Association of a D-Alanyl-D-Alanine Carboxypeptidase Gene with the Formation of Aberrantly Shaped Cells during the Induction of Viable but Nonculturable Vibrio parahaemolyticus

Applied and Environmental Microbiology

Volumn 79, Issue 23, 2013, Pages 7305-7312

  Hung, Wei Cheng ^a   Jane, Wann Neng ^b   Wong, Hin Chung ^a  

^a SOOCHOW UNIVERSITY   (Taiwan)

^b INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE; CELL WALL SYNTHESIS; CEPHALOSPORIN C; CONTROL MEDIUMS; GRAM-NEGATIVE BACTERIA; V. PARAHAEMOLYTICUS; VIABLE BUT NON-CULTURABLE; VIBRIO PARAHAEMOLYTICUS;

AMINO ACIDS; ANTIBIOTICS; BACTERIA; CYTOLOGY; GENE EXPRESSION;

CELLS;

ANTIBIOTICS; BACTERIUM; CELL ORGANELLE; ENZYME ACTIVITY; GENE EXPRESSION; MUTATION; SALT; SODIUM CHLORIDE;

CARBOXYPEPTIDASE TRANSPEPTIDASE; CEPHALOSPORIN C; CEPHALOSPORIN DERIVATIVE; CYCLOSERINE;

ARTICLE; CELL WALL; CHEMISTRY; COLD; CULTURE MEDIUM; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY; VIBRIO PARAHAEMOLYTICUS;

CELL WALL; CEPHALOSPORINS; COLD TEMPERATURE; CULTURE MEDIA; CYCLOSERINE; GENE EXPRESSION PROFILING; MICROBIAL VIABILITY; SERINE-TYPE D-ALA-D-ALA CARBOXYPEPTIDASE; VIBRIO PARAHAEMOLYTICUS;

EID: 84888262581     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01723-13     Document Type: Article

References (48)

