Abstract
Vibrio parahaemolyticus possesses two types of flagella: a single polar flagellum (Pof) for swimming and the peritrichous lateral flagella (Laf) for swarming. Expression of Laf genes has previously been reported to be regulated by the quorum sensing (QS) regulators AphA and OpaR. In the present study, we showed that OpaR, the QS regulator at high cell density (HCD), acted as a negative regulator of swimming motility and the transcription of Pof genes in V. parahaemolyticus. OpaR bound to the promoter-proximal DNA regions of flgAMN, flgMN, and flgBCDEFGHIJ within the Pof gene loci to repress their transcription, whereas it negatively regulates the transcription of flgKL-flaC in an indirect manner. Thus, this work investigated how QS regulated the swimming motility via direct action of its master regulator OpaR on the transcription of Pof genes in V. parahaemolyticus.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Chen, L., Qiu, Y., Tang, H., Hu, L.F., Yang, W.H., Zhu, X.J., Huang, X.X., Wang, T., and Zhang, Y.Q. 2018. ToxR is required for bio-film formation and motility of Vibrio parahaemolyticus. Biomed. Environ. Sci. 31, 848–850.
Chung, C.H., Fen, S., Yu, S.C., and Wong, H. 2016. Influence of oxyR on growth, biofilm formation, and mobility of Vibrio parahaemolyticus. Appl. Environ. Microbiol. 82, 788–796.
Enos-Berlage, J.L., Guvener, Z.T., Keenan, C.E., and McCarter, L.L. 2005. Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol. Microbiol. 55, 1160–1182.
Enos-Berlage, J.L. and McCarter, L.L. 2000. Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus. J. Bacteriol. 182, 5513–5520.
Gao, H., Zhang, Y., Yang, L., Liu, X., Guo, Z., Tan, Y., Han, Y., Huang, X., Zhou, D., and Yang, R. 2011. Regulatory effects of cAMP receptor protein (CRP) on porin genes and its own gene in Yersinia pestis. BMC Microbiol. 11, 40.
Gode-Potratz, C.J., Chodur, D.M., and McCarter, L.L. 2010. Calcium and iron regulate swarming and type III secretion in Vibrio parahaemolyticus. J. Bacteriol. 192, 6025–6038.
Gode-Potratz, C.J., Kustusch, R.J., Breheny, P.J., Weiss, D.S., and McCarter, L.L. 2011. Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence. Mol. Microbiol. 79, 240–263.
Hasegawa, H. and Häse, C.C. 2009. TetR-type transcriptional regulator VtpR functions as a global regulator in Vibrio tubiashii. Appl. Environ. Microbiol. 75, 7602–7609.
Henke, J.M. and Bassler, B.L. 2004. Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J. Bacteriol. 186, 3794–3805.
Jaques, S. and McCarter, L.L. 2006. Three new regulators of swarming in Vibrio parahaemolyticus. J. Bacteriol. 188, 2625–2635.
Kawagishi, I., Imagawa, M., Imae, Y., McCarter, L., and Homma, M. 1996. The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression. Mol. Microbiol. 20, 693–699.
Kernell Burke, A., Guthrie, L.T.C., Modise, T., Cormier, G., Jensen, R.V., McCarter, L.L., and Stevens, A.M. 2015. OpaR controls a network of downstream transcription factors in Vibrio parahaemolyticus BB22OP. PLoS ONE 10, e0121863.
Kim, S.M., Lee, D.H., and Choi, S.H. 2012. Evidence that the Vibrio vulnificus flagellar regulator FlhF is regulated by a quorum sensing master regulator SmcR. Microbiology 158, 2017–2025.
Kim, Y.K. and McCarter, L.L. 2000. Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol. 182, 3693–3704.
Kleber-Janke, T. and Becker, W.M. 2000. Use of modified BL21(DE3) Escherichia coli cells for high-level expression of recombinant peanut allergens affected by poor codon usage. Protein Expr. Purif. 19, 419–424.
Lu, R., Osei-Adjei, G., Huang, X., and Zhang, Y. 2018. Role and regulation of the orphan AphA protein of quorum sensing in pathogenic Vibrios. Future Microbiol. 13, 383–391.
Lu, R., Tang, H., Qiu, Y., Yang, W., Yang, H., Zhou, D., Huang, X., Hu, L., and Zhang, Y. 2019. Quorum sensing regulates the transcription of lateral flagellar genes in Vibrio parahaemolyticus. Future Microbiol. 14, 1043–1053.
Makino, K., Oshima, K., Kurokawa, K., Yokoyama, K., Uda, T., Tagomori, K., Iijima, Y., Najima, M., Nakano, M., Yamashita, A., et al. 2003. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361, 743–749.
McCarter, L.L. 1998. OpaR, a homolog of Vibrio harveyi LuxR, controls opacity of Vibrio parahaemolyticus. J. Bacteriol. 180, 3166–3173.
McCarter, L.L. 2001. Polar flagellar motility of the Vibrionaceae. Microbiol. Mol. Biol. Rev. 65, 445–462.
McCarter, L.L. 2004. Dual flagellar systems enable motility under different circumstances. J. Mol. Microbiol. Biotechnol. 7, 18–29.
