ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus

References

• Letchumanan V, Chan KG, Lee LH. Vibrio parahaemolyticus: a review on the pathogenesis, prevalence, and advance molecular identification techniques. Front Microbiol. 2014;5:705.
   PubMed Web of Science ®Google Scholar
• Zhang L, Orth K. Virulence determinants for Vibrio parahaemolyticus infection. Curr Opin Microbiol. 2013;16(1):70–14.
   PubMed Web of Science ®Google Scholar
• Ghenem L, Elhadi N, Alzahrani F, et al. Vibrio Parahaemolyticus: a review on distribution, pathogenesis, virulence determinants and epidemiology. Saudi J Med Med Sci. 2017;5(2):93–103. DOI:10.4103/sjmms.sjmms_30_17
   PubMed Web of Science ®Google Scholar
• Matsuda S, Hiyoshi H, Tandhavanant S, et al. Advances on Vibrio parahaemolyticus research in the postgenomic era. Microbiol Immunol. 2020;64(3):167–181. DOI:10.1111/1348-0421.12767
   PubMed Web of Science ®Google Scholar
• Paudyal N, Pan H, Liao XY, et al. A meta-analysis of major foodborne pathogens in Chinese food commodities between 2006 and 2016. Foodborne Pathog Dis. 2018;15(4):187–197. DOI:10.1089/fpd.2017.2417
   PubMed Web of Science ®Google Scholar
• Klein SL, West CKG, Mejia DM, et al. Genes similar to the Vibrio parahaemolyticus virulence-related genes tdh, tlh, and vscC2 occur in other vibrionaceae species isolated from a pristine estuary. Appl Environ Microb. 2014;80(2):595–602. DOI:10.1128/AEM.02895-13
   PubMed Web of Science ®Google Scholar
• Lee CT, Chen IT, Yang YT, et al. The opportunistic marine pathogen Vibrio parahaemolyticus becomes virulent by acquiring a plasmid that expresses a deadly toxin. Proc Natl Acad Sci, USA. 2015;112(34):10798–10803. DOI:10.1073/pnas.1503129112
   PubMed Web of Science ®Google Scholar
• Prachumwat A, Taengchaiyaphum S, Mungkongwongsiri N, et al. Update on early mortality syndrome/acute hepatopancreatic necrosis disease by April 2018. J World Aquacult Soc. 2019;50(1):5–17. DOI:10.1111/jwas.12559
   Web of Science ®Google Scholar
• Begg SL. The role of metal ions in the virulence and viability of bacterial pathogens. Biochem Soc Trans. 2019;47(1):77–87.
   PubMedGoogle Scholar
• Hood MI, Skaar EP. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol. 2012;10(8):525–537.
   PubMed Web of Science ®Google Scholar
• Burcham LR, Le Breton Y, Radin JN, et al. Identification of zinc-dependent mechanisms used by group B streptococcus to overcome calprotectin-mediated stress. MBio. 2020;11(6):e02302–20. DOI:10.1128/mBio.02302-20
   PubMed Web of Science ®Google Scholar
• Makthal N, Nguyen K, Do H, et al. A critical role of zinc importer AdcABC in group a Streptococcus-host interactions during infection and its Implications for vaccine development. EBioMedicine. 2017;21:131–141.
   PubMed Web of Science ®Google Scholar
• Chandrangsu P, Rensing C, Helmann JD. Metal homeostasis and resistance in bacteria. Nat Rev Microbiol. 2017;15(6):338–350.
   PubMed Web of Science ®Google Scholar
• Price SL, Vadyvaloo V, DeMarco JK, et al. Yersiniabactin contributes to overcoming zinc restriction during Yersinia pestis infection of mammalian and insect hosts. Proc Natl Acad Sci, USA. 2021;118(44):e2104073118. DOI:10.1073/pnas.2104073118
   PubMed Web of Science ®Google Scholar
• Honsa ES, Johnson MD, Rosch JW. The roles of transition metals in the physiology and pathogenesis of Streptococcus pneumoniae. Front Cell Infect Microbiol. 2013;3:92.
