{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T23:00:11Z","timestamp":1790031611410,"version":"4.0.1"},"reference-count":67,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,10,26]],"date-time":"2023-10-26T00:00:00Z","timestamp":1698278400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p><jats:italic>Vibrio cholerae<\/jats:italic> is a common waterborne pathogen that can cause pandemic cholera in humans. The bacterium with heavy metal-tolerant phenotypes is frequently isolated from aquatic products, however, its tolerance mechanisms remain unclear. In this study, we investigated for the first time the response of such <jats:italic>V. cholerae<\/jats:italic> isolates (<jats:italic>n<\/jats:italic>\u2009=\u20093) toward the heavy metal (Cd<jats:sup>2+<\/jats:sup>, Ni<jats:sup>2+<\/jats:sup>, Pb<jats:sup>2+<\/jats:sup>, and Zn<jats:sup>2+<\/jats:sup>) stresses by comparative secretomic and proteomic analyses. The results showed that sublethal concentrations of the Pb<jats:sup>2+<\/jats:sup> (200\u2009\u03bcg\/mL), Cd<jats:sup>2+<\/jats:sup> (12.5\u2009\u03bcg\/mL), and Zn<jats:sup>2+<\/jats:sup> (50\u2009\u03bcg\/mL) stresses for 2\u2009h significantly decreased the bacterial cell membrane fluidity, but increased cell surface hydrophobicity and inner membrane permeability, whereas the Ni<jats:sup>2+<\/jats:sup> (50\u2009\u03bcg\/mL) stress increased cell membrane fluidity (<jats:italic>p<\/jats:italic>\u2009&amp;lt;\u20090.05). The comparative secretomic and proteomic analysis revealed differentially expressed extracellular and intracellular proteins involved in common metabolic pathways in the <jats:italic>V. cholerae<\/jats:italic> isolates to reduce cytotoxicity of the heavy metal stresses, such as biosorption, transportation and effluxing, extracellular sequestration, and intracellular antioxidative defense. Meanwhile, different defensive strategies were also found in the <jats:italic>V. cholerae<\/jats:italic> isolates to cope with different heavy metal damage. Remarkably, a number of putative virulence and resistance-associated proteins were produced and\/or secreted by the <jats:italic>V. cholerae<\/jats:italic> isolates under the heavy metal stresses, suggesting an increased health risk in the aquatic products.<\/jats:p>","DOI":"10.3389\/fmicb.2023.1294177","type":"journal-article","created":{"date-parts":[[2023,10,26]],"date-time":"2023-10-26T13:33:48Z","timestamp":1698327228000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":16,"title":["Comparative secretomic and proteomic analysis reveal multiple defensive strategies developed by Vibrio cholerae against the heavy metal (Cd2+, Ni2+, Pb2+, and Zn2+) stresses"],"prefix":"10.3389","volume":"14","author":[{"given":"Beiyu","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingjing","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meng","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pan","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuming","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lu","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lanming","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,10,26]]},"reference":[{"key":"ref1","first-page":"489","article-title":"Trace elements and toxic heavy metals play a role in Buerger disease and atherosclerotic peripheral arterial occlusive disease","volume":"29","author":"Arslan","year":"2010","journal-title":"Int. Angiol."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"959","DOI":"10.1080\/15320383.2022.2028719","article-title":"Does the long-term contamination of lead (PbII) affect the bioremediation mechanisms of Microbacterium oxydans strain CM3 and CM7?","volume":"31","author":"Ashrafi","year":"2022","journal-title":"Soil Sediment Contamin."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41572-018-0005-8","article-title":"Vibrio spp. infections","volume":"4","author":"Baker-Austin","year":"2018","journal-title":"Nat. Rev. Dis. Primers."