Motility of Vibrio spp.: regulation and controlling strategies.
Biofilm
Molecules
Motility
Regulation
Transcription factors
Vibrio species
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
Oct 2020
Oct 2020
Historique:
received:
23
05
2020
accepted:
19
07
2020
revised:
15
07
2020
pubmed:
21
8
2020
medline:
15
5
2021
entrez:
21
8
2020
Statut:
ppublish
Résumé
Flagellar motility in bacteria is a highly regulated and complex cellular process that requires high energy investment for movement and host colonization. Motility plays an important role in the lifestyle of Vibrio spp. in the aquatic environment and during host colonization. Flagellar motility in vibrios is associated with several cellular processes, such as movement, colonization, adhesion, biofilm formation, and virulence. The transcription of all flagella-related genes occurs hierarchically and is regulated positively or negatively by several transcription factors and regulatory proteins. The flagellar regulatory hierarchy is well studied in Vibrio cholerae and Vibrio parahaemolyticus. Here, we compared the regulatory cascade and molecules involved in the flagellar motility of V. cholerae and V. parahaemolyticus in detail. The evolutionary relatedness of the master regulator of the polar and lateral flagella in different Vibrio species is also discussed. Although they can form symbiotic associations of some Vibrio species with humans and aquatic organisms can be harmed by several species of Vibrio as a result of surface contact, characterized by flagellar movement. Thus, targeting flagellar motility in pathogenic Vibrio species is considered a promising approach to control Vibrio infections. This approach, along with the strategies for controlling flagellar motility in different species of Vibrio using naturally derived and chemically synthesized compounds, is discussed in this review. KEY POINTS: • Vibrio species are ubiquitous and distributed across the aquatic environments. • The flagellar motility is responsible for the chemotactic movement and initial colonization to the host. • The transition from the motile into the biofilm stage is one of the crucial events in the infection. • Several signaling pathways are involved in the motility and formation of biofilm. • Attenuation of motility by naturally derived or chemically synthesized compounds could be a potential treatment for preventing Vibrio biofilm-associated infections.
Identifiants
pubmed: 32816086
doi: 10.1007/s00253-020-10794-7
pii: 10.1007/s00253-020-10794-7
doi:
Substances chimiques
Bacterial Proteins
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
8187-8208Subventions
Organisme : Ministry of Education
ID : NRF-2019R1A2C1087156
Références
Alavi M, Karimi N (2018) Antiplanktonic, antibiofilm, antiswarming motility and antiquorum sensing activities of green synthesized Ag-TiO2, TiO2-Ag, Ag-Cu and Cu-Ag nanocomposites against multi-drug-resistant bacteria. Artif Cells Nanomed Biotechnol 46(sup3):S399–S413. https://doi.org/10.1080/21691401.2018.1496923
doi: 10.1080/21691401.2018.1496923
pubmed: 30095025
Amera GM, Khan RJ, Pathak A, Jha RK, Muthukumaran J, Singh AK (2020) Computer aided ligand based screening for identification of promising molecules against enzymes involved in peptidoglycan biosynthetic pathway from Acinetobacter baumannii. Microb Pathog 147:104205. https://doi.org/10.1016/j.micpath.2020.104205
doi: 10.1016/j.micpath.2020.104205
pubmed: 32353580
Austin B (2010) Vibrios as causal agents of zoonoses. Vet Microbiol 140(3–4):310–317. https://doi.org/10.1016/j.vetmic.2009.03.015
doi: 10.1016/j.vetmic.2009.03.015
pubmed: 19342185
Ayala JC, Wang H, Silva AJ, Benitez JA (2015) Repression by H-NS of genes required for the biosynthesis of the Vibrio cholerae biofilm matrix is modulated by the second messenger cyclic diguanylic acid. Mol Microbiol 97(4):630–645. https://doi.org/10.1111/mmi.13058
doi: 10.1111/mmi.13058
pubmed: 25982817
pmcid: 4617317
Ayala JC, Silva AJ, Benitez JA (2017) H-NS: an overarching regulator of the Vibrio cholerae life cycle. Res Microbiol 168(1):16–25. https://doi.org/10.1016/j.resmic.2016.07.007
doi: 10.1016/j.resmic.2016.07.007
pubmed: 27492955
Beloin C, Renard S, Ghigo JM, Lebeaux D (2014) Novel approaches to combat bacterial biofilms. Curr Opin Pharmacol 18:61–68. https://doi.org/10.1016/j.coph.2014.09.005
doi: 10.1016/j.coph.2014.09.005
pubmed: 25254624
Beyhan S, Bilecen K, Salama SR, Casper-Lindley C, Yildiz FH (2007) Regulation of rugosity and biofilm formation in Vibrio cholerae: comparison of VpsT and VpsR regulons and epistasis analysis of vpsT, vpsR, and hapR. J Bacteriol 189(2):388–402. https://doi.org/10.1128/jb.00981-06
doi: 10.1128/jb.00981-06
pubmed: 17071756
Bhattaram V, Upadhyay A, Yin HB, Mooyottu S, Venkitanarayanan K (2017) Effect of dietary minerals on virulence attributes of Vibrio cholerae. Front Microbiol 8:911. https://doi.org/10.3389/fmicb.2017.00911
doi: 10.3389/fmicb.2017.00911
pubmed: 28579983
pmcid: 5437166
Bhunia AK (2008) Vibrio cholerae, V. parahaemolyticus, V. vulnificus foodborne microbial pathogens: mechanisms and pathogenesis. Springer New York, New York, pp 241–252
Boin MA, Austin MJ, Hase CC (2004) Chemotaxis in Vibrio cholerae. FEMS Microbiol Lett 239(1):1–8. https://doi.org/10.1016/j.femsle.2004.08.039
doi: 10.1016/j.femsle.2004.08.039
pubmed: 15451094
Boles BR, McCarter LL (2002) Vibrio parahaemolyticus scrABC, a novel operon affecting swarming and capsular polysaccharide regulation. J Bacteriol 184(21):5946–5954. https://doi.org/10.1128/jb.184.21.5946-5954.2002
doi: 10.1128/jb.184.21.5946-5954.2002
pubmed: 12374828
pmcid: 135390
Boyd EF, Carpenter MR, Chowdhury N, Cohen AL, Haines-Menges BL, Kalburge SS, Kingston JJ, Lubin JB, Ongagna-Yhombi SY, Whitaker WB (2015) Post-genomic analysis of members of the family vibrionaceae. Microbiol Spectr 3(5). https://doi.org/10.1128/microbiolspec.VE-0009-2014
