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Research Paper

ZntA maintains zinc and cadmium homeostasis and promotes oxidative stress resistance and virulence in Vibrio parahaemolyticus

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Article: 2327377 | Received 08 Oct 2023, Accepted 04 Mar 2024, Published online: 11 Mar 2024

References

  • Turner AG, Ong CY, Walker MJ, Djoko, KY, McEwan, AG. Transition metal homeostasis in Streptococcus pyogenes and streptococcus pneumoniae. Adv Microb Physiol. 2017;70:123–17 doi:10.1016/bs.ampbs.2017.01.002.
  • Begg SL. The role of metal ions in the virulence and viability of bacterial pathogens. Biochem Soc Trans. 2019;47(1):77–87. doi:10.1042/BST20180275.
  • Hood MI, Skaar EP. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol. 2012;10(8):525–537. doi:10.1038/nrmicro2836.
  • Price SL, Vadyvaloo V, DeMarco JK, Brady A, Gray PA, Kehl-Fie TE, Garneau-Tsodikova S, Perry RD, Lawrenz MB. Yersiniabactin contributes to overcoming zinc restriction during Yersinia pestis infection of mammalian and insect hosts. Proc Natl Acad Sci U S A. 2021;118(44):e2104073118. doi:10.1073/pnas.2104073118.
  • Chandrangsu P, Rensing C, Helmann JD. Metal homeostasis and resistance in bacteria. Nat Rev Microbiol. 2017;15(6):338–350. doi:10.1038/nrmicro.2017.15.
  • Akbari MS, Doran KS, Burcham LR. Metal homeostasis in pathogenic Streptococci. Microorganisms. 2022;10(8):1501. doi:10.3390/microorganisms10081501.
  • Murdoch CC, Skaar EP. Nutritional immunity: the battle for nutrient metals at the host-pathogen interface. Nat Rev Microbiol. 2022;20(11):657–670. doi:10.1038/s41579-022-00745-6.
  • Baker-Austin C, Oliver JD, Alam M, Ali A, Waldor MK, Qadri F, Martinez-Urtaza J. Vibrio spp. infections. Nat Rev Dis Primers. 2018;4(1):1–19. doi:10.1038/s41572-018-0005-8.
  • Martinez-Urtaza J, Baker-Austin C. Vibrio parahaemolyticus. Trends Microbiol. 2020;28(10):867–868. doi:10.1016/j.tim.2020.02.008.
  • Broberg CA, Calder TJ, Orth K. Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect. 2011;13(12–13):992–1001. doi:10.1016/j.micinf.2011.06.013.
  • Ghenem L, Elhadi N, Alzahrani F, Nishibuchi M. 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.
  • Paudyal N, Pan H, Liao X, Zhang X, Li X, Fang W, Yue M. 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.
  • Liu J, Bai L, Li W, Han H, Fu P, Ma X, Bi Z, Yang X, Zhang X, Zhen S. et al. Trends of foodborne diseases in China: lessons from laboratory-based surveillance since 2011. Front Med. 2018;12(1):48–57. doi:10.1007/s11684-017-0608-6.
  • Lee CT, Chen IT, Yang YT, Ko T-P, Huang Y-T, Huang J-Y, Huang M-F, Lin S-J, Chen C-Y, Lin S-S. et al. The opportunistic marine pathogen Vibrio parahaemolyticus becomes virulent by acquiring a plasmid that expresses a deadly toxin. Proc Natl Acad Sci U S A. 2015;112(34):10798–803. doi:10.1073/pnas.1503129112.
  • Chandran A, Priya PS, Meenatchi R, Vaishnavi S, Pavithra V, Ajith Kumar TT, Arockiaraj J. Insights into molecular aspects of pathogenesis and disease management in acute hepatopancreatic necrosis disease (AHPND): an updated review. Fish Shellfish Immunol. 2023;142:109138. doi:10.1016/j.fsi.2023.109138.
  • Kumar V, Roy S, Behera BK, Bossier P, Das BK. Acute hepatopancreatic necrosis disease (AHPND): Virulence, pathogenesis and mitigation strategies in shrimp aquaculture. Toxins. 2021;13(8):524. doi:10.3390/toxins13080524.
  • Karunasagar I, Joseph SW, Twedt RM, Hada H, Colwell RR. 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.