   PubMed Web of Science ®Google Scholar
• Karunasagar I, Joseph SW, Twedt RM, et al. Enhancement of Vibrio parahaemolyticus virulence by lysed erythrocyte factor and iron. Infect Immun. 1984;46(1):141–144. DOI:10.1128/iai.46.1.141-144.1984
   PubMed Web of Science ®Google Scholar
• Gode-Potratz CJ, Chodur DM, McCarter LL. Calcium and iron regulate swarming and type III secretion in Vibrio parahaemolyticus. J Bacteriol. 2010;192(22):6025–6038.
   PubMed Web of Science ®Google Scholar
• Zhou J, Lu C, Zhang D, et al. NMR-based metabolomics reveals the metabolite profiles of Vibrio parahaemolyticus under ferric iron stimulation. J Microbiol. 2017;55(8):628–634. DOI:10.1007/s12275-017-6551-z
   PubMed Web of Science ®Google Scholar
• León-Sicairos N, Angulo-Zamudio UA, de la Garza M, et al. Strategies of Vibrio parahaemolyticus to acquire nutritional iron during host colonization. Front Microbiol. 2015;6:702.
   PubMed Web of Science ®Google Scholar
• Andreini C, Banci L, Bertini I, et al. Zinc through the three domains of life. J Proteome Res. 2006;5(11):3173–3178. DOI:10.1021/pr0603699
   PubMed Web of Science ®Google Scholar
• Liu M, Yan M, Liu L, et al. Characterization of a novel zinc transporter ZnuA acquired by Vibrio parahaemolyticus through horizontal gene transfer. Front Cell Infect Microbiol. 2013;3:61.
   PubMed Web of Science ®Google Scholar
• 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(9359):743–749. DOI:10.1016/S0140-6736(03)12659-1
   PubMed Web of Science ®Google Scholar
• Sheng Y, Fan F, Jensen O, et al. Dual zinc transporter systems in Vibrio cholerae promote competitive advantages over gut microbiome. Infect Immun. 2015;83(10):3902–3908. DOI:10.1128/IAI.00447-15
   PubMed Web of Science ®Google Scholar
• Zheng C, Qiu J, Zhao X, et al. The AdcR-regulated AdcA and AdcAII contribute additively to zinc acquisition and virulence in Streptococcus suis. Vet Microbiol. 2022;269:109418.
   PubMed Web of Science ®Google Scholar
• Bu D, Luo H, Huo P, et al. KOBAS-i: intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Res. 2021;49(W1):W317–25. DOI:10.1093/nar/gkab447
   PubMed Web of Science ®Google Scholar
• Zhao F, Maren NA, Kosentka PZ, et al. An optimized protocol for stepwise optimization of real-time RT-PCR analysis. Hortic Res. 2021;8(1):179. DOI:10.1038/s41438-021-00616-w
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-delta delta C) method. Methods. 2001;25(4):402–408.
   PubMed Web of Science ®Google Scholar
• Milton DL, O’Toole R, Horstedt P, et al. Flagellin a is essential for the virulence of Vibrio anguillarum. J Bacteriol. 1996;178(5):1310–1319. DOI:10.1128/jb.178.5.1310-1319.1996
   PubMed Web of Science ®Google Scholar
• Morales VM, Bäckman A, Bagdasarian M. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene. 1991;97(1):39–47.
   PubMed Web of Science ®Google Scholar
• Whitaker WB, Richards GP, Boyd EF. Loss of sigma factor RpoN increases intestinal colonization of Vibrio parahaemolyticus in an adult mouse model. Infect Immun. 2014;82(2):544–556.