Brenzinger S, Pecina A, Mrusek D, Mann P, Volse K, Wimmi S, Ruppert U, Becker A, Ringgaard S, Bange G, Thormann KM (2018) ZomB is essential for flagellar motor reversals in Shewanella putrefaciens and Vibrio parahaemolyticus. Mol Microbiol 109(5):694–709. https://doi.org/10.1111/mmi.14070
doi: 10.1111/mmi.14070
pubmed: 29995998
Butler SM, Camilli A (2004) Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc Natl Acad Sci U S A 101(14):5018–5023. https://doi.org/10.1073/pnas.0308052101
doi: 10.1073/pnas.0308052101
pubmed: 15037750
pmcid: 387366
Cai S, Cheng H, Pang H, Jian J, Wu Z (2018) AcfA is an essential regulator for pathogenesis of fish pathogen Vibrio alginolyticus. Vet Microbiol 213:35–41. https://doi.org/10.1016/j.vetmic.2017.11.016
doi: 10.1016/j.vetmic.2017.11.016
pubmed: 29292001
Casper-Lindley C, Yildiz FH (2004) VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J Bacteriol 186(5):1574–1578. https://doi.org/10.1128/jb.186.5.1574-1578.2004
doi: 10.1128/jb.186.5.1574-1578.2004
pubmed: 14973043
pmcid: 344397
Charway GNA, Park S, Yu D, Je JY, Kim DH, Jung WK, Kim YM (2019) In vitro antibacterial and synergistic effect of chitosan-phytochemical conjugates against antibiotic resistant fish pathogenic bacteria. Indian J Microbiol 59(1):116–120. https://doi.org/10.1007/s12088-018-0750-0
doi: 10.1007/s12088-018-0750-0
pubmed: 30728641
Chen L, Qiu Y, Tang H, Hu LF, Yang WH, Zhu XJ, Huang XX, Wang T, Zhang YQ (2018) ToxR is required for biofilm formation and motility of Vibrio parahaemolyticus. Biomed Environ Sci 31(11):848–850. https://doi.org/10.3967/bes2018.112
doi: 10.3967/bes2018.112
pubmed: 30558705
Chiavelli DA, Marsh JW, Taylor RK (2001) The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol 67(7):3220–3225. https://doi.org/10.1128/aem.67.7.3220-3225.2001
doi: 10.1128/aem.67.7.3220-3225.2001
pubmed: 11425745
pmcid: 93004
Chourashi R, Mondal M, Sinha R, Debnath A, Das S, Koley H, Chatterjee NS (2016) Role of a sensor histidine kinase ChiS of Vibrio cholerae in pathogenesis. Int J Med Microbiol 306(8):657–665. https://doi.org/10.1016/j.ijmm.2016.09.003
doi: 10.1016/j.ijmm.2016.09.003
pubmed: 27670078
Chung CH, Fen SY, Yu SC, Wong HC (2016) Influence of oxyR on growth, biofilm formation, and mobility of Vibrio parahaemolyticus. Appl Environ Microbiol 82(3):788–796. https://doi.org/10.1128/AEM.02818-15
doi: 10.1128/AEM.02818-15
pubmed: 26590276
pmcid: 4725280
Commichau FM, Dickmanns A, Gundlach J, Ficner R, Stulke J (2015) A jack of all trades: the multiple roles of the unique essential second messenger cyclic di-AMP. Mol Microbiol 97(2):189–204. https://doi.org/10.1111/mmi.13026
doi: 10.1111/mmi.13026
pubmed: 25869574
Conner JG, Zamorano-Sánchez D, Park JH, Sondermann H, Yildiz FH (2017) The ins and outs of cyclic di-GMP signaling in Vibrio cholerae. Curr Opin Microbiol 36:20–29. https://doi.org/10.1016/j.mib.2017.01.002
doi: 10.1016/j.mib.2017.01.002
pubmed: 28171809
pmcid: 5534393
Correa NE, Klose KE (2005) Characterization of enhancer binding by the Vibrio cholerae flagellar regulatory protein FlrC. J Bacteriol 187(9):3158–3170. https://doi.org/10.1128/JB.187.9.3158-3170.2005
doi: 10.1128/JB.187.9.3158-3170.2005
pubmed: 15838043
pmcid: 1082837
Correa NE, Lauriano CM, McGee R, Klose KE (2000) Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization. Mol Microbiol 35(4):743–755. https://doi.org/10.1046/j.1365-2958.2000.01745.x
doi: 10.1046/j.1365-2958.2000.01745.x
pubmed: 10692152
Correa NE, Barker JR, Klose KE (2004) The Vibrio cholerae FlgM homologue is an anti-sigma28 factor that is secreted through the sheathed polar flagellum. J Bacteriol 186(14):4613–4619. https://doi.org/10.1128/jb.186.14.4613-4619.2004
doi: 10.1128/jb.186.14.4613-4619.2004
pubmed: 15231794
pmcid: 438600
Correa NE, Peng F, Klose KE (2005) Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J Bacteriol 187(18):6324–6332. https://doi.org/10.1128/JB.187.18.6324-6332.2005
doi: 10.1128/JB.187.18.6324-6332.2005
pubmed: 16159765
pmcid: 1236648
Dang H, Lovell CR (2015) Microbial surface colonization and biofilm development in marine environments. Microbiol Mol Biol Rev 80(1):91–138. https://doi.org/10.1128/MMBR.00037-15
doi: 10.1128/MMBR.00037-15
pubmed: 26700108
pmcid: 4711185
Dittmann KK, Porsby CH, Goncalves P, Mateiu RV, Sonnenschein EC, Bentzon-Tilia M, Egan S, Gram L (2019) Tropodithietic acid induces oxidative stress response, cell envelope biogenesis and iron uptake in Vibrio vulnificus. Environ Microbiol Rep 11(4):581–588. https://doi.org/10.1111/1758-2229.12771
doi: 10.1111/1758-2229.12771
pubmed: 31102321
Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15(2):167–193. https://doi.org/10.1128/cmr.15.2.167-193.2002
doi: 10.1128/cmr.15.2.167-193.2002
pubmed: 11932229
pmcid: 11932229
Echazarreta MA, Klose KE (2019) Vibrio flagellar synthesis. Front Cell Infect Microbiol 9:131. https://doi.org/10.3389/fcimb.2019.00131
doi: 10.3389/fcimb.2019.00131
pubmed: 31119103
pmcid: 6504787
Enos-Berlage JL, McCarter LL (2000) Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus. J Bacteriol 182(19):5513–5520. https://doi.org/10.1128/jb.182.19.5513-5520.2000
doi: 10.1128/jb.182.19.5513-5520.2000
pubmed: 10986256
pmcid: 110996
Eom SH, Lee DS, Jung YJ, Park JH, Choi JI, Yim MJ, Jeon JM, Kim HW, Son KT, Je JY, Lee MS, Kim YM (2014) The mechanism of antibacterial activity of phlorofucofuroeckol-A against methicillin-resistant Staphylococcus aureus. Appl Microbiol Biotechnol 98(23):9795–9804. https://doi.org/10.1007/s00253-014-6041-8
doi: 10.1007/s00253-014-6041-8
pubmed: 25267155
Ferreira RB, Antunes LC, Greenberg EP, McCarter LL (2008) Vibrio parahaemolyticus ScrC modulates cyclic dimeric GMP regulation of gene expression relevant to growth on surfaces. J Bacteriol 190(3):851–860. https://doi.org/10.1128/JB.01462-07
doi: 10.1128/JB.01462-07
pubmed: 17993539
