Abstract
The marine bacteria of the Vibrionaceae family are significant from the point of view of their role in the marine geochemical cycle, as well as symbionts and opportunistic pathogens of aquatic animals and humans. The well-known pathogens of this group, Vibrio cholerae, V. parahaemolyticus, and V. vulnificus, are responsible for significant morbidity and mortality associated with a range of infections from gastroenteritis to bacteremia acquired through the consumption of raw or undercooked seafood and exposure to seawater containing these pathogens. Although generally regarded as susceptible to commonly employed antibiotics, the antimicrobial resistance of Vibrio spp. has been on the rise in the last two decades, which has raised concern about future infections by these bacteria becoming increasingly challenging to treat. Diverse mechanisms of antimicrobial resistance have been discovered in pathogenic vibrios, the most important being the membrane efflux pumps, which contribute to antimicrobial resistance and their virulence, environmental fitness, and persistence through biofilm formation and quorum sensing. In this review, we discuss the evolution of antimicrobial resistance in pathogenic vibrios and some of the well-characterized efflux pumps’ contributions to the physiology of antimicrobial resistance, host and environment survival, and their pathogenicity.
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References
Abd El-Rahman OA, Rasslan F, Hassan SS et al (2023) The RND efflux pump gene expression in the biofilm formation of Acinetobacter baumannii. Antibiotics 12:419. https://doi.org/10.3390/antibiotics12020419
Ahmed HA, El Bayomi RM, Hussein MA et al (2018) Molecular characterization, antibiotic resistance pattern and biofilm formation of Vibrio parahaemolyticus and V. cholerae isolated from crustaceans and humans. Int J Food Microbiol 274:31–37. https://doi.org/10.1016/j.ijfoodmicro.2018.03.013
Alatoom AA, Aburto R, Hamood AN, Colmer-Hamood JA (2007) VceR negatively regulates the vceCAB MDR efflux operon and positively regulates its own synthesis in Vibrio cholerae 569B. Can J Microbiol 53:888–900. https://doi.org/10.1139/W07-054
Albert MJ, Siddique AK, Islam MS et al (1993) Large outbreak of clinical cholera due to Vibrio cholerae non-O1 in Bangladesh. Lancet 341:704. https://doi.org/10.1016/0140-6736(93)90481-u
Ali M, Nelson AR, Lopez AL, Sack DA (2015) Updated global burden of cholera in Endemic Countries. PLoS Negl Trop Dis 9:e0003832. https://doi.org/10.1371/journal.pntd.0003832
Alvarez-Ortega C, Olivares J, Martínez JL (2013) RND multidrug efflux pumps: what are they good for? Front Microbiol 4:7. https://doi.org/10.3389/fmicb.2013.00007
Archer EJ, Baker-Austin C, Osborn TJ et al (2023) Climate warming and increasing Vibrio vulnificus infections in North America. Sci Rep 13:3893. https://doi.org/10.1038/s41598-023-28247-2
Ayyappan MV, Balange AK, Nayak BB, Kumar S (2018) Distribution of potentially pathogenic Vibrio parahaemolyticus in seafood and the aquatic environment of Mumbai, India. Fish Technol 55:205–211
Bag PK, Bhowmik P, Hajra TK et al (2008) Putative virulence traits and pathogenicity of Vibrio cholerae Non-O1, Non-O139 isolates from surface waters in Kolkata, India. Appl Environ Microbiol 74:5635–5644. https://doi.org/10.1128/AEM.00029-08
Bai J, Mosley L, Fralick JA (2010) Evidence that the C-terminus of OprM is involved in the assembly of the VceAB-OprM efflux pump. FEBS Lett 584:1493–1497. https://doi.org/10.1016/j.febslet.2010.02.066
Baker-Austin C, McArthur JV, Lindell AH et al (2009) Multi-site analysis reveals widespread antibiotic resistance in the marine pathogen Vibrio vulnificus. Microb Ecol 57:151–159. https://doi.org/10.1007/s00248-008-9413-8
