Roles of Hfq in the stress adaptation and virulence in fish pathogen Vibrio alginolyticus and its potential application as a target for live attenuated vaccine

Applied Microbiology and Biotechnology

Volumn 91, Issue 2, 2011, Pages 353-364

  Liu, Huan ^a   Wang, Qiyao ^a   Liu, Qin ^a   Cao, Xiaodan ^a   Shi, Cunbin ^b   Zhang, Yuanxing ^a  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b SOUTH CHINA SEA FISHERIES RESEARCH INSTITUTE   (China)

Author keywords

Extracellular protease; Hfq; Quorum sensing; Stress resistance; Vibrio alginolyticus

Indexed keywords

EXTRACELLULAR PROTEASE; HFQ; QUORUM-SENSING; STRESS RESISTANCE; VIBRIO ALGINOLYTICUS;

AMINO ACIDS; BACTERIA; ETHANOL; GENE EXPRESSION; MARINE BIOLOGY;

GENE EXPRESSION REGULATION;

LIVE VACCINE; PROTEIN HFQ; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG;

ADAPTIVE RADIATION; BACTERIUM; DOSE-RESPONSE RELATIONSHIP; ECONOMIC ANALYSIS; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; FISH; GENE EXPRESSION; MUTATION; OSMOSIS; PATHOGENICITY; SENSITIVITY ANALYSIS; SURVIVAL; VACCINATION; VIRULENCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CONTROLLED STUDY; DRUG EFFICACY; NONHUMAN; PHENOTYPE; PLEIOTROPY; QUORUM SENSING; REGULATORY MECHANISM; VIBRIO ALGINOLYTICUS; VIBRIOSIS; ZEBRA FISH;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL VACCINES; CHINA; FISH DISEASES; FISHES; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; HOST FACTOR 1 PROTEIN; MOLECULAR SEQUENCE DATA; MUTATION; QUORUM SENSING; VACCINES, ATTENUATED; VIBRIO ALGINOLYTICUS; VIBRIO INFECTIONS; VIRULENCE; VIRULENCE FACTORS; ZEBRAFISH;

CHINA;

BACTERIA (MICROORGANISMS); VIBRIO ALGINOLYTICUS; VIBRIO HARVEYI;

EID: 79960701781     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3286-3     Document Type: Article

References (46)