Ferreira RBR, Chodur DM, Antunes LCM, Trimble MJ, McCarter LL (2012) Output targets and transcriptional regulation by a cyclic dimeric GMP-responsive circuit in the Vibrio parahaemolyticus Scr network. J Bacteriol 194(5):914–924. https://doi.org/10.1128/jb.05807-11
doi: 10.1128/jb.05807-11
pubmed: 22194449
pmcid: 3294815
Fleitas Martínez O, Cardoso MH, Ribeiro SM, Franco OL (2019) Recent advances in anti-virulence therapeutic strategies with a focus on dismantling bacterial membrane microdomains, toxin neutralization, quorum-sensing interference and biofilm inhibition. Front Cell Infect Microbiol 9:74. https://doi.org/10.3389/fcimb.2019.00074
doi: 10.3389/fcimb.2019.00074
pubmed: 31001485
pmcid: 6454102
Floyd KA, Lee CK, Xian W, Nametalla M, Valentine A, Crair B, Zhu S, Hughes HQ, Chlebek JL, Wu DC, Hwan Park J, Farhat AM, Lomba CJ, Ellison CK, Brun YV, Campos-Gomez J, Dalia AB, Liu J, Biais N, Wong GCL, Yildiz FH (2020) C-di-GMP modulates type IV MSHA pilus retraction and surface attachment in Vibrio cholerae. Nat Commun 11(1):1549. https://doi.org/10.1038/s41467-020-15331-8
doi: 10.1038/s41467-020-15331-8
pubmed: 32214098
pmcid: 7096442
Forier K, Raemdonck K, De Smedt SC, Demeester J, Coenye T, Braeckmans K (2014) Lipid and polymer nanoparticles for drug delivery to bacterial biofilms. J Control Release 190:607–623. https://doi.org/10.1016/j.jconrel.2014.03.055
doi: 10.1016/j.jconrel.2014.03.055
pubmed: 24794896
Galperin MY, Nikolskaya AN, Koonin EV (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203(1):11–21. https://doi.org/10.1111/j.1574-6968.2001.tb10814.x
doi: 10.1111/j.1574-6968.2001.tb10814.x
pubmed: 11557134
Gardel CL, Mekalanos JJ (1996) Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect Immun 64(6):2246–2255
doi: 10.1128/IAI.64.6.2246-2255.1996
Ghosh A, Paul K, Chowdhury R (2006) Role of the histone-like nucleoid structuring protein in colonization, motility, and bile-dependent repression of virulence gene expression in Vibrio cholerae. Infect Immun 74(5):3060–3064. https://doi.org/10.1128/iai.74.5.3060-3064.2006
doi: 10.1128/iai.74.5.3060-3064.2006
pubmed: 16622251
pmcid: 1459692
Giacomucci S, Cros CD, Perron X, Mathieu-Denoncourt A, Duperthuy M (2019) Flagella-dependent inhibition of biofilm formation by sub-inhibitory concentration of polymyxin B in Vibrio cholerae. PLoS One 14(8):e0221431. https://doi.org/10.1371/journal.pone.0221431
doi: 10.1371/journal.pone.0221431
pubmed: 31430343
pmcid: 6701800
Gode-Potratz CJ, Chodur DM, McCarter LL (2010) Calcium and iron regulate swarming and type III secretion in Vibrio parahaemolyticus. J Bacteriol 192(22):6025–6038. https://doi.org/10.1128/JB.00654-10
doi: 10.1128/JB.00654-10
pubmed: 20851895
pmcid: 2976450
Gode-Potratz CJ, Kustusch RJ, Breheny PJ, Weiss DS, McCarter LL (2011) Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence. Mol Microbiol 79(1):240–263. https://doi.org/10.1111/j.1365-2958.2010.07445.x
doi: 10.1111/j.1365-2958.2010.07445.x
pubmed: 21166906
Gu D, Meng H, Li Y, Ge H, Jiao X (2019) A GntR family transcription factor (VPA1701) for swarming motility and colonization of Vibrio parahaemolyticus. Pathogens 8(4):235. https://doi.org/10.3390/pathogens8040235
doi: 10.3390/pathogens8040235
pmcid: 6963403
Guo D, Yang Z, Zheng X, Kang S, Yang Z, Xu Y, Shi C, Tian H, Xia X (2019) Thymoquinone inhibits biofilm formation and attachment-invasion in host cells of Vibrio parahaemolyticus. Foodborne Pathog Dis 16(10):671–678. https://doi.org/10.1089/fpd.2018.2591
doi: 10.1089/fpd.2018.2591
pubmed: 31070474
Gurung AB, Ali MA, Lee J, Al-Hemaid F, Farah MA, Al-Anazi KM (2020) Molecular docking elucidates the plausible mechanisms underlying the anticancer properties of acetyldigitoxigenin from Adenium obesum. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2020.04.020
Güvener ZT, McCarter LL (2003) Multiple regulators control capsular polysaccharide production in Vibrio parahaemolyticus. J Bacteriol 185(18):5431–5441. https://doi.org/10.1128/jb.185.18.5431-5441.2003
doi: 10.1128/jb.185.18.5431-5441.2003
pubmed: 12949095
pmcid: 193756
Hathroubi S, Mekni MA, Domenico P, Nguyen D, Jacques M (2017) Biofilms: microbial shelters against antibiotics. Microb Drug Resist 23(2):147–156. https://doi.org/10.1089/mdr.2016.0087
doi: 10.1089/mdr.2016.0087
pubmed: 27214143
Huang L, Xu W, Su Y, Zhao L, Yan Q (2018) Regulatory role of the RstB-RstA system in adhesion, biofilm production, motility, and hemolysis. Microbiologyopen 7(5):e00599. https://doi.org/10.1002/mbo3.599
doi: 10.1002/mbo3.599
pubmed: 29573209
pmcid: 6182747
Jaques S, McCarter LL (2006) Three new regulators of swarming in Vibrio parahaemolyticus. J Bacteriol 188(7):2625–2635. https://doi.org/10.1128/JB.188.7.2625-2635.2006
doi: 10.1128/JB.188.7.2625-2635.2006
pubmed: 16547050
pmcid: 1428401
Jaques S, Kim YK, McCarter LL (1999) Mutations conferring resistance to phenamil and amiloride, inhibitors of sodium-driven motility of Vibrio parahaemolyticus. Proc Natl Acad Sci U S A 96(10):5740–5745. https://doi.org/10.1073/pnas.96.10.5740
doi: 10.1073/pnas.96.10.5740
pubmed: 10318954
pmcid: 21930
Jeong HG, Choi SH (2008) Evidence that AphB, essential for the virulence of Vibrio vulnificus, is a global regulator. J Bacteriol 190(10):3768–3773. https://doi.org/10.1128/JB.00058-08
doi: 10.1128/JB.00058-08
pubmed: 18344367
pmcid: 2395019
Jones CJ, Utada A, Davis KR, Thongsomboon W, Zamorano Sanchez D, Banakar V, Cegelski L, Wong GC, Yildiz FH (2015) C-di-GMP regulates motile to sessile transition by modulating MshA Pili biogenesis and near-surface motility behavior in Vibrio cholerae. PLoS Pathog 11(10):e1005068. https://doi.org/10.1371/journal.ppat.1005068
doi: 10.1371/journal.ppat.1005068
pubmed: 26505896
pmcid: 4624765
Jung D, Yum SJ, Jeong HG (2017) Characterization and evaluation of antimicrobial activity of actinonin against foodborne pathogens. Food Sci Biotechnol 26(6):1649–1657. https://doi.org/10.1007/s10068-017-0190-3
doi: 10.1007/s10068-017-0190-3
