Gene expression profiles of Vibrio parahaemolyticus in viable but non-culturable state

FEMS Microbiology Ecology

Volumn 91, Issue 5, 2015, Pages

  Meng, Lu ^a   Alter, Thomas ^a   Aho, Tommi ^b   Huehn, Stephan ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

Early stationary phase; Exponential phase; Microarray; VBNC; Viable but not culturable state; Vibrio parahaemolyticus; Whole genome gene expression

Indexed keywords

ARRAY; ASEXUAL REPRODUCTION; BACTERIUM; GENE EXPRESSION; GENOME; GROWTH RATE; METABOLISM; MICROBIAL ECOLOGY; NUCLEIC ACID; SURVIVAL;

VIBRIO PARAHAEMOLYTICUS; VIBRIO VULNIFICUS;

AMINO ACID; TRANSCRIPTOME;

BACTERIAL GENOME; BIOSYNTHESIS; DNA MICROARRAY; DOWN REGULATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIAL VIABILITY; MICROBIOLOGY; UPREGULATION; VIBRIO PARAHAEMOLYTICUS; VIBRIOSIS;

AMINO ACIDS; DOWN-REGULATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HUMANS; MICROBIAL VIABILITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTOME; UP-REGULATION; VIBRIO INFECTIONS; VIBRIO PARAHAEMOLYTICUS;

EID: 84939289428     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiv035     Document Type: Article

References (85)