1. C Bohn C Rigoulay P Bouloc 2007 No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus BMC Microbiol 7 10 10.1186/1471-2180-7-10 (Pubitemid 46277050)
2. XD Cao QY Wang Q Liu H Liu HH He YX Zhang 2010 Vibrio alginolyticus MviN is a LuxO-regulated protein and affects cytotoxicity toward EPC cell J Microbiol Biotechnol 20 271 280 1:CAS:528:DC%2BC3cXksVGjsb0%3D
3. Y Chao J Vogel 2010 The role of Hfq in bacterial pathogens Curr Opin Microbiol 13 24 33 10.1016/j.mib.2010.01.001 1:CAS:528:DC%2BC3cXhs1Ogsbc%3D
4. S Cheng Y Hu M Zhang L Sun 2010 Analysis of the vaccine potential of a natural avirulent Edwardsiella tarda isolate Vaccine 28 2716 2721 10.1016/j.vaccine.2010.01.023 1:CAS:528:DC%2BC3cXjtFyhs78%3D
5. JK Christiansen MH Larsen H Ingmer L Sogaard-Andersen BH Kallipolitis 2004 The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence J Bacteriol 186 3355 3362 10.1128/JB.186.11.3355-3362. 2004 1:CAS:528:DC%2BD2cXks1Cqsb8%3D (Pubitemid 38661530)
6. JW Costerton PS Stewart EP Greenberg 1999 Bacterial biofilms: a common cause of persistent infections Science 284 1318 1322 10.1126/science.284.5418. 1318 1:CAS:528:DyaK1MXjs1Squ78%3D (Pubitemid 29289651)
7. SM Denkin DR Nelson 1999 Induction of protease activity in Vibrio anguillarum by gastrointestinal mucus Appl Environ Microbiol 65 3555 3560 1:CAS:528:DyaK1MXltVOltr8%3D (Pubitemid 29398985)
8. JJ Dennis GJ Zylstra 1998 Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes Appl Environ Microbiol 64 2710 2715 1:CAS:528:DyaK1cXkt1OgsL0%3D (Pubitemid 28303324)
9. Y Ding B Davis M Waldor 2004 Hfq is essential for Vibrio cholerae virulence and downregulates σE expression Mol Microbiol 53 345 354 10.1111/j.1365-2958.2004.04142.x 1:CAS:528:DC%2BD2cXlvFentL8%3D (Pubitemid 38901403)
10. JL Enos-Berlage ZT Guvener CE Keenan LL McCarter 2005 Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus Mol Microbiol 55 1160 1182 10.1111/j.1365-2958.2004.04453.x 1:CAS:528:DC%2BD2MXit1emtbk%3D (Pubitemid 40299185)
11. L Fantappie MME Metruccio KL Seib 2009 The RNA chaperone Hfq is involved in stress response and virulence in Neisseria meningitidis and is a pleiotropic regulator of protein expression Infect Immun 77 1842 1853 10.1128/IAI.01216-08 1:CAS:528:DC%2BD1MXlsFSktL0%3D
12. MT Franze de Fernandez L Eoyang JT August 1968 Factor fraction required for the synthesis of bacteriophage Qbeta-RNA Nature 219 588 590 10.1038/219588a0 1:CAS:528:DyaF1cXltVeqt7Y%3D
13. BK Hammer BL Bassler 2007 Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae Proc Nat Acad Sci USA 104 11145 11149 10.1073/pnas.0703860104 1:CAS:528:DC%2BD2sXnvFGgtL4%3D (Pubitemid 47175108)
14. C Josenhans S Suerbaum 2002 The role of motility as a virulence factor in bacteria Int J Med Microbiol 291 605 614 10.1078/1438-4221-00173 1:CAS:528:DC%2BD38XksVKqtLo%3D (Pubitemid 34294495)
15. RR Kulesus K Diaz-Perez ES Slechta DS Eto MA Mulvey 2008 Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli Infec Immun 76 3019 3026 10.1128/IAI.00022-08 1:CAS:528:DC%2BD1cXotlKhtLk%3D
16. KK Lee SR Yu PC Liu 1997 Alkaline serine protease is an exotoxin of Vibrio alginolyticus in kuruma prawn, Penaeus japonicus Cur Microbiol 34 110 117 10.1007/s002849900153 (Pubitemid 27068684)
17. WL Liang SX Wang FG Yu LJ Zhang GM Qi YQ Liu SY Gao B Kan 2003 Construction and evaluation of a safe, live, oral Vibrio cholerae vaccine candidate, IEM108 Infec Immun 71 5498 5504 10.1128/IAI.71.10.5498-5504.2003 1:CAS:528:DC%2BD3sXnslylsbY%3D (Pubitemid 37205600)