pubmed: 30263702
pmcid: 6049706
Kawagishi I, Maekawa Y, Atsumi T, Homma M, Imae Y (1995) Isolation of the polar and lateral flagellum-defective mutants in Vibrio alginolyticus and identification of their flagellar driving energy sources. J Bacteriol 177(17):5158–5160. https://doi.org/10.1128/jb.177.17.5158-5160.1995
doi: 10.1128/jb.177.17.5158-5160.1995
pubmed: 7665498
pmcid: 177299
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. https://doi.org/10.1093/bioinformatics/bts199
doi: 10.1093/bioinformatics/bts199
pubmed: 22543367
pmcid: 22543367
Khan F, Khan MM, Kim YM (2018) Recent progress and future perspectives of antibiofilm drugs immobilized on nanomaterials. Curr Pharm Biotechnol 19(8):631–643. https://doi.org/10.2174/1389201019666180828090052
doi: 10.2174/1389201019666180828090052
pubmed: 30152281
Khan F, Oloketuyi SF, Kim YM (2019a) Diversity of bacteria and bacterial products as antibiofilm and antiquorum sensing drugs against pathogenic bacteria. Curr Drug Targets 20(11):1156–1179. https://doi.org/10.2174/1389450120666190423161249
doi: 10.2174/1389450120666190423161249
pubmed: 31020938
Khan F, Pham DTN, Oloketuyi SF, Kim YM (2019b) Regulation and controlling the motility properties of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 104(1):33–49. https://doi.org/10.1007/s00253-019-10201-w
doi: 10.1007/s00253-019-10201-w
pubmed: 31768614
Khan F, Pham DTN, Oloketuyi SF, Manivasagan P, Oh J, Kim YM (2020) Chitosan and their derivatives: antibiofilm drugs against pathogenic bacteria. Colloids Surf B Biointerfaces 185:110627. https://doi.org/10.1016/j.colsurfb.2019.110627
doi: 10.1016/j.colsurfb.2019.110627
pubmed: 31732391
Kim YK, McCarter LL (2000) Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J Bacteriol 182(13):3693–3704. https://doi.org/10.1128/jb.182.13.3693-3704.2000
doi: 10.1128/jb.182.13.3693-3704.2000
pubmed: 10850984
pmcid: 94540
Kim YK, McCarter LL (2007) ScrG, a GGDEF-EAL protein, participates in regulating swarming and sticking in Vibrio parahaemolyticus. J Bacteriol 189(11):4094–4107. https://doi.org/10.1128/JB.01510-06
doi: 10.1128/JB.01510-06
pubmed: 17400744
pmcid: 1913424
Kim MY, Park RY, Bai YH, Chung YY, Kim CM, Kim SY, Rhee JH, Shin SH (2006) X-Gal inhibits the swarming of Vibrio species. J Microbiol Methods 66(3):552–555. https://doi.org/10.1016/j.mimet.2006.01.004
doi: 10.1016/j.mimet.2006.01.004
pubmed: 16497398
Kim JR, Cha MH, Oh DR, Oh WK, Rhee JH, Kim YR (2010) Resveratrol modulates RTX toxin-induced cytotoxicity through interference in adhesion and toxin production. Eur J Pharmacol 642(1–3):163–168. https://doi.org/10.1016/j.ejphar.2010.05.037
doi: 10.1016/j.ejphar.2010.05.037
pubmed: 20553907
Kim BS, Jang SY, Bang YJ, Hwang J, Koo Y, Jang KK, Lim D, Kim MH, Choi SH (2018) QStatin, a selective inhibitor of quorum sensing in Vibrio species. mBio 9(1):e02262-17. https://doi.org/10.1128/mBio.02262-17
doi: 10.1128/mBio.02262-17
pubmed: 29382732
pmcid: 5790914
Kimbrough JH, Cribbs JT, McCarter LL (2020) Homologous c-di-GMP-binding Scr transcription factors orchestrate biofilm development in Vibrio parahaemolyticus. J Bacteriol 202(6):e00723–e00719. https://doi.org/10.1128/jb.00723-19
doi: 10.1128/jb.00723-19
pubmed: 31932310
pmcid: 7043675
Kirn TJ, Jude BA, Taylor RK (2005) A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438(7069):863–866. https://doi.org/10.1038/nature04249
doi: 10.1038/nature04249
pubmed: 16341015
Klose KE, Mekalanos JJ (1998) Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol Microbiol 28(3):501–520. https://doi.org/10.1046/j.1365-2958.1998.00809.x
doi: 10.1046/j.1365-2958.1998.00809.x
pubmed: 9632254
Kojima S, Yamamoto K, Kawagishi I, Homma M (1999) The polar flagellar motor of Vibrio cholerae is driven by an Na+ motive force. J Bacteriol 181(6):1927–1930
doi: 10.1128/JB.181.6.1927-1930.1999
Koo H, Allan RN, Howlin RP, Stoodley P, Hall-Stoodley L (2017) Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol 15(12):740–755. https://doi.org/10.1038/nrmicro.2017.99
doi: 10.1038/nrmicro.2017.99
pubmed: 28944770
pmcid: 5685531
Krasteva PV, Fong JCN, Shikuma NJ, Beyhan S, Navarro MVAS, Yildiz FH, Sondermann H (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327(5967):866–868. https://doi.org/10.1126/science.1181185
doi: 10.1126/science.1181185
pubmed: 20150502
pmcid: 2828054
Laganenka L, López ME, Colin R, Sourjik V (2020) Flagellum-mediated mechanosensing and RflP control motility state of pathogenic Escherichia coli. mBio 11(2): e02269-19. https://doi.org/10.1128/mBio.02269-19
Lauriano CM, Ghosh C, Correa NE, Klose KE (2004) The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J Bacteriol 186(15):4864–4874. https://doi.org/10.1128/JB.186.15.4864-4874.2004
doi: 10.1128/JB.186.15.4864-4874.2004
pubmed: 15262923
pmcid: 451641
Lim JG, Choi SH (2014) IscR is a global regulator essential for pathogenesis of Vibrio vulnificus and induced by host cells. Infect Immun 82(2):569–578. https://doi.org/10.1128/IAI.01141-13
doi: 10.1128/IAI.01141-13
pubmed: 24478072
pmcid: 3911388
Lim B, Beyhan S, Meir J, Yildiz FH (2006) Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol Microbiol 60(2):331–348. https://doi.org/10.1111/j.1365-2958.2006.05106.x
doi: 10.1111/j.1365-2958.2006.05106.x
pubmed: 16573684
Liu X, Beyhan S, Lim B, Linington RG, Yildiz FH (2010) Identification and characterization of a phosphodiesterase that inversely regulates motility and biofilm formation in Vibrio cholerae. J Bacteriol 192(18):4541–4552. https://doi.org/10.1128/jb.00209-10
doi: 10.1128/jb.00209-10
pubmed: 20622061
pmcid: 2937418
Lu R, Osei-Adjei G, Huang X, Zhang Y (2018) Role and regulation of the orphan AphA protein of quorum sensing in pathogenic Vibrios. Future Microbiol 13:383–391. https://doi.org/10.2217/fmb-2017-0165
doi: 10.2217/fmb-2017-0165
pubmed: 29441822
Lu L, Hu W, Tian Z, Yuan D, Yi G, Zhou Y, Cheng Q, Zhu J, Li M (2019) Developing natural products as potential anti-biofilm agents. Chin Med 14:11. https://doi.org/10.1186/s13020-019-0232-2