1. Food and Agriculture Organization of the United Nations and World Health Organization (FAO/WHO). 2011. Risk assessment of Vibrio parahaemolyticus in seafood: interpretative summary and technical report. Microbiological Risk Assessment Series no. 16. FAO/WHO, Rome Italy.
2. Pan T-M, Wang TK, Lee C-L, Chien S-W, Horng C-B. 1997. Foodborne disease outbreaks due to bacteria in Taiwan, 1986 to 1995. J. Clin. Microbiol. 35:1260-1262.
3. Nair GB, Ramamurthy T, Bhattacharya SK, Dutta B, Takeda Y, Sack DA. 2007. Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin. Microbiol. Rev. 20:39-48.
4. Du M, Chen J, Zhang X, Li A, Li Y. 2007. Characterization and resuscitation of viable but nonculturable Vibrio alginolyticus VIB283. Arch. Microbiol. 188:283-288.
5. Kondo K, Takade A, Amako K. 1994. Morphology of the viable but nonculturable Vibrio cholerae as determined by the freeze fixation technique. FEMS Microbiol. Lett. 123:179-184.
6. Colwell RR. 2000. Viable but nonculturable bacteria: a survival strategy. J. Infect. Chemother. 6:121-125.
7. Wong HC, Wang P, Chen SY, Chiu SW. 2004. Resuscitation of viable but non-culturable Vibrio parahaemolyticus in a minimum salt medium. FEMS Microbiol. Lett. 233:269-275.
8. Bates TC, Oliver JD. 2004. The viable but nonculturable state of Kanagawa positive and negative strains of Vibrio parahaemolyticus. J. Microbiol. 42:74-79.
9. Jiang XP, Chai TJ. 1996. Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Appl. Environ. Microbiol. 62:1300-1305.
10. Wong HC, Wang P. 2004. Induction of viable but non-culturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J. Appl. Microbiol. 96:359-366.
11. Wong HC, Shen CT, Chang CN, Lee YS, Oliver JD. 2004. Biochemical and virulence characterization of viable but nonculturable cells of Vibrio parahaemolyticus. J. Food Prot. 67:2430-2435.
12. Oliver JD. 2010. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev. 34:415-425.
13. Rahman I, Shahamat M, Chowdhury MA, Colwell RR. 1996. Potential virulence of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 62:115-120.
14. Su CP, Jane WN, Wong HC. 2013. Changes of ultrastructure and stress tolerance of Vibrio parahaemolyticus upon entering viable but nonculturable state. Int. J. Food Microbiol. 160:360-366.
15. Chen SY, Jane WN, Chen YS, Wong HC. 2009. Morphological changes of Vibrio parahaemolyticus under cold and starvation stresses. Int. J. Food Microbiol. 129:157-165.
16. Daniel RA, Errington J. 2003. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767-776.
17. Divakaruni AV, Baida C, White CL, Gober JW. 2007. The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. Mol. Microbiol. 66:174-188.
18. Nelson DE, Ghosh AS, Paulson AL, Young KD. 2002. Contribution of membrane-binding and enzymatic domains of penicillin binding protein 5 to maintenance of uniform cellular morphology of Escherichia coli. J. Bacteriol. 184:3630-3639.
19. Nelson DE, Young KD. 2000. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J. Bacteriol. 182: 1714-1721.
20. Nelson DE, Young KD. 2001. Contributions of PBP 5 and DDcarboxypeptidase penicillin binding proteins to maintenance of cell shape in Escherichia coli. J. Bacteriol. 183:3055-3064.
21. Nanninga N. 1998. Morphogenesis of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:110-129.
22. Dul MJ, McDonald WC. 1971. Morphological changes and antibioticinduced thermal resistance in vegetative cells of Bacillus subtilis. J. Bacteriol. 106:672-678.
23. Gullbrand B, Akerlund T, Nordstrom K. 1999. On the origin of branches in Escherichia coli. J. Bacteriol. 181:6607-6614.
24. Huang KC, Mukhopadhyay R, Wen B, Gitai Z, Wingreen NS. 2008. Cell shape and cell-wall organization in Gram-negative bacteria. Proc. Natl. Acad. Sci. U. S. A. 105:19282-19287.
25. Korat B, Mottl H, Keck W. 1991. Penicillin-binding protein 4 of Escherichia coli: molecular cloning of the dacB gene, controlled overexpression, and alterations in murein composition. Mol. Microbiol. 5:675-684.
26. Wang HW, Chung CH, Ma TY, Wong HC. 2013. Roles of alkyl hydroperoxide reductase subunit C (AhpC) in viable but nonculturable Vibrio parahaemolyticus. Appl. Environ. Microbiol. 79:3734-3743.
27. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, Iijima Y, Najima M, Nakano M, Yamashita A, Kubota Y, Kimura S, Yasunaga T, Honda T, Shinagawa H, Hattori M, Iida T. 2003. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361:743-749.
28. Vattakaven T, Bond P, Bradley G, Munn CB. 2006. Differential effects of temperature and starvation on induction of the viable-but-nonculturable state in the coral pathogens Vibrio shiloi and Vibrio tasmaniensis. Appl. Environ. Microbiol. 72:6508-6513.
29. Chaiyanan S, Chaiyanan S, Grim C, Maugel T, Huq A, Colwell RR. 2007. Ultrastructure of coccoid viable but non-culturable Vibrio cholerae. Environ. Microbiol. 9:393-402.
30. Henderson TA, Young KD, Denome SA, Elf PK. 1997. AmpC and AmpH, proteins related to the class C beta-lactamases, bind penicillin and contribute to the normal morphology of Escherichia coli. J. Bacteriol. 179: 6112-6121.
31. Pang H, Winkler HH. 1994. Analysis of the peptidoglycan of Rickettsia prowazekii. J. Bacteriol. 176:923-926.
32. Thomashow MF, Rittenberg SC. 1978. Penicillin-induced formation of osmotically stable spheroplasts in nongrowing Bdellovibrio bacteriovorus. J. Bacteriol. 133:1484-1491.
33. Chiu SW, Chen SY, Wong HC. 2008. Localization and expression of MreB in Vibrio parahaemolyticus under different stresses. Appl. Environ. Microbiol. 74:7016-7022.
34. Signoretto C, del Mar LM, TafiMC, Canepari P. 2000. Cell wall chemical composition of Enterococcus faecalis in the viable but nonculturable state. Appl. Environ. Microbiol. 66:1953-1959.
35. Jiang H, Si F, Margolin W, Sun SX. 2011. Mechanical control of bacterial cell shape. Biophys. J. 101:327-335.
36. Jiang H, Sun SX. 2010. Morphology, growth, and size limit of bacterial cells. Phys. Rev. Lett. 105:028101. doi:10.1103/PhysRevLett.105.028101.
37. Huang CY, Shih HW, Lin LY, Tien YW, Cheng TJ, Cheng WC, Wong CH, Ma C. 2012. Crystal structure of Staphylococcus aureus transglycosylase in complex with a lipid II analog and elucidation of peptidoglycan synthesis mechanism. Proc. Natl. Acad. Sci. U. S. A. 109:6496-6501.
38. Suvorov M, Lee M, Hesek D, Boggess B, Mobashery S. 2008. Lytic transglycosylase MltB of Escherichia coli and its role in recycling of peptidoglycan strands of bacterial cell wall. J. Am. Chem. Soc. 130:11878-11879.
39. Ikeda M, Wachi M, Jung HK, Ishino F, Matsuhashi M. 1991. The Esche-richia colimraYgene encodingUDP-N-acetylmuramoyl-pentapeptide: undecaprenyl- phosphate phospho-N-acetylmuramoyl-pentapeptide transferase. J. Bacteriol. 173:1021-1026.
40. Marcyjaniak M, Odintsov SG, Sabala I, Bochtler M. 2004. Peptidoglycan amidase MepA is a LAS metallopeptidase. J. Biol. Chem. 279:43982-43989.
41. Wanke C, Falchetto R, Amrhein N. 1992. The UDP-N-acetylglucosamine 1-carboxyvinyl-transferase of Enterobacter cloacae. Molecular cloning, sequencing of the gene and overexpression of the enzyme. FEBS Lett. 301:271-276.
42. Yang L, Zhou D, Liu X, Han H, Zhan L, Guo Z, Zhang L, Qin C, Wong HC, Yang R. 2009. Cold-induced gene expression profiles of Vibrio parahaemolyticus: a time-course analysis. FEMS Microbiol. Lett. 291:50-58.
43. Asakura H, Ishiwa A, Arakawa E, Makino S, Okada Y, Yamamoto S, Igimi S. 2007. Gene expression profile of Vibrio cholerae in the cold stressinduced viable but non-culturable state. Environ. Microbiol. 9:869-879.
44. Martin HH, Maskos C, Burger R. 1975. D-Alanyl-D-alanine carboxypeptidase in the bacterial form and L-form of Proteus mirabilis. Eur. J. Biochem. 55:465-473.
45. Chiu SW, Chen SY, Wong HC. 2008. Dynamic localization of MreB in Vibrio parahaemolyticus and in ectopic host Escherichia coli. Appl. Environ. Microbiol. 74:6739-6745.
46. Simon R, Priefer U, Pühler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat. Biotechnol. 1:784-791.
47. Philippe N, Alcaraz JP, Coursange E, Geiselmann J, Schneider D. 2004. Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 51:246-255.
48. Heath LS, Heath HE, LeBlanc PA, Smithberg SR, Dufour M, Simmonds RS, Sloan GL. 2004. The streptococcolytic enzyme zoocin A is a penicillinbinding protein. FEMS Microbiol. Lett. 236:205-211.