18. TM Link P Valentin-Hansen RG Brennan 2009 Structure of Escherichia coli Hfq bound to polyriboadenylate RNA Proc Nat Acad Sci USA 106 19292 19297 10.1073/pnas.0908744106 1:CAS:528:DC%2BD1MXhsFGns7rO
19. CH Liu W Cheng JP Hsu JC Chen 2004 Vibrio alginolyticus infection in the white shrimp Litopenaeus vannamei confirmed by polymerase chain reaction and 16S rDNA sequencing Dis Aqua Organ 61 169 174 10.3354/dao061169 1:CAS:528:DC%2BD2MXotFWrtQ%3D%3D (Pubitemid 39588250)
20. KJ Livak TD Schmittgen 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method Methods 25 402 408 10.1006/meth.2001.1262 1:CAS:528:DC%2BD38XhtFelt7s%3D (Pubitemid 34164012)
21. Q Ma Y Zhang 2007 Characterization of the Vibrio alginolyticus fur gene and localization of essential amino acid sites in fur by site-directed mutagenesis J Mol Microbiol Biotechnol 13 15 21 10.1159/000103593 (Pubitemid 351359830)
22. R Maharjan Z Zhou Y Ren Y Li J Gaffe D Schneider C McKenzie PR Reeves T Ferenci L Wang 2010 Genomic identification of a novel mutation in hfq that provides multiple benefits in evolving glucose-limited populations of Escherichia coli J Bacteriol 192 4517 4521 10.1128/JB.00368-10 1:CAS:528:DC%2BC3cXhtlegsbbO
23. KL Meibom AL Forslund K Kuoppa K Alkhuder I Dubail M Dupuis A Forsberg A Charbit 2009 Hfq, a novel pleiotropic regulator of virulence-associated genes in Francisella tularensis Infect Immun 77 1866 1880 10.1128/IAI.01496-08 1:CAS:528:DC%2BD1MXlsFSktLs%3D
24. DL Milton R O'Toole P Horstedt H Wolf-Watz 1996 Flagellin A is essential for the virulence of Vibrio anguillarum J Bacteriol 178 1310 1319 1:CAS:528:DyaK28XhsVSqurs%3D (Pubitemid 26073387)
25. VM Morales A Bäckman M Bagdasarian 1991 A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants Gene 97 39 47 10.1016/0378-1119(91)90007-X 1:CAS:528:DyaK3MXhsFynsbg%3D
26. A Muffler D Fischer R Hengge-Aronis 1996 The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli Genes Dev 10 1143 1151 10.1101/gad.10.9.1143 1:CAS:528:DyaK28XjtFajurw%3D (Pubitemid 26152855)
27. M Nakano A Takahashi Z Su N Harada K Mawatari Y Nakaya 2008 Hfq regulates the expression of the thermostable direct hemolysin gene in Vibrio parahaemolyticus BMC Microbiol 8 155 10.1186/1471-2180-8-155
28. GA O'Toole R Kolter 1998 Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development Mol Microbiol 30 295 304 10.1046/j.1365-2958.1998.01062.x (Pubitemid 28480181)
29. LJ Reed H Muench 1938 A simple method of estimating fifty per cent endpoints Am J Epidemiology 27 493 497
30. HP Rui Q Liu Y Ma QY Wang YX Zhang 2008 Roles of LuxR in regulating extracellular alkaline serine protease A, extracellular polysaccharide and mobility of Vibrio alginolyticus FEMS Microbiol Lett 285 155 162 10.1111/j.1574-6968.2008.01185.x 1:CAS:528:DC%2BD1cXhtVers7fO (Pubitemid 352000226)
31. HP Rui Q Liu QY Wang Y Ma H Liu CB Shi YX Zhang 2009 Role of alkaline serine protease, Asp, in Vibrio alginolyticus virulence and regulation of its expression by LuxO-LuxR regulatory System J Microbiol Biotechnol 19 431 438 10.4014/jmb.0807.404 1:CAS:528:DC%2BD1MXotFOmu7s%3D
32. A Sittka V Pfeiffer K Tedin J Vogel 2007 The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium Mol Microbiol 63 193 217 10.1111/j.1365-2958.2006.05489.x 1:CAS:528:DC%2BD2sXhsVyisLk%3D (Pubitemid 44968119)