doi: 10.1186/s13020-019-0232-2
pubmed: 30936939
pmcid: 6425673
Luo J, Dong B, Wang K, Cai S, Liu T, Cheng X, Lei D, Chen Y, Li Y, Kong J, Chen Y (2017) Baicalin inhibits biofilm formation, attenuates the quorum sensing-controlled virulence and enhances Pseudomonas aeruginosa clearance in a mouse peritoneal implant infection model. PLoS One 12(4):e0176883. https://doi.org/10.1371/journal.pone.0176883
doi: 10.1371/journal.pone.0176883
pubmed: 28453568
pmcid: 5409170
Lutz C, Erken M, Noorian P, Sun S, McDougald D (2013) Environmental reservoirs and mechanisms of persistence of Vibrio cholerae. Front Microbiol 4:375. https://doi.org/10.3389/fmicb.2013.00375
doi: 10.3389/fmicb.2013.00375
pubmed: 24379807
pmcid: 3863721
Malik V, Dhanjal JK, Kumari A, Radhakrishnan N, Singh K, Sundar D (2017) Function and structure-based screening of compounds, peptides and proteins to identify drug candidates. Methods 131:10–21. https://doi.org/10.1016/j.ymeth.2017.08.010
doi: 10.1016/j.ymeth.2017.08.010
pubmed: 28843611
Martinez RM, Dharmasena MN, Kirn TJ, Taylor RK (2009) Characterization of two outer membrane proteins, FlgO and FlgP, that influence Vibrio cholerae motility. J Bacteriol 191(18):5669–5679. https://doi.org/10.1128/JB.00632-09
doi: 10.1128/JB.00632-09
pubmed: 19592588
pmcid: 2737956
McCarter LL (1998) OpaR, a homolog of Vibrio harveyi LuxR, controls opacity of Vibrio parahaemolyticus. J Bacteriol 180(12):3166–3173
doi: 10.1128/JB.180.12.3166-3173.1998
McCarter LL (2001) Polar flagellar motility of the Vibrionaceae. Microbiol Mol Biol Rev 65(3):445–462. https://doi.org/10.1128/mmbr.65.3.445-462.2001
doi: 10.1128/mmbr.65.3.445-462.2001
pubmed: 11528005
pmcid: 99036
McCarter LL (2004) Dual flagellar systems enable motility under different circumstances. J Mol Microbiol Biotechnol 7(1–2):18–29. https://doi.org/10.1159/000077866
doi: 10.1159/000077866
pubmed: 15170400
McCarter LL, Wright ME (1993) Identification of genes encoding components of the swarmer cell flagellar motor and propeller and a sigma factor controlling differentiation of Vibrio parahaemolyticus. J Bacteriol 175(11):3361–3371. https://doi.org/10.1128/jb.175.11.3361-3371.1993
doi: 10.1128/jb.175.11.3361-3371.1993
pubmed: 8501040
pmcid: 204733
Meibom KL, Li XB, Nielsen AT, Wu CY, Roseman S, Schoolnik GK (2004) The Vibrio cholerae chitin utilization program. Proc Natl Acad Sci U S A 101(8):2524–2529. https://doi.org/10.1073/pnas.0308707101
doi: 10.1073/pnas.0308707101
pubmed: 14983042
pmcid: 356983
Millikan DS, Ruby EG (2003) FlrA, a σ54-dependent transcriptional activator in Vibrio fischeri, is required for motility and symbiotic light-organ colonization. J Bacteriol 185(12):3547–3557. https://doi.org/10.1128/jb.185.12.3547-3557.2003
doi: 10.1128/jb.185.12.3547-3557.2003
pubmed: 12775692
pmcid: 156232
Miyashiro T, Oehlert D, Ray VA, Visick KL, Ruby EG (2014) The putative oligosaccharide translocase SypK connects biofilm formation with quorum signaling in Vibrio fischeri. Microbiologyopen 3(6):836–848. https://doi.org/10.1002/mbo3.199
doi: 10.1002/mbo3.199
pubmed: 25257018
pmcid: 4263508
Moisi M, Jenul C, Butler SM, New A, Tutz S, Reidl J, Klose KE, Camilli A, Schild S (2009) A novel regulatory protein involved in motility of Vibrio cholerae. J Bacteriol 191(22):7027–7038. https://doi.org/10.1128/JB.00948-09
doi: 10.1128/JB.00948-09
pubmed: 19767434
pmcid: 2772493
Moravec AR, Siv AW, Hobby CR, Lindsay EN, Norbash LV, Shults DJ, Symes SJK, Giles DK (2017) Exogenous polyunsaturated fatty acids impact membrane remodeling and affect virulence phenotypes among pathogenic Vibrio species. Appl Environ Microbiol 83(22):e01415–e01417. https://doi.org/10.1128/AEM.01415-17
doi: 10.1128/AEM.01415-17
pubmed: 28864654
pmcid: 5666147
Morency LP, Gaudreault F, Najmanovich R (2018) Applications of the NRGsuite and the molecular docking software FlexAID in computational drug discovery and design. Methods Mol Biol 1762:367–388. https://doi.org/10.1007/978-1-4939-7756-7_18
doi: 10.1007/978-1-4939-7756-7_18
pubmed: 29594781
Mulat M, Pandita A, Khan F (2019) Medicinal plant compounds for combating the multi-drug resistant pathogenic bacteria: a review. Curr Pharm Biotechnol 20(3):183–196. https://doi.org/10.2174/1872210513666190308133429
doi: 10.2174/1872210513666190308133429
pubmed: 30854956
Na HS, Cha MH, Oh DR, Cho CW, Rhee JH, Kim YR (2011) Protective mechanism of curcumin against Vibrio vulnificus infection. FEMS Immunol Med Microbiol 63(3):355–362. https://doi.org/10.1111/j.1574-695X.2011.00855.x
doi: 10.1111/j.1574-695X.2011.00855.x
pubmed: 22092562
Ni B, Colin R, Link H, Endres RG, Sourjik V (2020) Growth-rate dependent resource investment in bacterial motile behavior quantitatively follows potential benefit of chemotaxis. Proc Natl Acad Sci U S A 117(1):595–601. https://doi.org/10.1073/pnas.1910849117
doi: 10.1073/pnas.1910849117
pubmed: 31871173
Noh HJ, Nagami S, Kim MJ, Kim J, Lee NK, Lee KH, Park SJ (2015) Role of VcrD1 protein in expression and secretion of flagellar components in Vibrio parahaemolyticus. Arch Microbiol 197(3):397–410. https://doi.org/10.1007/s00203-014-1069-9
doi: 10.1007/s00203-014-1069-9
pubmed: 25516430
Osunla CA, Okoh AI (2017) Vibrio pathogens: a public health concern in rural water resources in sub-Saharan Africa. Int J Environ Res Public Health 14(10):1188. https://doi.org/10.3390/ijerph14101188
doi: 10.3390/ijerph14101188
pmcid: 5664689
Packiavathy IA, Sasikumar P, Pandian SK, Veera Ravi A (2013) Prevention of quorum-sensing-mediated biofilm development and virulence factors production in Vibrio spp. by curcumin. Appl Microbiol Biotechnol 97(23):10177–10187. https://doi.org/10.1007/s00253-013-4704-5
doi: 10.1007/s00253-013-4704-5
pubmed: 23354447
Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM (2010) The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a “backstop brake” mechanism. Mol Cell 38(1):128–139. https://doi.org/10.1016/j.molcel.2010.03.001
doi: 10.1016/j.molcel.2010.03.001
pubmed: 20346719
pmcid: 20346719
Phan NQ, Uebanso T, Shimohata T, Nakahashi M, Mawatari K, Takahashi A (2015) DNA-binding protein HU coordinates pathogenicity in Vibrio parahaemolyticus. J Bacteriol 197(18):2958–2964. https://doi.org/10.1128/JB.00306-15
doi: 10.1128/JB.00306-15
pubmed: 26148713
pmcid: 4542175
Pratt JT, Tamayo R, Tischler AD, Camilli A (2007) PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J Biol Chem 282(17):12860–12870. https://doi.org/10.1074/jbc.M611593200
doi: 10.1074/jbc.M611593200
pubmed: 17307739
pmcid: 2790426
Pratt JT, McDonough E, Camilli A (2009) PhoB regulates motility, biofilms, and cyclic di-GMP in Vibrio cholerae. J Bacteriol 191(21):6632–6642. https://doi.org/10.1128/JB.00708-09
doi: 10.1128/JB.00708-09
pubmed: 19734314
pmcid: 2795287
Prouty MG, Correa NE, Klose KE (2001) The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol Microbiol 39(6):1595–1609. https://doi.org/10.1046/j.1365-2958.2001.02348.x
doi: 10.1046/j.1365-2958.2001.02348.x
pubmed: 11260476
Pursley BR, Maiden MM, Hsieh ML, Fernandez NL, Severin GB, Waters CM (2018) Cyclic di-GMP regulates TfoY in Vibrio cholerae to control motility by both transcriptional and posttranscriptional mechanisms. J Bacteriol 200(7):e00578–e00517. https://doi.org/10.1128/JB.00578-17
doi: 10.1128/JB.00578-17
pubmed: 29311281
pmcid: 5847662
Rajalaxmi M, Amsa Devi V, Karutha Pandian S (2016) In vitro evaluation of indole-3-carboxaldehyde on Vibrio parahaemolyticus biofilms. Biologia 71(3):247–255
doi: 10.1515/biolog-2016-0043
Rajamanikandan S, Jeyakanthan J, Srinivasan P (2017) Discovery of potent inhibitors targeting Vibrio harveyi LuxR through shape and e-pharmacophore based virtual screening and its biological evaluation. Microb Pathog 103:40–56. https://doi.org/10.1016/j.micpath.2016.12.003
doi: 10.1016/j.micpath.2016.12.003
pubmed: 27939874
Rasmussen L, White EL, Pathak A, Ayala JC, Wang H, Wu JH, Benitez JA, Silva AJ (2011) A high-throughput screening assay for inhibitors of bacterial motility identifies a novel inhibitor of the Na+-driven flagellar motor and virulence gene expression in Vibrio cholerae. Antimicrob Agents Chemother 55(9):4134–4143. https://doi.org/10.1128/AAC.00482-11
doi: 10.1128/AAC.00482-11
pubmed: 21709090
pmcid: 3165335
Reguera G, Kolter R (2005) Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. J Bacteriol 187(10):3551–3555. https://doi.org/10.1128/jb.187.10.3551-3555.2005
doi: 10.1128/jb.187.10.3551-3555.2005
pubmed: 15866944
pmcid: 1112007
Reidl J, Klose KE (2002) Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol Rev 26(2):125–139. https://doi.org/10.1111/j.1574-6976.2002.tb00605.x
doi: 10.1111/j.1574-6976.2002.tb00605.x
pubmed: 12069878
Roelofs KG, Jones CJ, Helman SR, Shang X, Orr MW, Goodson JR, Galperin MY, Yildiz FH, Lee VT (2015) Systematic identification of cyclic-di-GMP binding proteins in Vibrio cholerae reveals a novel class of cyclic-di-GMP-binding ATPases associated with type II secretion systems. PLoS Pathog 11(10):e1005232. https://doi.org/10.1371/journal.ppat.1005232
doi: 10.1371/journal.ppat.1005232
pubmed: 26506097
pmcid: 4624772
Rogers A, Townsley L, Gallego-Hernandez AL, Beyhan S, Kwuan L, Yildiz FH (2016) The LonA protease regulates biofilm formation, motility, virulence, and the type vi secretion system in Vibrio cholerae. J Bacteriol 198(6):973–985. https://doi.org/10.1128/JB.00741-15
doi: 10.1128/JB.00741-15
pubmed: 26755629
pmcid: 4772603
Romling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77(1):1–52. https://doi.org/10.1128/MMBR.00043-12
doi: 10.1128/MMBR.00043-12
pubmed: 23471616
pmcid: 3591986
Roy R, Tiwari M, Donelli G, Tiwari V (2018) Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence 9(1):522–554. https://doi.org/10.1080/21505594.2017.1313372
doi: 10.1080/21505594.2017.1313372
pubmed: 28362216
Ruby EG, Urbanowski M, Campbell J, Dunn A, Faini M, Gunsalus R, Lostroh P, Lupp C, McCann J, Millikan D, Schaefer A, Stabb E, Stevens A, Visick K, Whistler C, Greenberg EP (2005) Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci U S A 102(8):3004–3009. https://doi.org/10.1073/pnas.0409900102
doi: 10.1073/pnas.0409900102
pubmed: 15703294
pmcid: 549501
Rutherford ST, van Kessel JC, Shao Y, Bassler BL (2011) AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev 25(4):397–408. https://doi.org/10.1101/gad.2015011
doi: 10.1101/gad.2015011
pubmed: 21325136
pmcid: 3042162
Rybak MJ, McGrath BJ (1996) Combination antimicrobial therapy for bacterial infections. Guidelines for the clinician. Drugs 52(3):390–405. https://doi.org/10.2165/00003495-199652030-00005
doi: 10.2165/00003495-199652030-00005
pubmed: 8875129
Ryjenkov DA, Simm R, Romling U, Gomelsky M (2006) The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J Biol Chem 281(41):30310–30314. https://doi.org/10.1074/jbc.C600179200
doi: 10.1074/jbc.C600179200
pubmed: 16920715
Sakuma M, Nishikawa S, Inaba S, Nishigaki T, Kojima S, Homma M, Imada K (2019) Structure of the periplasmic domain of SflA involved in spatial regulation of the flagellar biogenesis of Vibrio reveals a TPR/SLR-like fold. J Biochem 166(2):197–204. https://doi.org/10.1093/jb/mvz027
doi: 10.1093/jb/mvz027
pubmed: 30989194
Santhakumari S, Jayakumar R, Logalakshmi R, Prabhu NM, Abdul Nazar AK, Karutha Pandian S, Veera Ravi A (2018) In vitro and in vivo effect of 2,6-Di-tert-butyl-4-methylphenol as an antibiofilm agent against quorum sensing mediated biofilm formation of Vibrio spp. Int J Food Microbiol 281:60–71. https://doi.org/10.1016/j.ijfoodmicro.2018.05.024
Satish L, Santhakumari S, Gowrishankar S, Pandian SK, Ravi AV, Ramesh M (2017) Rapid biosynthesized AgNPs from Gelidiella acerosa aqueous extract mitigates quorum sensing mediated biofilm formation of Vibrio species-an in vitro and in vivo approach. Environ Sci Pollut Res Int 24(35):27254–27268. https://doi.org/10.1007/s11356-017-0296-4