McCarter, L. and Silverman, M. 1989. Iron regulation of swarmer cell differentiation of Vibrio parahaemolyticus. J. Bacteriol. 171, 731–736.
Ng, W.L. and Bassler, B.L. 2009. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43, 197–222.
Nielsen, A.T., Dolganov, N.A., Otto, G., Miller, M.C., Wu, C.Y., and Schoolnik, G.K. 2006. RpoS controls the Vibrio cholerae mucosal escape response. PLoS Pathog. 2, e109.
Noh, H.J., Nagami, S., Kim, M.J., Kim, J., Lee, N.K., Lee, K.H., and Park, S.J. 2015. Role of VcrD1 protein in expression and secretion of flagellar components in Vibrio parahaemolyticus. Arch. Microbiol. 197, 397–410.
Park, K.S., Arita, M., Iida, T., and Honda, T. 2005. vpaH, a gene encoding a novel histone-like nucleoid structure-like protein that was possibly horizontally acquired, regulates the biogenesis of lateral flagella in trh-positive Vibrio parahaemolyticus TH3996. Infect. Immun. 73, 5754–5761.
Sun, F., Zhang, Y., Wang, L., Yan, X., Tan, Y., Guo, Z., Qiu, J., Yang, R., **a, P., and Zhou, D. 2012. Molecular characterization of direct target genes and cis-acting consensus recognized by quorum-sensing regulator AphA in Vibrio parahaemolyticus. PLoS ONE 7, e44210.
van Helden, J. 2003. Regulatory sequence analysis tools. Nucleic Acids Res. 31, 3593–3596.
van Kessel, J.C., Rutherford, S.T., Shao, Y., Utria, A.F., and Bassler, B.L. 2013. Individual and combined roles of the master regulators AphA and LuxR in control of the Vibrio harveyi quorum-sensing regulon. J. Bacteriol. 195, 436–443.
Wang, L., Ling, Y., Jiang, H., Qiu, Y., Qiu, J., Chen, H., Yang, R., and Zhou, D. 2013a. AphA is required for biofilm formation, motility, and virulence in pandemic Vibrio parahaemolyticus. Int. J. Food Microbiol. 160, 245–251.
Wang, Y., Zhang, Y., Yin, Z., Wang, J., Zhu, Y., Peng, H., Zhou, D., Qi, Z., and Yang, W. 2018. H-NS represses transcription of the flagellin gene lafA of lateral flagella in Vibrio parahaemolyticus. Can. J. Microbiol. 64, 69–74.
Wang, L., Zhou, D., Mao, P., Zhang, Y., Hou, J., Hu, Y., Li, J., Hou, S., Yang, R., Wang, R., et al. 2013b. Cell density- and quorum sensing-dependent expression of type VI secretion system 2 in Vibrio parahaemolyticus. PLoS ONE 8, e73363.
Yang, Q. and Defoirdt, T. 2015. Quorum sensing positively regulates flagellar motility in pathogenic Vibrio harveyi. Environ. Microbiol. 17, 960–968.
Yildiz, F.H. and Visick, K.L. 2009. Vibrio biofilms: so much the same yet so different. Trends Microbiol. 17, 109–118.
Zhang, Y., Gao, H., Osei-Adjei, G., Zhang, Y., Yang, W., Yang, H., Yin, Z., Huang, X., and Zhou, D. 2017. Transcriptional regulation of the type VI secretion system 1 genes by quorum sensing and ToxR in Vibrio parahaemolyticus. Front. Microbiol. 8, 2005.
Zhang, Y., Hu, L., Qiu, Y., Osei-Adjei, G., Tang, H., Zhang, Y., Zhang, R., Sheng, X., Xu, S., Yang, W., et al. 2019. QsvR integrates into quorum sensing circuit to control Vibrio parahaemolyticus virulence. Environ. Microbiol. 21, 1054–1067.
Zhang, Y., Qiu, Y., Tan, Y., Guo, Z., Yang, R., and Zhou, D. 2012. Trans-criptional regulation of opaR, qrr2-4 and aphA by the master quorum-sensing regulator OpaR in Vibrio parahaemolyticus. PLoS ONE 7, e34622.
Zhou, D., Yan, X., Qu, F., Wang, L., Zhang, Y., Hou, J., Hu, Y., Li, J., **n, S., Qiu, J., et al. 2013. Quorum sensing modulates transcription of cpsQ-mfpABC and mfpABC in Vibrio parahaemolyticus. Int. J. Food Microbiol. 166, 458–463.
Zhu, S., Kojima, S., and Homma, M. 2013. Structure, gene regulation and environmental response of flagella in Vibrio. Front. Microbiol. 4, 410.
Acknowledgements
This work was supported by the Postdoctoral Science Foundation Funded Project of Jiangsu Province (Grant No. 2020Z102), the National Natural Science Foundation of China (82072239) and the China Postdoctoral Science Foundation (Grant No. 2020M681513).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
The authors have no conflicts of interest to report.
Rights and permissions
About this article
Cite this article
Lu, R., Sun, J., Qiu, Y. et al. The quorum sensing regulator OpaR is a repressor of polar flagellum genes in Vibrio parahaemolyticus. J Microbiol. 59, 651–657 (2021). https://doi.org/10.1007/s12275-021-0629-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12275-021-0629-3