   PubMed Web of Science ®Google Scholar
• Heering J, Alvarado A, Ringgaard S. Induction of cellular differentiation and single cell imaging of Vibrio parahaemolyticus swimmer and swarmer cells. J Visualized Exp. 2017;123:55842. DOI:10.3791/55842
   PubMed Web of Science ®Google Scholar
• Croxatto A, Chalker VJ, Lauritz J, et al. VanT, a homologue of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment, and biofilm production in Vibrio anguillarum. J Bacteriol. 2002;184(6):1617–1629. DOI:10.1128/JB.184.6.1617-1629.2002
   PubMed Web of Science ®Google Scholar
• Gu D, Zhang Y, Wang Q, et al. S-nitrosylation-mediated activation of a histidine kinase represses the type 3 secretion system and promotes virulence of an enteric pathogen. Nat Commun. 2020;11(1):5777. DOI:10.1038/s41467-020-19506-1
   PubMed Web of Science ®Google Scholar
• Xiao Y, Chen H, Nie L, et al. Identification of c-di-GMP/FleQ-regulated new target genes, including cyaA, encoding adenylate cyclase, in Pseudomonas putida. mSystems. 2021;6(3):e00295–21. DOI:10.1128/mSystems.00295-21
   PubMed Web of Science ®Google Scholar
• Novichkov PS, Kazakov AE, Ravcheev DA, et al. RegPrecise 3.0 – a resource for genome-scale exploration of transcriptional regulation in bacteria. BMC Genomics. 2013;14(1):745. DOI:10.1186/1471-2164-14-745
   PubMedGoogle Scholar
• Varela PF, Velours C, Aumont-Nicaise M, et al. Biophysical and structural characterization of a zinc-responsive repressor of the MarR superfamily. PLoS ONE. 2019;14(2):e0210123. DOI:10.1371/journal.pone.0210123
   PubMed Web of Science ®Google Scholar
• Wątły J, Potocki S, Rowińska-Żyrek M. Zinc homeostasis at the bacteria/host interface-from coordination chemistry to nutritional immunity. Chemistry. 2016;22(45):15992–10.
   PubMed Web of Science ®Google Scholar
• Capdevila DA, Wang J, Giedroc DP. Bacterial strategies to maintain zinc metallostasis at the host-pathogen interface. J Biol Chem. 2016;291(40):20858–20868.
   PubMed Web of Science ®Google Scholar
• Quan GM, Xia PP, Lian SQ, et al. Zinc uptake system ZnuACB is essential for maintaining pathogenic phenotype of F4ac(+) enterotoxigenic E. coli (ETEC) under a zinc restricted environment. Vet Res. 2020;51(1):127. DOI:10.1186/s13567-020-00854-1
   PubMed Web of Science ®Google Scholar
• Goethe E, Gieseke A, Laarmann K, et al. Identification and characterization of Mycobacterium smegmatis and Mycobacterium avium subsp. paratuberculosis zinc transporters. J Bacteriol. 2021;203(11):e00049–21. DOI:10.1128/JB.00049-21
   PubMed Web of Science ®Google Scholar
• Santos RERS, da Silva WP, Harrison S, et al. The zinc transporter ZnuABC is critical for the virulence of Chromobacterium violaceum and contributes to diverse zinc-dependent physiological processes. Infect Immun. 2021;89(11):e00311–21. DOI:10.1128/IAI.00311-21
   PubMed Web of Science ®Google Scholar
• Goethe E, Laarmann K, Luhrs J, et al. Critical role of Zur and SmtB in zinc homeostasis of Mycobacterium smegmatis. mSystems. 2020;5(2):e00880–19. DOI:10.1128/mSystems.00880-19
   PubMed Web of Science ®Google Scholar
• Bobrov AG, Kirillina O, Fosso MY, et al. Zinc transporters YbtX and ZnuABC are required for the virulence of Yersinia pestis in bubonic and pneumonic plague in mice. Metallomics. 2017;9(6):757–772. DOI:10.1039/C7MT00126F
   PubMed Web of Science ®Google Scholar
• Broberg CA, Calder TJ, Orth K. Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect. 2011;13(12–13):992–01.
   PubMed Web of Science ®Google Scholar
• Wang R, Zhong Y, Gu X, et al. The pathogenesis, detection, and prevention of Vibrio parahaemolyticus. Front Microbiol. 2015;6:144.
   PubMed Web of Science ®Google Scholar
• Merchant SS, Helmann JD. Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation. Adv Microb Physiol. 2012;60:91–210.