Baker-Austin C, Oliver JD, Alam M et al (2018) Vibrio spp. infections. Nat Rev Dis Primers 4:8. https://doi.org/10.1038/s41572-018-0005-8
Bassler BL, Wright M, Showalter RE, Silverman MR (1993) Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9:773–786. https://doi.org/10.1111/j.1365-2958.1993.tb01737.x
Begum A, Rahman MM, Ogawa W et al (2005) Gene cloning and characterization of four MATE family multidrug efflux pumps from Vibrio cholerae non-O1. Microbiol Immunol 49:949–957. https://doi.org/10.1111/j.1348-0421.2005.tb03690.x
Bhattacharya K, Kanungo S, Sur D et al (2011) Tetracycline-resistant Vibrio cholerae O1, Kolkata, India. Emerg Infect Dis 17:568–569. https://doi.org/10.3201/eid1703.101176
Bina XR, Bina JE (2023) Vibrio cholerae RND efflux systems: mediators of stress responses, colonization and pathogenesis. Front Cell Infect Microbiol 13:1203487. https://doi.org/10.3389/fcimb.2023.1203487
Bina JE, Provenzano D, Wang C et al (2006) Characterization of the Vibrio cholerae vexAB and vexCD efflux systems. Arch Microbiol 186:171–181. https://doi.org/10.1007/s00203-006-0133-5
Bina XR, Provenzano D, Nguyen N, Bina JE (2008) Vibrio cholerae RND family efflux systems are required for antimicrobial resistance, optimal virulence factor production, and colonization of the infant mouse small intestine. Infect Immun 76:3595–3605. https://doi.org/10.1128/IAI.01620-07
Bina XR, Howard MF, Taylor-Mulneix DL et al (2018) The Vibrio cholerae RND efflux systems impact virulence factor production and adaptive responses via periplasmic sensor proteins. PLoS Pathog 14:e1006804. https://doi.org/10.1371/journal.ppat.1006804
Blevins SM, Bronze MS (2010) Robert Koch and the ‘golden age’ of bacteriology. Int J Infect Dis 14:e744–e751. https://doi.org/10.1016/j.ijid.2009.12.003
Bonnin-Jusserand M, Copin S, Le Bris C et al (2019) Vibrio species involved in seafood-borne outbreaks (Vibrio cholerae, V. parahaemolyticus and V. vulnificus): review of microbiological versus recent molecular detection methods in seafood products. Crit Rev Food Sci Nutr 59:597–610. https://doi.org/10.1080/10408398.2017.1384715
Briet A, Helsens N, Delannoy S et al (2018) NDM-1-producing Vibrio parahaemolyticus isolated from imported seafood. J Antimicrob Chemother 73:2578–2579. https://doi.org/10.1093/jac/dky200
Bross MH, Soch K, Morales R, Mitchell RB (2007) Vibrio vulnificus infection: diagnosis and treatment. AFP 76:539–544
Brown MH, Paulsen IT, Skurray RA (1999) The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol 31:394–395. https://doi.org/10.1046/j.1365-2958.1999.01162.x
Bruns MM, Kakarla P, Floyd JT et al (2017) Modulation of the multidrug efflux pump EmrD-3 from Vibrio cholerae by Allium sativum extract and the bioactive agent allyl sulfide plus synergistic enhancement of antimicrobial susceptibility by A. sativum extract. Arch Microbiol 199:1103–1112. https://doi.org/10.1007/s00203-017-1378-x
Burse A, Weingart H, Ullrich MS (2004) NorM, an Erwinia amylovora multidrug efflux pump involved in in vitro competition with other epiphytic bacteria. Appl Environ Microbiol 70:693–703. https://doi.org/10.1128/AEM.70.2.693-703.2004
Castellano S, Claxton DP, Ficici E et al (2021) Conserved binding site in the N-lobe of prokaryotic MATE transporters suggests a role for Na+ in ion-coupled drug efflux. J Biol Chem 296:100262. https://doi.org/10.1016/j.jbc.2021.100262
CDC (2023) General Information, Cholera. https://www.cdc.gov/cholera/general/index.html. Accessed 13 Aug 2023
Ceccarelli D, Salvia AM, Sami J, Cappuccinelli P, Colombo MM (2006) New cluster of plasmid-located class 1 integrons in Vibrio cholerae O1 and a dfrA15 cassette-containing integron in Vibrio parahaemolyticus isolated in Angola. Antimicrob Agents Chemother 50(7):2493–2499