1. Abella M, Erill I, Jara M, et al. Widespread distribution of a lexAregulated DNA damage-inducible multiple gene cassette in the Proteobacteria phylum. Mol Microbiol 2004;54:212-22.
2. Asakura H, Ishiwa A, Arakawa E, et al. Gene expression profile of Vibrio cholerae in the cold stress-induced viable but nonculturable state. Environ Microbiol 2007;9:869-79.
3. Bansal T, Englert D, Lee J, et al. Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157: H7 chemotaxis, colonization, and gene expression. Infect Immun 2007;75:4597-607.
4. Bolstad BM, Irizarry RA, Astrand M, et al. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003;19:185- 93.
5. Campoy S, Salvador N, Cortes P, et al. Expression of canonical SOS genes is not under LexA repression in Bdellovibrio bacteriovorus. J Bacteriol 2005;187:5367-75.
6. Chaiyanan S, Huq A, Maugel T, et al. Viability of the nonculturable Vibrio cholerae O1 and O139. Syst Appl Microbiol 2001;24:331-41.
7. Chen SY, Jane WN, Chen YS, et al. Morphological changes of Vibrio parahaemolyticus under cold and starvation stresses. Int J Food Microbiol 2009;129:157-65.
8. Chilcott GS, Hughes KT. Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli. Microbiol Mol Biol R 2000;64:694-708.
9. Collyn F, Lety MA, Nair S, et al. Yersinia pseudotuberculosis harbors a type IV pilus gene cluster that contributes to pathogenicity. Infect Immun 2002;70:6196-205.
10. Colwell RR. Viable but nonculturable bacteria: a survival strategy. J Infect Chemother 2000;6:121-5.
11. Colwell RR, Brayton P, Herrington D, et al. Viable but non culturable Vibrio cholerae O1 revert to a cultivable state in the human intestine. World J Microb Biot 1996;12:28-31.
12. Coutard F, Pommepuy M, Loaec S, et al. mRNA detection by reverse transcription-PCR for monitoring viability and potential virulence in a pathogenic strain of Vibrio parahaemolyticus in viable but nonculturable state. J Appl Microbiol 2005;98:951-61.
13. daRocha RP, Paquola AC, Marques Mdo V, et al. Characterization of the SOS regulon of Caulobacter crescentus. J Bacteriol 2008;190:1209-18.
14. Datta PP, Bhadra RK. Cold shock response and major cold shock proteins of Vibrio cholerae. Appl Environ Microb 2003;69:6361-9.
15. Erill I, Campoy S, Mazon G, et al. Dispersal and regulation of an adaptive mutagenesis cassette in the bacteria domain. Nucleic Acids Res 2006;34:66-77.
16. Fakruddin M, Mannan KSB, Andrews S. Viable but nonculturable bacteria: food safety and public health perspective. 2013;2013:703813.
17. FAO/WHO. Risk assessment of Vibrio parahaemolyticus in seafood: interpretative summary and technical report. Microbiological Risk Assessment Series No.16. Rome 2011.
18. Fasold M, Binder H. Variation of RNA quality and quantity are major sources of batch effects in microarray expression data. Microarrays 2014;3:322-39.
19. Fischer-Le Saux M, Hervio-Heath D, Loaec S, et al. Detection of cytotoxin-hemolysin mRNA in nonculturable populations of environmental and clinical Vibrio vulnificus strains in artificial seawater. Appl Environ Microb 2002;68:5641-6.
20. Foster PL. Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol 2007;42:373-97.
21. Fujino T, Okuno Y, Nakada D, et al. On the bacteriological examination of shirasu food poisoning. Med J Osaka Univ 1953;4:299-304.
22. Gonzalez-Escalona N, Fey A, Hofle MG, et al. Quantitative reverse transcription polymerase chain reaction analysis of Vibrio cholerae cells entering the viable but non-culturable state and starvation in response to cold shock. Environ Microbiol 2006;8:658-66.
23. Gonzalez-Escalona N, Martinez-Urtaza J, Romero J, et al. Determination of molecular phylogenetics of Vibrio parahaemolyticus strains bymultilocus sequence typing. J Bacteriol 2008;190:2831-40.
24. Gopal S, Otta SK, Kumar S, et al. The occurrence of Vibrio species in tropical shrimp culture environments; implications for food safety. Int J Food Microbiol 2005;102:151-9.
25. Guerry P. Campylobacter flagella: not just for motility. Trends Microbiol 2007;15:456-61.
26. Heim S, Lleo M, Bonato B, et al. The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J Bacteriol 2002;184:6739-45.
27. Hu M, Zhang C, Mu Y, et al. Indole affects biofilm formation in bacteria. Indian J Microbiol 2010;50:362-8.
28. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009a;37:1-13.
29. Huang daW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009b;4:44-57.