   PubMed Web of Science ®Google Scholar
• Lam LN, Brunson DN, Molina JJ, et al. The AdcACB/AdcAII system is essential for zinc homeostasis and an important contributor of Enterococcus faecalis virulence. Virulence. 2022;13(1):592–08. DOI:10.1080/21505594.2022.2056965
   PubMed Web of Science ®Google Scholar
• Plumptre CD, Eijkelkamp BA, Morey JR, et al. AdcA and AdcAII employ distinct zinc acquisition mechanisms and contribute additively to zinc homeostasis in Streptococcus pneumoniae. Mol Microbiol. 2014;91(4):834–851. DOI:10.1111/mmi.12504
   PubMed Web of Science ®Google Scholar
• Bayle L, Chimalapati S, Schoehn G, et al. Zinc uptake by Streptococcus pneumoniae depends on both AdcA and AdcAII and is essential for normal bacterial morphology and virulence. Mol Microbiol. 2011;82(4):904–916. DOI:10.1111/j.1365-2958.2011.07862.x
   PubMed Web of Science ®Google Scholar
• Pan Y, Chen Y, Chen J, et al. The adc regulon mediates zinc homeostasis in Streptococcus mutans. Mol Oral Microbiol. 2021;36(5):278–290. DOI:10.1111/omi.12350
   PubMed Web of Science ®Google Scholar
• Makthal N, Do H, Wendel BM, et al. Group a Streptococcus AdcR regulon participates in bacterial defense against host-mediated zinc sequestration and contributes to virulence. Infect Immun. 2020;88(8):e00097–20. DOI:10.1128/IAI.00097-20
   PubMed Web of Science ®Google Scholar
• Ganguly T, Peterson AM, Kajfasz JK, et al. Zinc import mediated by AdcABC is critical for colonization of the dental biofilm by Streptococcus mutans in an animal model. Mol Oral Microbiol. 2021;36(3):214–224. DOI:10.1111/omi.12337
   PubMed Web of Science ®Google Scholar
• Moreau GB, Qin A, Mann BJ. Zinc acquisition mechanisms differ between environmental and virulent Francisella species. J Bacteriol. 2018;200(4):e00587–17.
   PubMed Web of Science ®Google Scholar
• Nielubowicz GR, Smith SN, Mobley HL. Zinc uptake contributes to motility and provides a competitive advantage to Proteus mirabilis during experimental urinary tract infection. Infect Immun. 2010;78(6):2823–2833.
   PubMed Web of Science ®Google Scholar
• Ammendola S, D’Amico Y, Chirullo B, et al. Zinc is required to ensure the expression of flagella and the ability to form biofilms in. Salmonella enterica sv Typhimurium. Metallomics. 2016;8(10):1131–1140. DOI:10.1039/C6MT00108D
   PubMed Web of Science ®Google Scholar
• Desrosiers DC, Bearden SW, Mier I, et al. Znu is the predominant zinc importer in Yersinia pestis during in vitro growth but is not essential for virulence. Infect Immun. 2010;78(12):5163–5177. DOI:10.1128/IAI.00732-10
   PubMed Web of Science ®Google Scholar
• McDevitt CA, Ogunniyi AD, Valkov E, et al. A molecular mechanism for bacterial susceptibility to zinc. PLOS Pathogens. 2011;7(11):e1002357. DOI:10.1371/journal.ppat.1002357
   PubMed Web of Science ®Google Scholar
• Livny J, Zhou XH, Mandlik A, et al. Comparative RNA-Seq based dissection of the regulatory networks and environmental stimuli underlying Vibrio parahaemolyticus gene expression during infection. Nucleic Acids Res. 2014;42(19):12212–12223. DOI:10.1093/nar/gku891
   PubMed Web of Science ®Google Scholar
• Choi S, Bird AJ. Zinc’ing sensibly: controlling zinc homeostasis at the transcriptional level. Metallomics. 2014;6(7):1198–15.
   PubMed Web of Science ®Google Scholar
• Kandari D, Joshi H, Bhatnagar R. Zur: zinc-sensing transcriptional regulator in a diverse set of bacterial species. Pathogens. 2021;10(3):344.
   PubMed Web of Science ®Google Scholar