENE EXPRESSION REGULATION, BACTERIAL; TEMPERATURE; TRANSCRIPTION FACTORS;

EID: 84896473169     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01444-13     Document Type: Article

References (44)

1. Rood JI, Lyristis M. 1995. Regulation of extracellular toxin production in Clostridium perfringens. Trends Microbiol. 3:192-196. http://dx.doi.org/10.1016/S0966-842X(00)88919-2.
2. Modi N, Wilcox MH. 2001. Evidence for antibiotic induced Clostridium perfringens diarrhoea. J. Clin. Pathol. 54:748-751. http://dx.doi.org/10.1136/jcp.54.10.748.
3. Stevens DL, Aldape MJ, Bryant AE. 2012. Life-threatening clostridial infections. Anaerobe 18:254-259. http://dx.doi.org/10.1016/j.anaerobe.2011.11.001.
4. Varga JJ, Therit B, Melville SB. 2008. Type IV pili and the CcpA protein are needed for maximal biofilm formation by the gram-positive anaerobic pathogen Clostridium perfringens. Infect. Immun. 76:4944-4951. http://dx.doi.org/10.1128/IAI.00692-08.
5. Flemming H-C, Wingender J. 2010. The biofilm matrix. Nat. Rev. Microbiol. 8:623-633. http://dx.doi.org/10.1038/nrmicro2415.
6. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35:322-332. http://dx.doi.org/10.1016/j.ijantimicag.2009.12.011.
7. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. 2001. Fruiting body formation by Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 98:11621-11626. http://dx.doi.org/10.1073/pnas.191384198.
8. Hamon M, Lazazzera B. 2001. The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol. Microbiol. 42:1199-1209. http://dx.doi.org/10.1046/j.1365-2958.2001.02709.x.
9. Steiner E, Dago AE, Young DI, Heap JT, Minton NP, Hoch JA, Young M. 2011. Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum. Mol. Microbiol. 80:641-654. http://dx.doi.org/10.1111/j.1365-2958.2011.07608.x.
10. Huang I-H, Waters M, Grau RR, Sarker MR. 2004. Disruption of the gene (spo0A) encoding sporulation transcription factor blocks endospore formation and enterotoxin production in enterotoxigenic Clostridium perfringens type A. FEMS Microbiol. Lett. 233:233-240. http://dx.doi.org/10.1111/j.1574-6968.2004.tb09487.x.
11. Rosenbusch KE, Bakker D, Kuijper EJ, Smits WK. 2012. C. difficile 630δerm Spo0A regulates sporulation, but does not contribute to toxin production, by direct high-affinity binding to target DNA. PLoS One 7:e48608. http://dx.doi.org/10.1371/journal.pone.0048608.
12. Dawson LF, Valiente E, Faulds-Pain A, Donahue EH, Wren BW. 2012. Characterisation of Clostridium difficile biofilm formation, a role for Spo0A. PLoS One 7:e50527. http://dx.doi.org/10.1371/journal.pone.0050527.
13. Shimizu T, Ohtani K, Hirakawa H, Ohshima K, Yamashita A, Shiba T, Ogasawara N, Hattori M, Kuhara S, Hayashi H. 2002. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc. Natl. Acad. Sci. U. S. A. 99:996-1001. http://dx.doi.org/10.1073/pnas.022493799.
14. Obana N, Nakamura K. 2011. A novel toxin regulator, the CPE1446-CPE1447 protein heteromeric complex, controls toxin genes in Clostridium perfringens. J. Bacteriol. 193:4417-4424. http://dx.doi.org/10.1128/JB.00262-11.
15. Nariya H, Miyata S, Suzuki M, Tamai E, Okabe A. 2011. Development and application of a method for counterselectable in-frame deletion in Clostridium perfringens. Appl. Environ. Microbiol. 77:1375-1382. http://dx.doi.org/10.1128/AEM.01572-10.