30. Kong RY, Lee SK, Law TW, et al. Rapid detection of six types of bacterial pathogens in marine waters by multiplex PCR. Water Res 2002;36:2802-12.
31. Lahtinen SJ, Ahokoski H, Reinikainen JP, et al. Degradation of 16S rRNA and attributes of viability of viable but nonculturable probiotic bacteria. Lett Appl Microbiol 2008;46:693-8.
32. Lai CJ, Chen SY, Lin IH, et al. Change of protein profiles in the induction of the viable but nonculturable state of Vibrio parahaemolyticus. Int J Food Microbiol 2009;135:118-24.
33. Lee J, Bansal T, Jayaraman A, et al. Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl Environ Microb 2007;73:4100-9.
34. Lee JH, Lee J. Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 2010;34:426-44.
35. Lee JH, Kim YG, Kim CJ, et al. Indole-3-acetaldehyde from Rhodococcus sp. BFI 332 inhibits Escherichia coli O157: H7 biofilm formation. Appl Microbiol Biot 2012;96:1071-8.
36. Li L, Mendis N, Trigui H, et al. The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol 2014;5:1-20.
37. Limthammahisorn S, Brady YJ, Arias CR. In vivo gene expression of cold shock and other stress-related genes in Vibrio vulnificus during shellstock temperature control conditions in oysters. J Appl Microbiol 2009;106:642-50.
38. Little JW. Mechanism of specific LexA cleavage: autodigestion and the role of RecA coprotease. Biochimie 1991;73:411-21.
39. Little JW, Mount DW. The SOS regulatory system of Escherichia coli. Cell 1982;29:11-22.
40. Lleo MM, Bonato B, Tafi MC, et al. Resuscitation rate in different enterococcal species in the viable but non-culturable state. J Appl Microbiol 2001;91:1095-102.
41. McLaughlin JB, DePaola A, Bopp CA, et al. Outbreak of Vibrio parahaemolyticus gastroenteritis associated with Alaskan oysters. New Engl J Med 2005;353:1463-70.
42. Makino K, Oshima K, Kurokawa K, et al. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 2003;361:743-9.
43. Mazon G, Campoy S, Erill I, et al. Identification of the Acidobacterium capsulatum LexA box reveals a lateral acquisition of the Alphaproteobacteria lexA gene. Microbiology 2006;152:1109- 18.
44. Meibom KL, Li XB, Nielsen AT, et al. The Vibrio cholerae chitin utilization program. P Natl Acad Sci USA 2004;101:2524-9.
45. Mishra A, Taneja N, Sharma M. Viability kinetics, induction, resuscitation and quantitative real-time polymerase chain reaction analyses of viable but nonculturable Vibrio cholerae O1 in freshwater microcosm. J Appl Microbiol 2012;112:945- 53.
46. Montanchez I, Arana I, Parada C, et al. Reprogramming of Vibrio harveyi gene expression during adaptation in cold seawater. FEMS Microbiol Ecol 2014;87:193-203.
47. Morey JS, Ryan JC, Van Dolah FM. Microarray validation: factors influencing correlation between oligonucleotidemicroarrays and real-time PCR. Biol Proced Online 2006;8:175-93.
48. Nasu H, Iida T, Sugahara T, et al. A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3: K6 strains. J Clin Microbiol 2000;38:2156-61.
49. NicolòMS, Guglielmino SPP. Viable but nonculturable bacteria in food. In: Maddock J (ed). Public Health-Methodology, Environmental and Systems Issues. Rijeka: INTECH Open Access Publisher, 2012, 189-216.
50. O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol 2000;54:49-79.
51. Oliver JD. Problems in detecting dormant (VBNC) cells, and the role of DNA elements in this response. In: Jansson JK, van Elsas JD, Bailey M (eds). Tracking Genetically-Engineered Microorganisms. Texas: Landes Bioscience, 2000, 1-15.
52. Oliver JD. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 2010;34:415-25.
53. Ongagna-Yhombi SY, Boyd EF. Biosynthesis of the osmoprotectant ectoine, but not glycine betaine, is critical for survival of osmotically stressed Vibrio parahaemolyticus cells. Appl Environ Microb 2013;79:5038-49.
54. Pahel G, Zelenetz AD, Tyler BM. gltB gene and regulation of nitrogen metabolism by glutamine synthetase in Escherichia coli. J Bacteriol 1978;133:139-48.
55. Paranjpye RN, Strom MS. A Vibrio vulnificus type IV pilin contributes to biofilm formation, adherence to epithelial cells, and virulence. Infect Immun 2005;73:1411-22.
56. Pasquaroli S, Zandri G, Vignaroli C, et al. Antibiotic pressure can induce the viable but non-culturable state in Staphylococcus aureus growing in biofilms. J Antimicrob Chemoth 2013;68:1812-7.
57. Postgate JR, Hunter JR. The survival of starved bacteria. J Gen Microbiol 1962;29:233-63.