  • Gode-Potratz CJ, Chodur DM, McCarter LL. Calcium and iron regulate swarming and type III secretion in Vibrio parahaemolyticus. J Bacteriol. 2010;192(22):6025–38. doi:10.1128/JB.00654-10.
  • Jiao L, Dai T, Zhong S, Jin M, Sun P, Zhou Q. Vibrio parahaemolyticus infection influenced trace element homeostasis, impaired antioxidant function, and induced inflammation response in Litopenaeus vannamei. Biol Trace Elem Res. 2021;199(1):329–337. doi:10.1007/s12011-020-02120-z.
  • León-Sicairos N, Angulo-Zamudio UA, de la Garza M, Velázquez-Román J, Flores-Villaseñor HM, Canizalez-Román A. Strategies of Vibrio parahaemolyticus to acquire nutritional iron during host colonization. Front Microbiol. 2015;6:702. doi:10.3389/fmicb.2015.00702.
  • Liu M, Yan M, Liu L, Chen S. Characterization of a novel zinc transporter ZnuA acquired by Vibrio parahaemolyticus through horizontal gene transfer. Front Cell Infect Microbiol. 2013;3:61. doi:10.3389/fcimb.2013.00061.
  • Zhao Y, Kong M, Yang J, Zhao X, Shi Y, Zhai Y, Qiu J, Zheng C. The DmeRF system is involved in maintaining cobalt homeostasis in Vibrio parahaemolyticus. Int J Mol Sci. 2022;24(1):414. doi:10.3390/ijms24010414.
  • Zheng C, Qiu J, Zhai Y, Wei M, Zhou X, Jiao X. ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus. Virulence. 2023;14(1):2156196. doi:10.1080/21505594.2022.2156196.
  • Rensing C, Mitra B, Rosen BP. The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc Natl Acad Sci U S A. 1997;94(26):14326–31. doi:10.1073/pnas.94.26.14326.
  • Wang K, Sitsel O, Meloni G, Autzen HE, Andersson M, Klymchuk T, Nielsen AM, Rees DC, Nissen P, Gourdon P. et al. Structure and mechanism of Zn2+–transporting P-type ATPases. Nature. 2014;514(7523):518–22. doi:10.1038/nature13618.
  • Maunders EA, Ganio K, Hayes AJ, Neville SL, Davies MR, Strugnell RA, McDevitt CA, Tan A. The role of ZntA in Klebsiella pneumoniae zinc homeostasis. Microbiol Spectr. 2022;10(1):e0177321. doi:10.1128/spectrum.01773-21.
  • Karash S, Jiang T, Kwon YM. Genome-wide characterization of salmonella typhimurium genes required for the fitness under iron restriction. BMC Genom Data. 2022;23(1):55. doi:10.1186/s12863-022-01069-3.
  • Turner AG, Ong CL, Gillen CM, Davies MR, West NP, McEwan AG, Walker MJ. Manganese homeostasis in group a streptococcus is critical for resistance to oxidative stress and virulence. mBio. 2015;6(2):00278–15. doi:10.1128/mBio.00278-15.
  • Chaoprasid P, Nookabkaew S, Sukchawalit R, Mongkolsuk S. Roles of Agrobacterium tumefaciens C58 ZntA and ZntB and the transcriptional regulator ZntR in controlling Cd2+/Zn2+/Co2+ resistance and the peroxide stress response. Microbiology. 2015;161(9):1730–1740. doi:10.1099/mic.0.000135.
  • Suryawati B. Zinc homeostasis mechanism and its role in bacterial virulence capacity. AIP Conf Proc. 2018;2021:070021 doi:10.1063/1.5062819.
  • Brocklehurst KR, Hobman JL, Lawley B, Blank L, Marshall SJ, Brown NL, Morby AP. ZntR is a Zn(II)-responsive MerR-like transcriptional regulator of zntA in Escherichia coli. Mol Microbiol. 1999;31(3):893–902. doi:10.1046/j.1365-2958.1999.01229.x.
  • Outten CE, Outten FW, O’Halloran TV. DNA distortion mechanism for transcriptional activation by ZntR, a Zn(II)-responsive MerR homologue in Escherichia coli. J Biol Chem. 1999;274(53):37517–24. doi:10.1074/jbc.274.53.37517.