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1016\/j.jphotobiol.2018.03.002","article-title":"Evaluation of membrane fluidity of multidrug-resistant isolates of Escherichia coli and Staphylococcus aureus in presence and absence of antibiotics","volume":"181","author":"Bessa","year":"2018","journal-title":"J. Photochem. Photobiol. B"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/s0162-3109(99)00115-0","article-title":"Kininergic system and arterial hypertension following chronic exposure to inorganic lead","volume":"44","author":"Carmignani","year":"1999","journal-title":"Immunopharmacology"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"412","DOI":"10.3390\/antibiotics10040412","article-title":"First experimental evidence for the presence of potentially toxic Vibrio cholerae in snails, and virulence, cross-resistance and genetic diversity of the bacterium in 36 species of aquatic food animals","volume":"10","author":"Chen","year":"2021","journal-title":"Antibiotics"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"e0221521","DOI":"10.1128\/aem.02215-21","article-title":"Transcriptome analysis on key metabolic pathways in Rhodotorula mucilaginosa under Pb(II) stress","volume":"88","author":"Chen","year":"2022","journal-title":"Appl. Environ. Microbiol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"4112","DOI":"10.1111\/1462-2920.14976","article-title":"The Vibrio cholerae type VI secretion system: toxins, regulators and consequences","volume":"22","author":"Crisan","year":"2020","journal-title":"Environ. Microbiol."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"e0153322","DOI":"10.1128\/spectrum.01533-22","article-title":"An important role of the type VI secretion system of Pseudomonas aeruginosa regulated by Dnr in response to anaerobic en-vironments","volume":"10","author":"Dang","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"A83","DOI":"10.1016\/j.vaccine.2019.06.031","article-title":"Antibiotic resistance in Vibrio cholerae: understanding the ecology of resistance genes and mechanisms","volume":"38","author":"Das","year":"2020","journal-title":"Vaccine"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"1205","DOI":"10.3390\/ijms24021205","article-title":"Taurine alleviates cadmium-induced hepatotoxicity by regulating autophagy flux","volume":"24","author":"Duan","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"100905","DOI":"10.1016\/j.drup.2022.100905","article-title":"ABC transporters affects tumor immune microenvironment to regulate cancer immunotherapy and multidrug resistance","volume":"66","author":"Fan","year":"2023","journal-title":"Drug Resist. Updat."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"128935","DOI":"10.1016\/j.jhazmat.2022.128935","article-title":"Resistance properties and adaptation mechanism of cadmium in an enriched strain, Cupriavidus nantongensis X1(T)","volume":"434","author":"Fang","year":"2022","journal-title":"J. Hazard. Mater."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"1526","DOI":"10.1089\/mdr.2020.0269","article-title":"Virulence, resistance, and genomic fingerprint traits of Vibrio cholerae isolated from 12 species of aquatic products in Shang-hai, China","volume":"26","author":"Fu","year":"2020","journal-title":"Microb. Drug Resist."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"3782","DOI":"10.3390\/ijerph17113782","article-title":"The effects of cadmium toxicity","volume":"17","author":"Genchi","year":"2020","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"4059","DOI":"10.3390\/ijerph17114059","article-title":"Sorption mechanism and optimization study for the bioremediation of Pb(II) and cd(II) contamination by two novel isolat-ed strains Q3 and Q5 of Bacillus sp","volume":"17","author":"Heidari","year":"2020","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"104357","DOI":"10.1016\/j.micpath.2020.104357","article-title":"BaeSR activates type VI secretion system expression in porcine extra-intestinal pathogenic Escherichia coli to enhance bacterial resistance to zinc stress","volume":"147","author":"Hu","year":"2020","journal-title":"Microb. Pathog."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1016\/j.ecoenv.2019.06.027","article-title":"The cytotoxicities in prokaryote and eukaryote varied for CdSe and CdSe\/ZnS quantum dots and differed from cadmium ions","volume":"181","author":"Hu","year":"2019","journal-title":"Ecotoxicol. Approximately. Saf."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"128805","DOI":"10.1016\/j.cej.2021.128805","article-title":"Rapid bacteria capturing and killing by AgNPs\/N-CD@ZnO hybrids strengthened photo-responsive xerogel for rapid healing of bacteria-infected wounds","volume":"414","author":"Huang","year":"2021","journal-title":"Chem. Eng. J."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"4609","DOI":"10.1021\/acs.est.8b06787","article-title":"Multiple transcriptional mechanisms collectively mediate copper resistance in Cupriavidus gilardii CR3","volume":"53","author":"Huang","year":"2019","journal-title":"Environ. Sci. Technol."