58. Radman M. Phenomenology of an inducible mutagenic DNA repair pathway in Escherichia coli: SOS repair hypothesis. In: Prakash L (ed). Molecular and Environmental Aspects of Mutagenesis. New York: Charles C Thomas Publisher, 1974, 128-42.
59. Raman T, O'Connor TP, Hackett NR, et al. Quality control in microarray assessment of gene expression in human airway epithelium. BMC Genomics 2009;10:493.
60. Sanchez-Alberola N, Campoy S, Barbe J, et al. Analysis of the SOS response of Vibrio and other bacteria with multiple chromosomes. BMC Genomics 2012;13:58.
61. Schroeder A,Mueller O, Stocker S, et al. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 2006;7:3.
62. Shime-Hattori A, Iida T, Arita M, et al. Two type IV pili of Vibrio parahaemolyticus play different roles in biofilm formation. FEMS Microbiol Lett 2006;264:89-97.
63. Slayton RB, Newton AE, Depaola A, et al. Clam-associated vibriosis, USA, 1988-2010. Epidemiol Infect 2014;142:1083-8.
64. Smith B, Oliver JD. In situ and in vitro gene expression by Vibrio vulnificus during entry into, persistence within, and resuscitation from the viable but nonculturable state. Appl Environ Microb 2006;72:1445-51.
65. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mo B 2004;3:1-25.
66. Stretton S, Danon SJ, Kjelleberg S, et al. Changes in cell morphology and motility in the marine Vibrio sp. strain S14 during conditions of starvation and recovery. FEMS Microbiol Lett 1997;146:23-9.
67. Sturn A, Quackenbush J, Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics 2002;18:207-8.
68. Su YC, Liu C. Vibrio parahaemolyticus: a concern of seafood safety. Food Microbiol 2007;24:549-58.
69. Thompson FL, Cleenwerck I, Swings J, et al. Genomic diversity and homologous recombination in Vibrio parahaemolyticus as revealed by amplified fragment length polymorphism (AFLP) and multilocus sequence analysis (MLSA). Microbes Environ 2007;22:373-9.
70. Trevors JT. Viable but non-culturable (VBNC) bacteria: gene expression in planktonic and biofilm cells. J Microbiol Meth 2011;86:266-73.
71. Vieira RH, de Sousa OV, Costa RA, et al. Raw oysters can be a risk for infections. Braz J Infect Dis 2010;14:66-70.
72. Vora GJ,Meador CE, Bird MM, et al. Microarray-based detection of genetic heterogeneity, antimicrobial resistance, and the viable but nonculturable state in human pathogenic Vibrio spp. P Natl Acad Sci USA 2005;102:19109-14.
73. Walker GC. The SOS response of Escherichia coli. In: Neidhardt FC, Ingraham JL, Low KB, et al. (eds). Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, Part IV. Washington, DC: American Society for Microbiology, 1987, 1346-57.
74. Wang S, Levin RE. Discrimination of viable Vibrio vulnificus cells from dead cells in real-time PCR. J Microbiol Meth 2006;64: 1-8.
75. Warner DF, Ndwandwe DE, Abrahams GL, et al. Essential roles for imuA'- and imuB-encoded accessory factors in DnaE2- dependent mutagenesis in Mycobacterium tuberculosis. P Natl Acad Sci USA 2010;107:13093-8.
76. Weichart D, McDougald D, Jacobs D, et al. In situ analysis of nucleic acids in cold-induced nonculturable Vibrio vulnificus. Appl Environ Microb 1997;63:2754-8.
77. Wertman KF, Mount DW. Nucleotide sequence binding specificity of the LexA repressor of Escherichia coli K-12. J Bacteriol 1985;163:376-84.
78. Wong HC,Wang P. Induction of viable but nonculturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J Appl Microbiol 2004;96:359-66.
79. Wu L, Thompson DK, Liu X, et al. Development and evaluation of microarray-based whole-genome hybridization for detection of microorganisms within the context of environmental applications. Environ Sci Technol 2004;38:6775-82.
80. Xu HS, Roberts N, Singleton FL, et al. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb Ecol 1982;8: 313-23.
81. Yang L, Zhou D, Liu X, et al. Cold-induced gene expression profiles of Vibrio parahaemolyticus: a time-course analysis. FEMS Microbiol Lett 2009;291:50-8.
82. Yaron S,Matthews KR. A reverse transcriptase-polymerase chain reaction assay for detection of viable Escherichia coli O157: H7: investigation of specific target genes. J Appl Microbiol 2002;92:633-40.
83. Yergeau E, Kang S, He Z, et al. Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J 2007;1:163-79.
84. Zhong L, Chen J, Zhang XH, et al. Entry of Vibrio cincinnatiensis into viable but nonculturable state and its resuscitation. Lett Appl Microbiol 2009;48:247-52.
85. Zhu L, Li Q. Stress-induced cellular adaptive mutagenesis. Yi chuan 2014;36:327-35.