16. Obana N, Nomura N, Nakamura K. 2013. Structural requirement in Clostridium perfringens collagenase mRNA 5' leader sequence for translational induction through small RNA-mRNA base pairing. J. Bacteriol. 195:2937-2946. http://dx.doi.org/10.1128/JB.00148-13.
17. Roche. 2008. DIG application manual for filter hybridization. Roche Diagnostics GmbH, Freiburg, Germany. https://www.roche-applied-science.com/wcsstore/RASCatalogAssetStore/Articles/05353149001_08.08.pdf.
18. Abe K, Obana N, Nakamura K. 2010. Effects of depletion of RNAbinding protein Tex on the expression of toxin genes in Clostridium perfringens. Biosci. Biotechnol. Biochem. 74:1564-1571. http://dx.doi.org/10.1271/bbb.100135.
19. Yawata Y, Toda K, Setoyama E, Fukuda J, Suzuki H, Uchiyama H, Nomura N. 2010. Monitoring biofilm development in a microfluidic device using modified confocal reflection microscopy. J. Biosci. Bioeng. 110:377-380. http://dx.doi.org/10.1016/j.jbiosc.2010.04.002.
20. Inaba T, Ichihara T, Yawata Y, Toyofuku M, Uchiyama H, Nomura N. 2013. Three-dimensional visualization of mixed species biofilm formation together with its substratum. Microbiol. Immunol. 57:589-593. http://dx.doi.org/10.1111/1348-0421.12064.
21. Shapiro RS, Cowen LE. 2012. Thermal control of microbial development and virulence: molecular mechanisms of microbial temperature sensing. mBio 3(5):e00238-12. http://dx.doi.org/10.1128/mBio.00238-12.
22. Konkel ME, Tilly K. 2000. Temperature-regulated expression of bacterial virulence genes. Microbes Infect. 2:157-166. http://dx.doi.org/10.1016/S1286-4579(00)00272-0.
23. Morikawa M, Kagihiro S, Haruki M, Takano K, Branda S, Kolter R, Kanaya S. 2006. Biofilm formation by a Bacillus subtilis strain that produces gamma-polyglutamate. Microbiology 152:2801-2807. http://dx.doi.org/10.1099/mic.0.29060-0.
24. Friedman L, Kolter R. 2003. Genes involved in matrix formation inPseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 51:675-690. http://dx.doi.org/10.1046/j.1365-2958.2003.03877.x.
25. Vilain S, Pretorius JM, Theron J, Brözel VS. 2009. DNA as an adhesin: Bacillus cereus requires extracellularDNAto form biofilms. Appl. Environ. Microbiol. 75:2861-2868. http://dx.doi.org/10.1128/AEM.01317-08.
26. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487. http://dx.doi.org/10.1126/science.295.5559.1487.
27. Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. 2013. Sticking together: building a biofilm the Bacillus subtilis way. Nat. Rev. Microbiol. 11:157-168. http://dx.doi.org/10.1038/nrmicro2960.
28. Hamon M, Stanley NR, Britton R, Grossman AD, Lazazzera B. 2004. Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis. Mol. Microbiol. 52:847-860. http://dx.doi.org/10.1111/j.1365-2958.2004.04023.x.
29. Katayama S, Matsushita O, Jung CM, Minami J, Okabe A. 1999. Promoter upstream bent DNA activates the transcription of the Clostridium perfringens phospholipase C gene in a low temperature-dependent manner. EMBO J. 18:3442-3450. http://dx.doi.org/10.1093/emboj/18.12.3442.
30. Jordan S, Rietkötter E, Strauch MA, Kalamorz F, Butcher BG, Helmann JD, Mascher T. 2007. LiaRS-dependent gene expression is embedded in transition state regulation in Bacillus subtilis. Microbiology 153:2530-2540. http://dx.doi.org/10.1099/mic.0.2007/006817-0.