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1099\/mic.0.070284-0","article-title":"Lead resistance in micro-organisms","volume":"160","author":"Jaros\u0142awiecka","year":"2014","journal-title":"Microbiology"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"e0012121","DOI":"10.1128\/iai.00121-21","article-title":"Salmonella typhimurium adhesin OmpV activates host immunity to confer protection against systemic and gastrointestinal infection in mice","volume":"89","author":"Kaur","year":"2021","journal-title":"Infect. Immun."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"e1009881","DOI":"10.1371\/journal.ppat.1009881","article-title":"PASTA kinase-dependent control of peptidoglycan synthesis via ReoM is required for cell wall stress responses, cytosolic survival, and virulence in Listeria monocytogenes","volume":"17","author":"Kelliher","year":"2021","journal-title":"PLoS Pathog."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"165","DOI":"10.3390\/pathogens10020165","article-title":"The minimum inhibitory concentration of antibiotics: methods, interpretation, clinical relevance","volume":"10","author":"Kowalska-Krochmal","year":"2021","journal-title":"Pathogens"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"37434","DOI":"10.1038\/srep37434","article-title":"Metabolic response induced by parasitic plant-fungus interactions hinder amino sugar and nucleotide sugar metabolism in the host","volume":"6","author":"Lee","year":"2016","journal-title":"Sci. Rep."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"4346","DOI":"10.1038\/s41598-019-39554-y","article-title":"Small-molecule inhibitor of HlyU attenuates virulence of Vibrio species","volume":"9","author":"Lee","year":"2019","journal-title":"Sci. Rep."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1007\/s11274-020-02900-8","article-title":"Biochemical pathways to \u03b1-ketoglutarate, a multi-faceted metabolite","volume":"36","author":"Legendre","year":"2020","journal-title":"World J. Microbiol. Biotechnol."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.jhazmat.2019.02.006","article-title":"Sub-lethal concentrations of heavy metals induce antibiotic resistance via mutagenesis","volume":"369","author":"Li","year":"2019","journal-title":"J. Hazard. Mater."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"2918","DOI":"10.3390\/foods11182912","article-title":"Stress response mechanisms of Salmonella enteritidis to sodium hypochlorite at the proteomic level","volume":"11","author":"Li","year":"2022","journal-title":"Foods"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"1057284","DOI":"10.3389\/fmicb.2022.1057284","article-title":"Protective effects of thiamine on Wickerhamomyces anomalus against ethanol stress","volume":"13","author":"Li","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.micres.2018.06.006","article-title":"Secretome analysis of alkaliphilic bacterium Bacillus lehensis G1 in response to pH changes","volume":"215","author":"Ling","year":"2018","journal-title":"Microbiol. Res."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1039\/c8mt00374b","article-title":"Designating ligand specificities to metal uptake ABC transporters in Thermus thermophilus HB8","volume":"11","author":"Mandal","year":"2019","journal-title":"Metallomics"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"14271","DOI":"10.1007\/s11356-021-12583-9","article-title":"Bacterial tolerance strategies against lead toxicity and their relevance in bioremediation application","volume":"28","author":"Mitra","year":"2021","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"110694","DOI":"10.1016\/j.ecoenv.2020.110694","article-title":"Dynamic proteomic analysis of Phanerochaete chrysosporium under copper stress","volume":"198","author":"Okay","year":"2020","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"639582","DOI":"10.3389\/fmicb.2021.639582","article-title":"Peptidoglycan-binding anchor is a Pseudomonas aeruginosa OmpA family lipoprotein with importance for outer membrane vesicles, biofilms, and the periplasmic shape","volume":"12","author":"Paulsson","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"mfab015","DOI":"10.1093\/mtomcs\/mfab015","article-title":"Glutathione-coordinated metal complexes as substrates for cellular transporters","volume":"13","author":"Pearson","year":"2021","journal-title":"Metallomics"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"3718","DOI":"10.1016\/j.bpj.2021.07.016","article-title":"Membrane hydrophobicity determines the activation free energy of passive lipid transport","volume":"120","author":"Rogers","year":"2021","journal-title":"Biophys. J."