Savoia D (2012) Plant-derived antimicrobial compounds: alternatives to antibiotics. Future Microbiol 7(8):979–990. https://doi.org/10.2217/fmb.12.68
doi: 10.2217/fmb.12.68
pubmed: 22913356
Schild S, Tamayo R, Nelson EJ, Qadri F, Calderwood SB, Camilli A (2007) Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell Host Microbe 2(4):264–277. https://doi.org/10.1016/j.chom.2007.09.004
doi: 10.1016/j.chom.2007.09.004
pubmed: 18005744
pmcid: 2169296
Seghal Kiran G, Priyadharshini S, Dobson ADW, Gnanamani E, Selvin J (2016) Degradation intermediates of polyhydroxy butyrate inhibits phenotypic expression of virulence factors and biofilm formation in luminescent Vibrio sp. PUGSK8. NPJ Biofilms Microbi 2(16002). https://doi.org/10.1038/npjbiofilms.2016.2
Shikuma NJ, Davis KR, Fong JN, Yildiz FH (2013) The transcriptional regulator, CosR, controls compatible solute biosynthesis and transport, motility and biofilm formation in Vibrio cholerae. Environ Microbiol 15(5):1387–1399. https://doi.org/10.1111/j.1462-2920.2012.02805.x
doi: 10.1111/j.1462-2920.2012.02805.x
pubmed: 22690884
Shinoda S, Nakahara N, Uchida E, Hiraga M (1985) Lateral flagellar antigen of Vibrio alginolyticus and Vibrio harveyi: existence of serovars common to the two species. Microbiol Immunol 29(3):173–182. https://doi.org/10.1111/j.1348-0421.1985.tb00817.x
doi: 10.1111/j.1348-0421.1985.tb00817.x
pubmed: 4010543
Silva AJ, Benitez JA (2016) Vibrio cholerae biofilms and cholera pathogenesis. PLoS Negl Trop Dis 10(2):e0004330. https://doi.org/10.1371/journal.pntd.0004330
doi: 10.1371/journal.pntd.0004330
pubmed: 26845681
pmcid: 4741415
Sowndarya J, Farisa Banu S, Madhura G, Yuvalakshmi P, Rubini D, Bandeira Junior G, Baldisserotto B, Vadivel V, Nithyanand P (2019) Agro food by-products and essential oil constituents curtail virulence and biofilm of Vibrio harveyi. Microb Pathog 135:103633. https://doi.org/10.1016/j.micpath.2019.103633
doi: 10.1016/j.micpath.2019.103633
pubmed: 31326562
Srinivasan R, Santhakumari S, Ravi AV (2017) In vitro antibiofilm efficacy of Piper betle against quorum sensing mediated biofilm formation of luminescent Vibrio harveyi. Microb Pathog 110:232–239. https://doi.org/10.1016/j.micpath.2017.07.001
doi: 10.1016/j.micpath.2017.07.001
pubmed: 28687321
Srivastava D, Hsieh ML, Khataokar A, Neiditch MB, Waters CM (2013) Cyclic di-GMP inhibits Vibrio cholerae motility by repressing induction of transcription and inducing extracellular polysaccharide production. Mol Microbiol 90(6):1262–1276. https://doi.org/10.1111/mmi.12432
doi: 10.1111/mmi.12432
pubmed: 24134710
Stewart BJ, McCarter LL (2003) Lateral flagellar gene system of Vibrio parahaemolyticus. J Bacteriol 185(15):4508–4518. https://doi.org/10.1128/jb.185.15.4508-4518.2003
doi: 10.1128/jb.185.15.4508-4518.2003
pubmed: 12867460
pmcid: 165745
Sun Y, Guo D, Hua Z, Sun H, Zheng Z, Xia X, Shi C (2019) Attenuation of multiple Vibrio parahaemolyticus virulence factors by citral. Front Microbiol 10:894. https://doi.org/10.3389/fmicb.2019.00894
doi: 10.3389/fmicb.2019.00894
pubmed: 31073298
pmcid: 6495081
Syed KA, Beyhan S, Correa N, Queen J, Liu J, Peng F, Satchell KJ, Yildiz F, Klose KE (2009) The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J Bacteriol 191(21):6555–6570. https://doi.org/10.1128/JB.00949-09
doi: 10.1128/JB.00949-09
pubmed: 19717600
pmcid: 2795290
Takekawa N, Kwon S, Nishioka N, Kojima S, Homma M (2016) HubP, a polar landmark protein, regulates flagellar number by assisting in the proper polar localization of FlhG in Vibrio alginolyticus. J Bacteriol 198(22):3091–3098. https://doi.org/10.1128/JB.00462-16
doi: 10.1128/JB.00462-16
pubmed: 27573015
pmcid: 5075038
Tamayo R, Patimalla B, Camilli A (2010) Growth in a biofilm induces a hyperinfectious phenotype in Vibrio cholerae. Infect Immun 78(8):3560–3569. https://doi.org/10.1128/IAI.00048-10
doi: 10.1128/IAI.00048-10
pubmed: 20515927
pmcid: 2916270
Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR (1990) Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56(6):1977–1980
doi: 10.1128/AEM.56.6.1977-1980.1990
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. https://doi.org/10.1093/molbev/msr121
doi: 10.1093/molbev/msr121
pubmed: 3203626
pmcid: 3203626
Teschler JK, Zamorano-Sanchez D, Utada AS, Warner CJ, Wong GC, Linington RG, Yildiz FH (2015) Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat Rev Microbiol 13(5):255–268. https://doi.org/10.1038/nrmicro3433
doi: 10.1038/nrmicro3433
pubmed: 25895940
pmcid: 4437738
Teschler JK, Cheng AT, Yildiz FH (2017) The two-component signal transduction system VxrAB positively regulates Vibrio cholerae biofilm formation. J Bacteriol 199(18):e00139–e00117. https://doi.org/10.1128/JB.00139-17
doi: 10.1128/JB.00139-17
pubmed: 28607158
pmcid: 5573074
Tischler AD, Camilli A (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53(3):857–869. https://doi.org/10.1111/j.1365-2958.2004.04155.x
doi: 10.1111/j.1365-2958.2004.04155.x
pubmed: 15255898
pmcid: 2790424
Trimble MJ, McCarter LL (2011) Bis-(3′-5′)-cyclic dimeric GMP-linked quorum sensing controls swarming in Vibrio parahaemolyticus. Proc Natl Acad Sci U S A 108(44):18079–18084. https://doi.org/10.1073/pnas.1113790108
doi: 10.1073/pnas.1113790108
pubmed: 22006340
pmcid: 3207653
Tsang J, Hoover TR (2014) Themes and variations: regulation of RpoN-dependent flagellar genes across diverse bacterial species. Scientifica (Cairo) 2014:681754–681754. https://doi.org/10.1155/2014/681754
doi: 10.1155/2014/681754
Tyers M, Wright GD (2019) Drug combinations: a strategy to extend the life of antibiotics in the 21st century. Nat Rev Microbiol 17(3):141–155. https://doi.org/10.1038/s41579-018-0141-x
doi: 10.1038/s41579-018-0141-x
pubmed: 30683887