Ceccarelli D, Chen A, Hasan NA et al (2015) Non-O1/Non-O139 Vibrio cholerae carrying multiple virulence factors and V. cholerae O1 in the Chesapeake Bay Maryland. Appl Environ Microbiol 81:1909–1918. https://doi.org/10.1128/AEM.03540-14
Chakraborty S, Nair GB, Shinoda S (1997) Pathogenic vibrios in the natural aquatic environment. Rev Environ Health 12:63–80. https://doi.org/10.1515/REVEH.1997.12.2.63
Chang G (2003) Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation. J Mol Biol 330:419–430. https://doi.org/10.1016/s0022-2836(03)00587-4
Changsen C, Likhitrattanapisal S, Lunha K et al (2023) Incidence, genetic diversity, and antimicrobial resistance profiles of Vibrio parahaemolyticus in seafood in Bangkok and eastern Thailand. PeerJ 11:e15283. https://doi.org/10.7717/peerj.15283
Chatterjee P, Kanungo S, Bhattacharya SK, Dutta S (2020) Mapping cholera outbreaks and antibiotic resistant Vibrio cholerae in India: an assessment of existing data and a scoping review of the literature. Vaccine 38:A93–A104. https://doi.org/10.1016/j.vaccine.2019.12.003
Chen S, Wang H, Katzianer DS et al (2013) LysR family activator-regulated major facilitator superfamily transporters are involved in Vibrio cholerae antimicrobial compound resistance and intestinal colonisation. Int J Antimicrob Agents 41:188–192. https://doi.org/10.1016/j.ijantimicag.2012.10.008
Chen Y-T, Tang H-J, Chao C-M, Lai C-C (2015) Clinical manifestations of non-O1 Vibrio cholerae infections. PLoS ONE 10:e0116904. https://doi.org/10.1371/journal.pone.0116904
Chen X, Li Y, Yao W et al (2020) A new emerging serotype of Vibrio parahaemolyticus in China is rapidly becoming the main epidemic strain. Clin Microbiol Infect 26:644.e1-644.e7. https://doi.org/10.1016/j.cmi.2019.09.024
Chowdhury NR, Stine OC, Morris JG, Nair GB (2004) Assessment of evolution of pandemic Vibrio parahaemolyticus by multilocus sequence typing. J Clin Microbiol 42:1280–1282. https://doi.org/10.1128/jcm.42.3.1280-1282.2004
Claxton DP, Jagessar KL, Mchaourab HS (2021) Principles of alternating access in multidrug and toxin extrusion (MATE) transporters. J Mol Biol 433:166959. https://doi.org/10.1016/j.jmb.2021.166959
Colmer JA, Fralick JA, Hamood AN (1998) Isolation and characterization of a putative multidrug resistance pump from Vibrio cholerae. Mol Microbiol 27:63–72. https://doi.org/10.1046/j.1365-2958.1998.00657.x
Colwell RR (2000) Viable but nonculturable bacteria: a survival strategy. J Infect Chemother 6:121–125. https://doi.org/10.1007/PL00012151
Colwell RR, Kaper J, Joseph SW (1977) Vibrio cholerae, Vibrio parahaemolyticus, and other vibrios: occurrence and distribution in Chesapeake Bay. Science 198:394–396
Costa WF, Giambiagi-deMarval M, Laport MS (2021) Antibiotic and heavy metal susceptibility of non-cholera Vibrio isolated from Marine Sponges and Sea Urchins: could they pose a potential risk to public health? Antibiotics (Basel) 10:1561. https://doi.org/10.3390/antibiotics10121561
Coutinho FH, Tschoeke DA, Clementino MM et al (2019) Genomic basis of antibiotic resistance in Vibrio parahaemolyticus strain JPA1. Mem Inst Oswaldo Cruz 114:e190053. https://doi.org/10.1590/0074-02760190053
Cutugno L, Mc Cafferty J, Pané-Farré J et al (2020) rpoB mutations conferring rifampicin-resistance affect growth, stress response and motility in Vibrio vulnificus. Microbiology (Reading) 166:1160–1170. https://doi.org/10.1099/mic.0.000991
da Silva LV, Ossai S, Chigbu P, Parveen S (2021) Antimicrobial and genetic profiles of Vibrio vulnificus and Vibrio parahaemolyticus isolated From the Maryland Coastal Bays. United States Front Microbiol 12:676249. https://doi.org/10.3389/fmicb.2021.676249