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00244-018-0555-5","article-title":"The chronic effects of copper and cadmium on life history traits across Cladocera species: a meta-analysis","volume":"76","author":"Sadeq","year":"2019","journal-title":"Arch. Environ. Contam. Toxicol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"1946","DOI":"10.3390\/healthcare11131946","article-title":"Antimicrobial resistance: a growing serious threat for global public health","volume":"11","author":"Salamm","year":"2023","journal-title":"Healthcare"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"2002","DOI":"10.3390\/microorganisms10102002","article-title":"Proteomic study of response to copper, cadmium, and chrome ion stress in Yarrowia lipolytica strains isolated from andean mine tailings in Peru","volume":"10","author":"S\u00e1nchez-Rojas","year":"2022","journal-title":"Microorganisms"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"104408","DOI":"10.1016\/j.jprot.2021.104408","article-title":"Comparative proteomics and secretomics revealed virulence, and coresistance-related factors in non O1\/O139 Vibrio cholerae recovered from 16 species of consumable aquatic animals","volume":"251","author":"Shan","year":"2022","journal-title":"J. Proteome"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.mib.2021.09.007","article-title":"Animal models for dissecting Vibrio cholerae intestinal pathogenesis and immunity","volume":"65","author":"Sit","year":"2022","journal-title":"Curr. Opin. Microbiol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"115214","DOI":"10.1016\/j.ecoenv.2023.115214","article-title":"The regulatory metabolic networks of the Brassica campestris L. hairy roots in response to cadmium stress revealed from proteome studies combined with a transcriptome analysis","volume":"263","author":"Sun","year":"2023","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"3488","DOI":"10.3390\/cells11213488","article-title":"Concentration-dependent global quantitative proteome response of Staphylococcus epidermidis RP62A biofilms to subinhibi-tory tigecycline","volume":"11","author":"Sung","year":"2022","journal-title":"Cells"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"106892","DOI":"10.1016\/j.envint.2021.106892","article-title":"Current and future threats to human health in the anthropocene","volume":"158","author":"Tong","year":"2022","journal-title":"Env. Int."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.scitotenv.2012.05.026","article-title":"Compost as a source of microbial isolates for the bioremediation of heavy metals: in vitro selection","volume":"431","author":"Vargas-Garc\u00eda Mdel","year":"2012","journal-title":"Sci. Total Environ."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1016\/j.mimet.2013.11.009","article-title":"1,6-Diphenyl-1,3,5-hexatrine as a reporter of inner spore membrane fluidity in Bacillus subtilis and Alicyclobacillus acidoterrestris","volume":"96","author":"Voss","year":"2014","journal-title":"J. Microbiol. Methods"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"108957","DOI":"10.1016\/j.celrep.2021.108957","article-title":"Pseudomonas aeruginosa T6SS-mediated molybdate transport contributes to bacterial competition during anaerobiosis","volume":"35","author":"Wang","year":"2021","journal-title":"Cell Rep."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"2055440","DOI":"10.1080\/19490976.2022.2055440","article-title":"Type VI secretion system-associated FHA domain protein TagH regulates the hemolytic activity and virulence of Vibrio cholerae","volume":"14","author":"Wang","year":"2022","journal-title":"Gut Microbes"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"5699","DOI":"10.1007\/s00253-019-09885-x","article-title":"YKL107W from Saccharomyces cerevisiae encodes a novel aldehyde reductase for detoxification of acetaldehyde, glycolaldehyde, and furfural","volume":"103","author":"Wang","year":"2019","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"16125","DOI":"10.3390\/ijerph192316125","article-title":"Water quality criteria and ecological risk assessment of typical transition metals in South Asia","volume":"19","author":"Wang","year":"2022","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"22708","DOI":"10.1007\/s11356-020-08685-5","article-title":"Heavy metals in aquatic products and the health risk assessment to population in China","volume":"27","author":"Wang","year":"2020","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"4964","DOI":"10.3390\/ijerph20064964","article-title":"Bioremediation of heavy metals by the genus Bacillus","volume":"20","author":"Wr\u00f3bel","year":"2023","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"747421","DOI":"10.3389\/fmicb.2021.747421","article-title":"Nicotinamide adenine dinucleotide-dependent flavin oxidoreductase