Wang H, Wu J-H, Ayala JC, Benitez JA, Silva AJ (2011) Interplay among cyclic diguanylate, HapR, and the general stress response regulator (RpoS) in the regulation of Vibrio cholerae hemagglutinin/protease. J Bacteriol 193(23):6529–6538. https://doi.org/10.1128/JB.05166-11
doi: 10.1128/JB.05166-11
pubmed: 21965573
pmcid: 3232884
Wang H, Ayala JC, Benitez JA, Silva AJ (2012a) Interaction of the histone-like nucleoid structuring protein and the general stress response regulator RpoS at Vibrio cholerae promoters that regulate motility and hemagglutinin/protease expression. J Bacteriol 194(5):1205–1215. https://doi.org/10.1128/jb.05900-11
doi: 10.1128/jb.05900-11
pubmed: 22194453
pmcid: 3294804
Wang H, Ayala JC, Silva AJ, Benitez JA (2012b) The histone-like nucleoid structuring protein (H-NS) is a repressor of Vibrio cholerae exopolysaccharide biosynthesis (vps) genes. Appl Environ Microbiol 78(7):2482–2488. https://doi.org/10.1128/aem.07629-11
doi: 10.1128/aem.07629-11
pubmed: 22287003
pmcid: 3302599
Wang H, Zhang L, Silva AJ, Benitez JA (2013a) A quinazoline-2,4-diamino analog suppresses Vibrio cholerae flagellar motility by interacting with motor protein PomB and induces envelope stress. Antimicrob Agents Chemother 57(8):3950–3959. https://doi.org/10.1128/AAC.00473-13
doi: 10.1128/AAC.00473-13
pubmed: 23733460
pmcid: 3719709
Wang L, Ling Y, Jiang H, Qiu Y, Qiu J, Chen H, Yang R, Zhou D (2013b) AphA is required for biofilm formation, motility, and virulence in pandemic Vibrio parahaemolyticus. Int J Food Microbiol 160(3):245–251. https://doi.org/10.1016/j.ijfoodmicro.2012.11.004
doi: 10.1016/j.ijfoodmicro.2012.11.004
pubmed: 23290231
Wang H, Ayala JC, Benitez JA, Silva AJ (2014) The LuxR-type regulator VpsT negatively controls the transcription of rpoS, encoding the general stress response regulator, in Vibrio cholerae biofilms. J Bacteriol 196(5):1020–1030. https://doi.org/10.1128/jb.00993-13
doi: 10.1128/jb.00993-13
pubmed: 24363348
pmcid: 3957697
Wang H, Silva AJ, Benitez JA (2017) 3-Amino 1,8-naphthalimide, a structural analog of the anti-cholera drug virstatin inhibits chemically-biased swimming and swarming motility in vibrios. Microbes Infect 19(6):370–375. https://doi.org/10.1016/j.micinf.2017.03.003
Waters CM, Lu W, Rabinowitz JD, Bassler BL (2008) Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol 190(7):2527–2536. https://doi.org/10.1128/JB.01756-07
doi: 10.1128/JB.01756-07
pubmed: 18223081
pmcid: 2293178
Worthington RJ, Richards JJ, Melander C (2012) Small molecule control of bacterial biofilms. Org Biomol Chem 10(37):7457–7474. https://doi.org/10.1039/c2ob25835h
doi: 10.1039/c2ob25835h
pubmed: 22733439
pmcid: 3431441
Wright PM, Seiple IB, Myers AG (2014) The evolving role of chemical synthesis in antibacterial drug discovery. Angew Chem Int Ed Engl 53(34):8840–8869. https://doi.org/10.1002/anie.201310843
doi: 10.1002/anie.201310843
pubmed: 24990531
pmcid: 4536949
Xiu P, Liu R, Zhang D, Sun C (2017) Pumilacidin-like lipopeptides derived from marine bacterium Bacillus sp. strain 176 suppress the motility of Vibrio alginolyticus. Appl Environ Microbiol 83(12):e00450–e00417. https://doi.org/10.1128/AEM.00450-17
doi: 10.1128/AEM.00450-17
pubmed: 28389538
pmcid: 5452807
Yang Q, Defoirdt T (2015) Quorum sensing positively regulates flagellar motility in pathogenic Vibrio harveyi. Environ Microbiol 17(4):960–968. https://doi.org/10.1111/1462-2920.12420
doi: 10.1111/1462-2920.12420
pubmed: 24528485
Yang M, Frey EM, Liu Z, Bishar R, Zhu J (2010) The virulence transcriptional activator AphA enhances biofilm formation by Vibrio cholerae by activating expression of the biofilm regulator VpsT. Infect Immun 78(2):697–703. https://doi.org/10.1128/iai.00429-09
doi: 10.1128/iai.00429-09
pubmed: 19933826
Yildiz FH, Schoolnik GK (1999) Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci U S A 96(7):4028–4033. https://doi.org/10.1073/pnas.96.7.4028
doi: 10.1073/pnas.96.7.4028
pubmed: 10097157
pmcid: 22414
Yildiz FH, Visick KL (2009) Vibrio biofilms: so much the same yet so different. Trends Microbiol 17(3):109–118. https://doi.org/10.1016/j.tim.2008.12.004
Yildiz FH, Dolganov NA, Schoolnik GK (2001) VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS(ETr)-associated phenotypes in Vibrio cholerae O1 El Tor. J Bacteriol 183(5):1716–1726. https://doi.org/10.1128/jb.183.5.1716-1726.2001
doi: 10.1128/jb.183.5.1716-1726.2001
pubmed: 11160103
pmcid: 95057
Zamorano-Sánchez D, Fong JCN, Kilic S, Erill I, Yildiz FH (2015) Identification and characterization of VpsR and VpsT binding sites in Vibrio cholerae. J Bacteriol 197(7):1221–1235. https://doi.org/10.1128/JB.02439-14
doi: 10.1128/JB.02439-14
pubmed: 25622616
pmcid: 4352665
Zhang L, Osei-Adjei G, Zhang Y, Gao H, Yang W, Zhou D, Huang X, Yang H, Zhang Y (2017) CalR is required for the expression of T6SS2 and the adhesion of Vibrio parahaemolyticus to HeLa cells. Arch Microbiol 199(6):931–938. https://doi.org/10.1007/s00203-017-1361-6
doi: 10.1007/s00203-017-1361-6
pubmed: 28378143
Zhang L, Weng Y, Wu Y, Wang X, Yin Z, Yang H, Yang W, Zhang Y (2018) H-NS is an activator of exopolysaccharide biosynthesis genes transcription in Vibrio parahaemolyticus. Microb Pathog 116:164–167. https://doi.org/10.1016/j.micpath.2018.01.025
doi: 10.1016/j.micpath.2018.01.025
pubmed: 29366862
Zhu J, Mekalanos JJ (2003) Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5(4):647–656. https://doi.org/10.1016/s1534-5807(03)00295-8
doi: 10.1016/s1534-5807(03)00295-8
pubmed: 14536065
Zhu S, Kojima S, Homma M (2013) Structure, gene regulation and environmental response of flagella in Vibrio. Front Microbiol 4:410. https://doi.org/10.3389/fmicb.2013.00410
Zorraquino V, García B, Latasa C, Echeverz M, Toledo-Arana A, Valle J, Lasa I, Solano C (2013) Coordinated cyclic-Di-GMP repression of Salmonella motility through YcgR and cellulose. J Bacteriol 195(3):417–428. https://doi.org/10.1128/jb.01789-12
doi: 10.1128/jb.01789-12
pubmed: 23161026
pmcid: 3554008