31. Varga JJ, Nguyen V, O'Brien DK, Rodgers K, Walker R, Melville SB. 2006. Type IV pili-dependent gliding motility in the Gram-positive pathogen Clostridium perfringens and other clostridia. Mol. Microbiol. 62:680-694. http://dx.doi.org/10.1111/j.1365-2958.2006.05414.x.
32. Rodgers K, Arvidson CG, Melville S. 2011. Expression of a Clostridium perfringens type IV pilin by Neisseria gonorrhoeae mediates adherence to muscle cells. Infect. Immun. 79:3096-3105. http://dx.doi.org/10.1128/IAI.00909-10.
33. de Hoon MJL, Makita Y, Nakai K, Miyano S. 2005. Prediction of transcriptional terminators in Bacillus subtilis and related species. PLoS Comput. Biol. 1:e25. http://dx.doi.org/10.1371/journal.pcbi.0010025.
34. Dapa T, Leuzzi R, Ng YK, Baban ST, Adamo R, Kuehne SA, Scarselli M, Minton NP, Serruto D, Unnikrishnan M. 2013. Multiple factors modulate biofilm formation by the anaerobic pathogen Clostridium difficile. J. Bacteriol. 195:545-555. http://dx.doi.org/10.1128/JB.01980-12.
35. Nallapareddy S, Singh K. 2006. Endocarditis and biofilm-associated pili of Enterococcus faecalis. J. Clin. Invest. 116:2799-2807. http://dx.doi.org/10.1172/JCI29021.
36. Manetti AG, Zingaretti C, Falugi F, Capo S, Bombaci M, Bagnoli F, Gambellini G, Bensi G, Mora M, Edwards AM, Musser JM, Graviss EA, Telford JL, Grandi G, Margarit I. 2007. Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol. Microbiol. 64:968-983. http://dx.doi.org/10.1111/j.1365-2958.2007.05704.x.
37. Watnick PI, Fullner KJ, Kolter R. 1999. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 181:3606-3609.
38. Danne C, Dramsi S. 2012. Pili of gram-positive bacteria: roles in host colonization. Res. Microbiol. 163:645-658. http://dx.doi.org/10.1016/j.resmic.2012.10.012.
39. Strauch M, Webb V, Spiegelman G, Hoch JA. 1990. The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. Proc. Natl. Acad. Sci. U. S. A. 87:1801-1805. http://dx.doi.org/10.1073/pnas.87.5.1801.
40. Katayama S, Matsushita O, Tamai E, Miyata S, Okabe A. 2001. Phased A-tracts bind to the alpha subunit of RNA polymerase with increased affinity at low temperature. FEBS Lett. 509:235-238. http://dx.doi.org/10.1016/S0014-5793(01)03148-9.
41. Weiss-Muszkat M, Shakh D, Zhou Y, Pinto R, Belausov E, Chapman MR, Sela S. 2010. Biofilm formation by and multicellular behavior of Escherichia coli O55:H7, an atypical enteropathogenic strain. Appl. Environ. Microbiol. 76:1545-1554. http://dx.doi.org/10.1128/AEM.01395-09.
42. Piao Z, Sze CC, Barysheva O, Iida K, Yoshida S. 2006. Temperatureregulated formation of mycelial mat-like biofilms by Legionella pneumophila. Appl. Environ. Microbiol. 72:1613-1622. http://dx.doi.org/10.1128/AEM.72.2.1613-1622.2006.
43. Lemon KP, Freitag NE, Kolter R. 2010. The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. J. Bacteriol. 192: 3969-3976. http://dx.doi.org/10.1128/JB.00179-10.
44. Wijman JG, de Leeuw PP, Moezelaar R, Zwietering MH, Abee T. 2007. Air-liquid interface biofilms of Bacillus cereus: formation, sporulation, and dispersion. Appl. Environ. Microbiol. 73:1481-1488. http://dx.doi.org/10.1128/AEM.01781-06.