Dahanayake PS, Hossain S, Wickramanayake MVKS et al (2020) Manila clam (Ruditapes philippinarum) marketed in Korea as a source of vibrios harbouring virulence and β-lactam resistance genes. Lett Appl Microbiol 71:46–53. https://doi.org/10.1111/lam.13229
Dalsgaard A, Forslund A, Petersen A et al (2000) Class 1 integron-borne, multiple-antibiotic resistance encoded by a 150-kilobase conjugative plasmid in epidemic Vibrio cholerae O1 strains isolated in Guinea-Bissau. J Clin Microbiol 38:3774–3779. https://doi.org/10.1128/JCM.38.10.3774-3779.2000
Das B, Verma J, Kumar P et al (2020) Antibiotic resistance in Vibrio cholerae: understanding the ecology of resistance genes and mechanisms. Vaccine 38(Suppl 1):A83–A92. https://doi.org/10.1016/j.vaccine.2019.06.031
Dawan J, Li Y, Lu F et al (2022) Role of efflux pump-mediated antibiotic resistance in quorum sensing-regulated biofilm formation by Salmonella typhimurium. Pathogens 11:147. https://doi.org/10.3390/pathogens11020147
De Jesus M, Jin J, Guffanti AA, Krulwich TA (2005) Importance of the GP dipeptide of the antiporter motif and other membrane-embedded proline and glycine residues in tetracycline efflux protein Tet(L). Biochemistry 44:12896–12904. https://doi.org/10.1021/bi050762c
Deen J, Mengel MA, Clemens JD (2020) Epidemiology of cholera. Vaccine 38:A31–A40. https://doi.org/10.1016/j.vaccine.2019.07.078
Deepanjali A, Kumar HS, Karunasagar I (2005) Seasonal variation in abundance of total and pathogenic Vibrio parahaemolyticus bacteria in oysters along the southwest coast of India. Appl Environ Microbiol 71:3575–3580. https://doi.org/10.1128/AEM.71.7.3575-3580.2005
Delmar JA, Su CC, Yu EW (2014) Bacterial multidrug efflux transporters. Annu Rev Biophys 43:93–117. https://doi.org/10.1146/annurev-biophys-051013-022855
Dengo-Baloi LC, Semá-Baltazar CA, Manhique LV et al (2017) Antibiotics resistance in El Tor Vibrio cholerae 01 isolated during cholera outbreaks in Mozambique from 2012 to 2015. PLoS ONE 12:e0181496. https://doi.org/10.1371/journal.pone.0181496
DePaola A, Nordstrom JL, Bowers JC et al (2003) Seasonal abundance of total and pathogenic Vibrio parahaemolyticus in Alabama oysters. Appl Environ Microbiol 69:1521–1526
Deshayes S, Daurel C, Cattoir V et al (2015) Non-O1, non-O139 Vibrio cholerae bacteraemia: case report and literature review. Springerplus 4:575. https://doi.org/10.1186/s40064-015-1346-3
Destoumieux-Garzón D, Duperthuy M, Vanhove AS et al (2014) Resistance to antimicrobial peptides in vibrios. Antibiotics (basel) 3:540–563. https://doi.org/10.3390/antibiotics3040540
Dhakne P, Pillai M, Mishra S et al (2023) Refinement of safety and efficacy of anti-cancer chemotherapeutics by tailoring their site-specific intracellular bioavailability through transporter modulation. Biochim Biophys Acta 1878:188906. https://doi.org/10.1016/j.bbcan.2023.188906
Du D, Wang-Kan X, Neuberger A et al (2018) Multidrug efflux pumps: structure, function and regulation. Nat Rev Microbiol 16:523–539. https://doi.org/10.1038/s41579-018-0048-6
Dubon JM, Palmer CJ, Ager AL et al (1997) Emergence of multiple drug-resistant Vibrio cholerae O1 in San Pedro Sula. Honduras Lancet 349:924. https://doi.org/10.1016/s0140-6736(05)62699-2
Dutta D, Chowdhury G, Pazhani GP et al (2013) Vibrio cholerae non-O1, non-o139 serogroups and cholera-like diarrhea, Kolkata, India. Emerg Infect Dis 19:464–467. https://doi.org/10.3201/eid1903.121156
Dutta D, Kaushik A, Kumar D, Bag S (2021) Foodborne pathogenic vibrios: antimicrobial resistance. Front Microbiol 12:638331. https://doi.org/10.3389/fmicb.2021.638331
ECDC (2023) Cholera worldwide overview. https://www.ecdc.europa.eu/en/all-topics-z/cholera/surveillance-and-disease-data/cholera-monthly. Accessed 14 Aug 2023