  • Wang D, Hosteen O, Fierke CA. ZntR-mediated transcription of zntA responds to nanomolar intracellular free zinc. J Inorg Biochem. 2012;111:173–81. doi:10.1016/j.jinorgbio.2012.02.008.
  • Singh VK, Xiong A, Usgaard TR, Chakrabarti S, Deora R, Misra TK, Jayaswal RK. ZntR is an autoregulatory protein and negatively regulates the chromosomal zinc resistance operon znt of Staphylococcus aureus. Mol Microbiol. 1999;33(1):200–207. doi:10.1046/j.1365-2958.1999.01466.x.
  • Xiong J, Li D, Li H, He M, Miller SJ, Yu L, Rensing C, Wang G. Genome analysis and characterization of zinc efflux systems of a highly zinc-resistant bacterium, Comamonas testosteroni S44. Res Microbiol. 2011;162(7):671–679. doi:10.1016/j.resmic.2011.06.002.
  • Sheehan LM, Budnick JA, Roop RM 2nd, Caswell CC. Coordinated zinc homeostasis is essential for the wild-type virulence of Brucella abortus. J Bacteriol. 2015;197(9):1582–1591. doi:10.1128/JB.02543-14.
  • Schulz V, Schmidt-Vogler C, Strohmeyer P, Weber S, Kleemann D, Nies DH, Herzberg M. Behind the shield of czc: ZntR controls expression of the gene for the zinc-exporting P-type ATPase ZntA in cupriavidus metallidurans. J Bacteriol. 2021;203(11):e00052–21. doi:10.1128/JB.00052-21.
  • Andreini C, Banci L, Bertini I, Rosato A. Zinc through the three domains of life. J Proteome Res. 2006;5(11):3173–3178. doi:10.1021/pr0603699.
  • Lonergan ZR, Skaar EP. Nutrient zinc at the Host-Pathogen Interface. Trends Biochem Sci. 2019;44(12):1041–1056. doi:10.1016/j.tibs.2019.06.010.
  • Li Z, Song X, Wang J, Bai X, Gao E, Wei G. Nickel and cobalt resistance properties of Sinorhizobium meliloti isolated from Medicago lupulina growing in gold mine tailing. PeerJ. 2018;6:e5202. doi:10.7717/peerj.5202.
  • Zheng C, Jia M, Gao M, Lu T, Li L, Zhou P. PmtA functions as a ferrous iron and cobalt efflux pump in Streptococcus suis. Emerg Microbes Infect. 2019;8(1):1254–1264. doi:10.1080/22221751.2019.1660233.
  • Xu Z, Wang P, Wang H, Yu ZH, Au-Yeung HY, Hirayama T, Sun H, Yan A. Zinc excess increases cellular demand for iron and decreases tolerance to copper in Escherichia coli. J Biol Chem. 2019;294(45):16978–16991. doi:10.1074/jbc.RA119.010023.
  • Zheng C, Wei M, Qiu J, Jia M, Zhou X, Jiao X. TroR negatively regulates the TroABCD system and is required for resistance to metal toxicity and virulence in streptococcus suis. Appl Environ Microbiol. 2021;87(20):e0137521. doi:10.1128/AEM.01375-21.
  • Turner AG, Ong CY, Djoko KY, West NP, Davies MR, McEwan AG, Walker MJ. The PerR-regulated P1B-4-Type ATPase (PmtA) acts as a ferrous iron efflux pump in Streptococcus pyogenes. Infect Immun. 2017;85(6):e00140–17. doi:10.1128/IAI.00140-17.
  • Guan G, Pinochet-Barros A, Gaballa A, Patel SJ, Argüello JM, Helmann JD. PfeT, a P1B4-type ATPase, effluxes ferrous iron and protects Bacillus subtilis against iron intoxication. Mol Microbiol. 2015;98(4):787–803. doi:10.1111/mmi.13158.
  • Gaballa A, Helmann JD. A peroxide-induced zinc uptake system plays an important role in protection against oxidative stress in Bacillus subtilis. Mol Microbiol. 2002;45(4):997–1005. doi:10.1046/j.1365-2958.2002.03068.x.
  • Cerasi M, Liu JZ, Ammendola S, Poe AJ, Petrarca P, Pesciaroli M, Pasquali P, Raffatellu M, Battistoni A. The ZupT transporter plays an important role in zinc homeostasis and contributes to Salmonella enterica virulence. Metallomics. 2014;6(4):845–853. doi:10.1039/C3MT00352C.
