Abstract
Vibrio alginolyticus as a common pathogen infecting humans and marine animals has become a severe threat to the global mariculture industry. Using liquid chromatography and tandem-mass spectrometry (LC–MS/MS) analysis, comparative proteomics between dctP-deletion (ΔdctP) strain and wild-type V. alginolyticus HY9901 was profiled, and total of 547 differentially expressed proteins (DEPs) were identified. In these DEPs, 310 proteins were upregulated and 237 proteins were downregulated. Comparative proteomics of ΔdctP and wild-type strains identified some important regulated factors of colonization and virulent proteins. The regulated factors of bacterial colonization mainly included LuxR and ToxR (biofilm formation), flagellins (FlaB and FlrB), mannose-sensitive hemagglutinin (MshA) pilus, various substrates of the type II secretion system (EpsD, SecD and SecF) and type IV secretion system (ClpV), quorum sensing systems (LuxR homologous ValR), the virulent heat shock proteins (IbpA and YbeY), lipopolysaccharide LptE, outer membrane proteins (OmpU and TolC), glutamate synthases (GltB and GltD), oligopeptide permease (OppA) and siderophores (IrgA). In our previous study, biological characteristics (swarming motility, biofilm formation, cell adhesion and colonized ability) were significantly decreased and LD50 was significantly increased of ΔdctP compared to wide-type. Taken together, these results suggest that DctP protein plays an important role in controlling biological characteristics through DEPs in this study to finally affecting intestinal colonization and virulence.
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REFERENCES
Yang, W., Ding, D., Zhang, C., Zhang, C., Zhou, J., and Su, X., Proteome Sci., 2015, vol. 13, no. 19. https://doi.org/10.1186/s12953-015-0075-4
Morris, J.G. Jr. and Black, R.E., N. Engl. J. Med., 1985, vol. 312, no. 6, pp. 343-350. https://doi.org/10.1056/nejm198502073120604
Jacobs Slifka, K.M., Newton, A.E., and Mahon, B.E., Epidemiol. Infect., 2017, vol. 145, no. 7, pp. 1491–1499. https://doi.org/10.1017/S0950268817000140
Rhie, M.N., Park, B., Ko, H.J., Choi, I.G., and Kim, O.B., MicrobiologyOpen, 2018, vol. 7, no. 3, p. e00565. https://doi.org/10.1002/mbo3.565
Walmsley, A.R., Shaw, J.G., and Kelly, D.J., Biochemistry, 1992, vol. 31, no. 45, pp. 11175–11181. https://doi.org/10.1021/bi00160a031
Cai, S., Cheng, H., Pang, H., Jian, J., and Wu, Z., Vet. Microbiol., 2018, vol. 213, pp. 35–41. https://doi.org/10.1016/j.vetmic.2017.11.016
Hughes, K.J., Everiss, K.D., Kovach, M.E., and Peterson, K.M., Gene, 1995, vol. 156, no. 1, pp. 59–61. https://doi.org/10.1016/0378-1119(95)00054-a
Zhang, Y., Tan, H., Yang, S., Huang, Y., Cai, S., Jian, J., et al., J. Fish Dis., 2022, vol. 45, no. 3, pp. 421–434. https://doi.org/10.1111/jfd.13571
Yildiz, F.H. and Visick, K.L., Trends Microbiol., 2009, vol. 17, no. 3, pp. 109–118. https://doi.org/10.1016/j.tim.2008.12.004