of Mycoplasma hyopneumoniae functions as a potential novel virulence factor and not only as a metabolic enzyme","volume":"12","author":"Xie","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"27338","DOI":"10.1007\/s11356-019-05287-8","article-title":"Virulence, antimicrobial and heavy metal tolerance, and genetic diversity of Vibrio cholerae recovered from commonly consumed freshwater fish","volume":"26","author":"Xu","year":"2019","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1016\/j.carbpol.2016.04.098","article-title":"3,6-O-[N-(2-Aminoethyl)-acetamideyl]-chitosan exerts antibacterial activity by a membrane damage mechanism","volume":"149","author":"Yan","year":"2016","journal-title":"Carbohydr. Polym."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"896767","DOI":"10.3389\/fmicb.2022.896767","article-title":"Diverse aquatic animal matrices play a key role in survival and potential virulence of non-O1\/O139 Vibrio cholerae isolates","volume":"13","author":"Yan","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"595709","DOI":"10.3389\/fcimb.2020.595709","article-title":"Prophage-related gene VpaChn25_0724 contributes to cell membrane integrity and growth of Vibrio parahaemolyticus CHN25","volume":"10","author":"Yang","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"115049","DOI":"10.1016\/j.ecoenv.2023.115049","article-title":"Autophagy-mediated ferroptosis involved in nickel-induced nephrotoxicity in the mice","volume":"259","author":"Yang","year":"2023","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1186\/s12866-020-1705-2","article-title":"An operon consisting of a P-type ATPase gene and a transcriptional regulator gene responsible for cadmium resistances in Bacillus vietamensis 151-6 and Bacillus marisflavi 151-25","volume":"20","author":"Yu","year":"2020","journal-title":"BMC Microbiol."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"3777","DOI":"10.3390\/foods11233777","article-title":"Genomic and transcriptomic analysis reveal multiple strategies for the cadmium tolerance in Vibrio parahaemolyticus N10-18 isolated from aquatic animal ostrea gigas thunberg","volume":"11","author":"Yu","year":"2022","journal-title":"Foods"},{"key":"ref62","doi-asserted-by":"publisher","first-page":"15435","DOI":"10.3390\/ijerph192315435","article-title":"Spatial distribution, source analysis and health risk study of heavy metals in the Liujiang River basin in different seasons","volume":"19","author":"Yu","year":"2022","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"101504","DOI":"10.1016\/j.eti.2021.101504","article-title":"Heavy metal water pollution: a fresh look about hazards, novel and conventional remediation methods","volume":"22","author":"Zamora-Ledezma","year":"2021","journal-title":"Environ. Technol. Innov."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"102179","DOI":"10.1016\/j.mib.2022.102179","article-title":"Making sense of drug-efflux transporters in the physiological environment","volume":"69","author":"Zgurskaya","year":"2022","journal-title":"Curr. Opin. Microbiol."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1080\/15226514.2022.2092064","article-title":"Enolase, a cadmium resistance related protein from hyperaccumulator plant Phytolacca americana, increase the tolerance of Escherichia coli to cadmium stress","volume":"25","author":"Zhao","year":"2023","journal-title":"Int. J. Phytoremediation"},{"key":"ref66","doi-asserted-by":"publisher","first-page":"124962","DOI":"10.1016\/j.jhazmat.2020.124962","article-title":"Can heavy metal pollution induce bacterial resistance to heavy metals and antibiotics in soils from an ancient land-mine?","volume":"411","author":"Zhong","year":"2021","journal-title":"J. Hazard. Mater."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"1453","DOI":"10.3389\/fmicb.2020.01453","article-title":"Comparative proteomics and secretomics revealed virulence and antibiotic resistance-associated factors in Vibrio parahaemolyticus recovered from commonly consumed aquatic products","volume":"11","author":"Zhu","year":"2020","journal-title":"Front. Microbiol."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1294177\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,26]],"date-time":"2023-10-26T13:33:51Z","timestamp":1698327231000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1294177\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,26]]},"references-count":67,"alternative-id":["10.3389\/fmicb.2023.1294177"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2023.1294177","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,26]]},"article-number":"1294177"}}