  • Brenot A, Weston BF, Caparon MG. A PerR-regulated metal transporter (PmtA) is an interface between oxidative stress and metal homeostasis in Streptococcus pyogenes. Mol Microbiol. 2007;63(4):1185–96. doi:10.1111/j.1365-2958.2006.05577.x.
  • Ganguly T, Peterson AM, Burkholder M, Kajfasz JK, Abranches J, Lemos JA. ZccE is a novel P-type ATPase that protects Streptococcus mutans against zinc intoxication. PloS Pathog. 2022;18(8):e1010477. doi:10.1371/journal.ppat.1010477.
  • Ong CL, Gillen CM, Barnett TC, Walker MJ, McEwan AG. An antimicrobial role for zinc in innate immune defense against Group A Streptococcus. J Infect Dis. 2014;209(10):1500–1508. doi:10.1093/infdis/jiu053.
  • Sullivan MJ, Goh KGK, Ulett GC, Johnson MDL. Cellular management of zinc in group B streptococcus supports bacterial resistance against metal intoxication and promotes disseminated infection. mSphere. 2021;6(3):e00105–21. doi:10.1128/mSphere.00105-21.
  • Chen L, Li X, Xu P, He Z-G. A novel zinc exporter CtpG enhances resistance to zinc toxicity and survival in Mycobacterium bovis. Microbiol Spectr. 2022;10(2):e0145621. doi:10.1128/spectrum.01456-21.
  • Huang K, Wang D, Frederiksen RF, Rensing C, Olsen JE, Fresno AH. Investigation of the role of genes encoding zinc exporters zntA, zitB, and fieF during Salmonella Typhimurium infection. Front Microbiol. 2017;8:2656. doi:10.3389/fmicb.2017.02656.
  • Paranjpye RN, Myers MS, Yount EC, Thompson JL. Zebrafish as a model for Vibrio parahaemolyticus virulence. Microbiol. 2013;159(Pt_12):2605–2615. doi:10.1099/mic.0.067637-0.
  • Zhang Q, Dong X, Chen B, Zhang Y, Zu Y, Li W. Zebrafish as a useful model for zoonotic Vibrio parahaemolyticus pathogenicity in fish and human. Dev Comp Immunol. 2016;55:159–168. doi:10.1016/j.dci.2015.10.021.
  • Nag D, Farr DA, Walton MG, Withey JH. Zebrafish models for pathogenic Vibrios. J Bacteriol. 2020;202(24):e00165–20. doi:10.1128/JB.00165-20.
  • Zhong X, Lu Z, Wang F, Yao N, Shi M, Yang M. Characterization of GefA, a GGEEF domain-containing protein that modulates Vibrio parahaemolyticus motility, biofilm formation, and virulence. Appl Environ Microbiol. 2022;88(6):e0223921. doi:10.1128/aem.02239-21.
  • Wu CQ, Zhang T, Zhang W, Shi M, Tu F, Yu A, Li M, Yang M. Two DsbA proteins are important for Vibrio parahaemolyticus pathogenesis. Front Microbiol. 2019;10:1103. doi:10.3389/fmicb.2019.01103.
  • Bobrov AG, Kirillina O, Fosso MY, Fetherston JD, Miller MC, VanCleave TT, Burlison JA, Arnold WK, Lawrenz MB, Garneau-Tsodikova S. 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.
  • Milton DL, O’Toole R, Horstedt P, Wolf-Watz H. 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.
  • Chimalapati S, Lafrance AE, Chen L, Orth K. Vibrio parahaemolyticus: basic techniques for growth, genetic manipulation, and analysis of virulence factors. Curr Protoc Microbiol. 2020;59(1):e131. doi:10.1002/cpmc.131.
  • 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. doi:10.1016/0378-1119(91)90007-X.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262.
  • Novichkov PS, Kazakov AE, Ravcheev DA, Leyn SA, Kovaleva GY, Sutormin RA, Kazanov MD, Riehl W, Arkin AP, Dubchak I. 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.
  • Croxatto A, Chalker VJ, Lauritz J, Jass J, Hardman A, Williams P, Camara M, Milton DL. 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.