Luo, G., Huang, L., Su, Y., Qin, Y., Xu, X., Zhao, L., et al., Emerg. Microbes Infect., 2016, vol. 5, no. 8, p. e85. https://doi.org/10.1038/emi.2016.82
Kim, S.Y., Thanh, X.T., Jeong, K., Kim, S.B.K., Pan, S.O., Jung, C.H., et al., Infect. Immun., 2014, vol. 82, no. 1, pp. 29–42. https://doi.org/10.1128/IAI.00654-13
Echazarreta, M.A., Kepple, J.L., Yen, L-H., Chen, Y., and Klose, K.E., J. Bacteriol., 2018, vol. 200, no. 15, p. e00029-18. https://doi.org/10.1128/JB.000
Floyd, K.A., Lee, C.K., Xian, W., Nametalla, M., Valentine, A., Crair, B., et al., Nat. Commun., 2020, vol.11, no. 1, p. 1549. https://doi.org/10.1038/s41467-020-15331-8
Jones, C.J., Utada, A., Davis, K.R., Thongsomboon, W., Sanchez, D.Z., Banakar, V., et al., PLoS Pathog., 2015, vol. 11, no. 10, p. e1005068. https://doi.org/10.1371/journal.ppat.1005068
Watnick, P.I., Fullner, K.J., and Kolter, R., J. Bacteriol., 1999, vol. 181, no. 11, pp. 3606–3609. https://doi.org/10.1128/jb.181.11.3606-3609.1999
O’Boyle, N., Houeix, B., Kilcoyne, M., Joshi, L., and Boyd, A., Int. J. Med. Microbiol., 2013, vol. 303, no. 8, pp. 563–573. https://doi.org/10.1016/j.ijmm.2013.07.010
Davis, B.M., Lawson, E.H., Sandkvist, M., Ali, A., So zhamannan, S., and Waldor, M.K., Science, 2000, vol. 288, no. 5464, pp. 333–335. https://doi.org/10.1126/science.288.5464.333
Hand, N.J., Klein, R., Laskewitz, A., and Pohlschröder, M., J. Bacteriol., 2006, vol. 188, no. 4, pp. 1251–1259. https://doi.org/10.1128/jb.188.4.1251-1259.2006
Ali, A., Johnson, J.A., Franco, A.A., Metzger, D.J., Connell, T.D., Morris, J.G., et al., Infect. Immun., 2000, vol. 68, no. 4, pp. 1967–1974. https://doi.org/10.1128/IAI.68.4.1967-1974.2000
Cornelis, G.R., Nat. Rev. Microbiol., 2006, vol. 4, no. 11, pp. 811–825. https://doi.org/10.1038/nrmicro1526
Luo, G., Xu, X., Zhao, L., Qin, Y., Huang, L., Su, Y., et al., J. Fish. Dis., 2019, vol. 42, no. 7, pp. 991–1000. https://doi.org/10.1111/jfd.13001
Basler, M., Pilhofer, M., Henderson, G.P., Jensen, G.J., and Mekalanos, J.J., Nature, 2012, vol. 483, no. 7388, pp. 182–186. https://doi.org/10.1038/nature10846
Bolhassani, A. and Agi, E., Clin. Chim. Acta, 2019, vol. 498, pp. 90–100. https://doi.org/10.1016/j.cca.2019.08.015
Kitagawa, M., Matsumura, Y., and Tsuchido, T., FEMS Microbiol. Lett., 2000, vol. 184, no. 2, pp. 165–171. https://doi.org/10.1111/j.1574-6968.2000.tb09009.x
Kuczynska-Wisnik, D., Matuszewska, E., and Laskowska, E., Microbiology (Reading), 2010, vol. 156, no. Pt 1, pp. 148–157. https://doi.org/10.1099/mic.0.032334-0
Vercruysse, M., Kohrer, C., Davies, B.W., Arnold, M.F.F., Mekalanos, J.J., RajBhandary, U.L., et al., PLoS Pathog., 2014, vol. 10, no. 6, p. e1004175. https://doi.org/10.1371/journal.ppat.1004175
Xia, Y., Xu, C., Wang, D., Weng, Y., Jin, Y., Bai, F., et al., Appl. Environ. Microbiol., 2020, vol. 87, no. 5, p. e02171-20. https://doi.org/10.1128/AEM.02171-20
Nikaido, H., Microbiol. Mol. Biol. Rev., 2003, vol. 67, no. 4, pp. 593–656. https://doi.org/10.1128/mmbr.67.4.593-656.2003