33. E Sonnleitner M Schuster T Sorger-Domenigg EP Greenberg U Bläsi 2006 Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aeruginosa Mol Microbiol 59 1542 1558 10.1111/j.1365-2958.2006.05032.x 1:CAS:528:DC%2BD28Xit1Shtr8%3D
34. T Soper P Mandin N Majdalani S Gottesman SA Woodson 2010 Positive regulation by small RNAs and the role of Hfq Proc Nat Acad Sci USA 107 9602 9607 10.1073/pnas.1004435107 1:CAS:528:DC%2BC3cXntFGqs7c%3D
35. SA Sousa CG Ramos LM Moreira JH Leitao 2010 The hfq gene is required for stress resistance and full virulence of Burkholderia cepacia to the nematode Caenorhabditis elegans Microbiology 156 896 908 10.1099/mic.0.035139-0 1:CAS:528:DC%2BC3cXktFOktr4%3D
36. S Stepanovi D Vukovi I Daki B Savi 2000 A modified microtiter-plate test for quantification of staphylococcal biofilm formation J Microbiol Methods 40 175 179 10.1016/S0167-7012(00)00122-6 (Pubitemid 30107900)
37. KM Thompson VA Rhodius S Gottesman 2007 σE regulates and is regulated by a small RNA in Escherichia coli J Bacteriol 189 4243 4256 10.1128/JB.00020-07 1:CAS:528:DC%2BD2sXmt1equ7c%3D (Pubitemid 46847373)
38. Y Tian QY Wang Q Liu Y Ma XD Cao LY Guan YX Zhang 2008 Involvement of LuxS in the regulation of motility and flagella biogenesis in Vibrio alginolyticus Biosci Biotechnol Biochem 72 1063 1071 10.1271/bbb.70812 1:CAS:528:DC%2BD1cXls1Wqs7g%3D (Pubitemid 351679360)
39. Y Tian QY Wang Q Liu Y Ma XD Cao YX Zhang 2008 Role of RpoS in stress survival, synthesis of extracellular autoinducer 2, and virulence in Vibrio alginolyticus Arch Microbiol 190 585 594 10.1007/s00203-008-0410-6 1:CAS:528:DC%2BD1cXht1artbjL
40. O Torres-Quesada RI Oruezabal A Peregrina E Jofré J Lloret R Rivilla N Toro JI Jiménez-Zurdo 2010 The Sinorhizobium meliloti RNA chaperone Hfq influences central carbon metabolism and the symbiotic interaction with alfalfa BMC Microbiol 10 71 10.1186/1471-2180-10-71
41. HCT Tsui HCE Leung ME Winkler 1994 Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12 Mol Microbiol 13 35 49 10.1111/j.1365-2958.1994.tb00400.x 1:CAS:528:DyaK2cXltVerur0%3D (Pubitemid 24220541)
42. QY Wang Q Liu Y Ma HP Rui YX Zhang 2007 LuxO controls extracellular protease, haemolytic activities and siderophore production in fish pathogen Vibrio alginolyticus J Appl Microbiology 103 1525 1534 10.1111/j.1365-2672.2007. 03380.x 1:CAS:528:DC%2BD2sXhsVSlsLjJ (Pubitemid 47620546)
43. B Weber A Croxatto C Chen DL Milton 2008 RpoS induces expression of the Vibrio anguillarum quorum-sensing regulator VanT Microbiology 154 767 780 10.1099/mic.0.2007/014167-0 1:CAS:528:DC%2BD1cXjvFers7g%3D (Pubitemid 351736291)
44. Z Yang Q Liu QY Wang YX Zhang 2008 Novel bacterial surface display systems based on outer membrane anchoring elements from the marine bacterium Vibrio anguillarum Appl Environ Microbiol 74 4359 4365 10.1128/AEM.02499-07 1:CAS:528:DC%2BD1cXptVeitr4%3D (Pubitemid 352031017)
45. J Ye Y Ma Q Liu DL Zhao QY Wang YX Zhang 2008 Regulation of Vibrio alginolyticus virulence by the LuxS quorum-sensing system J Fish Dis 31 161 169 10.1111/j.1365-2761.2007.00882.x 1:CAS:528:DC%2BD1cXktVSgsbs%3D (Pubitemid 351207245)
46. J Zhu JJ Mekalanos 2003 Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae Dev Cell 5 647 656 10.1016/S1534-5807(03)00295-8 1:CAS:528:DC%2BD3sXotlWjsr0%3D (Pubitemid 37243052)