Bacterial Lipopolysaccharides. Structure, Chemical Synthesis, Biogenesis and Interaction with Host Cells, Knirel, Y.A. and Valvano, M.A., Eds., Vienna: Springer, 2011, pp. 311–337. https://doi.org/10.1007/978-3-7091-0733-1_10
Wu, T., McCandlish, A.C., Gronenberg, L.S., Chng, S., Silhavy, T.J., and Kahne, D., Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, no. 31, pp. 11754–11759. https://doi.org/10.1073/pnas.0604744103
Withey, J.H. and DiRita, V.J., Mol. Microbiol., 2006, vol. 59, no. 6, pp. 1779–1789. https://doi.org/10.1111/j.1365-2958.2006.05053.x
Provenzano, D., and Klose, K.E., Proc. Natl. Acad. Sci. U. S. A., 2000, vol. 97, no. 18, pp. 10220–10224. https://doi.org/10.1073/pnas.170219997
Merrell, D.S., Bailey, C., Kaper, J.B., and Camilli, A., J. Bacteriol., 2001, vol. 183, no. 9, pp. 2746–2754. https://doi.org/10.1128/JB.183.9.2746-2754.2001
Duperthuy, M., Schmitt, P., Garzon, E., Caro, A., Rosa, R.D., Roux, F.L., et al., Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no. 7, pp. 2993–2998. https://doi.org/10.1073/pnas.1015326108
Goo, S.Y., Lee, H.J., Kim, W.H., Han, K., Park, D., Lee, H., et al., Infect. Immun., 2006, vol. 74, no. 10, pp. 5586–5594. https://doi.org/10.1128/IAI.00171-06
Weng, Y., Fields, E.G., Bina, T.F., Budnick, J.A., Kunkle, D.E., Bina, X.R., et al., Infect. Immun., 2021, vol. 89, no. 10, p. e0024221. https://doi.org/10.1128/iai.00242-21
Zhu, Z., Dong, C., Weng, S., and He, J., Fish Shellfish Immunol., 2019, vol. 86, pp. 143–151. https://doi.org/10.1016/j.fsi.2018.11.037
Lee, E.M., Ahn, S.H., Park, J.H., Lee, J.H., Ahn, S.C., and Kong, I.S., FEMS Microbiol. Lett., 2004, vol. 240, no. 1, pp. 21–30. https://doi.org/10.1016/j.femsle.2004.09.007
Wu, T.K., Wang, Y.K., Chen, Y.C., Feng, J.M., Liu, Y.H., and Wang, T.Y., J. Bacteriol., 2007, vol. 189, no. 22, pp. 8215–8223. https://doi.org/10.1128/JB.01039-07
Seliger, S.S., Mey, A.R., Valle, A.M., and Payne, S.M., Mol. Microbiol., 2001, vol. 39, no. 3, pp. 801–812. https://doi.org/10.1046/j.1365-2958.2001.02273.x
Leon-Sicairos, N., Angulo-Zamudio, U.A., de La Garza, M., Velázquez-Román, J., Flores-Villaseñor, H.M., and Canizalez-Román, A., Front. Microbiol., 2015, vol. 6, p. 702. https://doi.org/10.3389/fmicb.2015.00702
Huang, Y., Suo, Y., Shi, C., Szlavik, J., Shi, X.M., and Knøchel, S., Int. J. Food Microbiol., 2013, vol. 163, no. 2–3, pp. 223–230. https://doi.org/10.1016/j.ijfoodmicro.2013.02.023
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This work was funded by the Natural Science Foundation of Shenzhen City (JCYJ20190813114409506 and JCYJ20210324130003009) and the Natural Science Foundation of Guangdong Province (no. 2021A1515010532).
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Zhang, Y.L., Wu, F., Huang, Y.C. et al. Mechanisms Underlying the Virulence and Intestinal Colonization of the Vibrio alginolyticus HY9901 DctP Protein with Proteomic Analysis. Appl Biochem Microbiol 59, 646–658 (2023). https://doi.org/10.1134/S0003683823050198
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DOI: https://doi.org/10.1134/S0003683823050198