Elmahdi S, DaSilva LV, Parveen S (2016) Antibiotic resistance of Vibrio parahaemolyticus and Vibrio vulnificus in various countries: a review. Food Microbiol 57:128–134. https://doi.org/10.1016/j.fm.2016.02.008
Evans K, Passador L, Srikumar R et al (1998) Influence of the MexAB-OprM multidrug efflux system on quorum sensing in Pseudomonas aeruginosa. J Bacteriol 180:5443–5447
Faruque SM, Kamruzzaman M, Meraj IM et al (2003a) Pathogenic potential of environmental Vibrio cholerae strains carrying genetic variants of the toxin-coregulated pilus pathogenicity Island. Infect Immun 71:1020–1025. https://doi.org/10.1128/IAI.71.2.1020-1025.2003
Faruque SM, Sack DA, Sack RB et al (2003b) Emergence and evolution of Vibrio cholerae O139. Proc Natl Acad Sci U S A 100:1304–1309. https://doi.org/10.1073/pnas.0337468100
Fernández-Vélez I, Bidegain G, Ben-Horin T (2023) Predicting the growth of Vibrio parahaemolyticus in oysters under varying ambient temperature. Microorganisms 11:1169. https://doi.org/10.3390/microorganisms11051169
Ghenem L, Elhadi N, Alzahrani F, Nishibuchi M (2017) Vibrio parahaemolyticus: a review on distribution, pathogenesis, virulence determinants and epidemiology. Saudi J Med Med Sci 5:93–103. https://doi.org/10.4103/sjmms.sjmms_30_17
Ginn SL, Brown MH, Skurray RA (2000) The TetA (K) tetracycline/H+ antiporter from Staphylococcus aureus: mutagenesis and functional analysis of motif C. J Bacteriol 182:1492–1498
Gladkikh AS, Feranchuk SI, Ponomareva AS et al (2020) Antibiotic resistance in Vibrio cholerae El Tor strains isolated during cholera complications in Siberia and the Far East of Russia. Infect Genet Evol 78:104096. https://doi.org/10.1016/j.meegid.2019.104096
Glass RI, Huq I, Alim AR, Yunus M (1980) Emergence of multiply antibiotic-resistant Vibrio cholerae in Bangladesh. J Infect Dis 142:939–942. https://doi.org/10.1093/infdis/142.6.939
Griffith JK, Baker ME, Rouch DA et al (1992) Membrane transport proteins: implications of sequence comparisons. Curr Opin Cell Biol 4:684–695. https://doi.org/10.1016/0955-0674(92)90090-y
Griffith JK, Cuellar DH, Fordyce CA et al (1994) Structure and function of the class C tetracycline/H+ antiporter: three independent groups of phenotypes are conferred by TetA (C). Mol Membr Biol 11:271–277. https://doi.org/10.3109/09687689409160437
Grudlewska-Buda K, Bauza-Kaszewska J, Wiktorczyk-Kapischke N et al (2023) Antibiotic resistance in selected emerging bacterial foodborne pathogens-an issue of concern? Antibiotics (basel) 12:880. https://doi.org/10.3390/antibiotics12050880
Guillaume Y, Ternier R, Vissieres K et al (2018) Responding to cholera in Haiti: implications for the national plan to eliminate cholera by 2022. J Infect Dis 218:S167–S170. https://doi.org/10.1093/infdis/jiy491
Gulig PA, Bourdage KL, Starks AM (2005) Molecular pathogenesis of Vibrio vulnificus. J Microbiol 43:118–131
Hammer BK, Bassler BL (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50:101–104
Han F, Walker RD, Janes ME et al (2007) Antimicrobial susceptibilities of Vibrio parahaemolyticus and Vibrio vulnificus isolates from Louisiana Gulf and retail raw Oysters. Appl Environ Microbiol 73:7096–7098. https://doi.org/10.1128/AEM.01116-07
Hao Y, Wang Y, Bi Z et al (2015) A case of non-O1/non-O139 Vibrio cholerae septicemia and meningitis in a neonate. Int J Infect Dis 35:117–119. https://doi.org/10.1016/j.ijid.2015.05.004
Harris JB, LaRocque RC, Qadri F et al (2012) Cholera. Lancet 379:2466–2476. https://doi.org/10.1016/S0140-6736(12)60436-X
Hassan KA, Galea M, Wu J et al (2006) Functional effects of intramembranous proline substitutions in the staphylococcal multidrug transporter QacA. FEMS Microbiol Lett 263:76–85
Hassan KA, Maher C, Elbourne LD et al (2021) Increasing the PACE of characterising novel transporters by functional genomics. Curr Opin Microbiol 64:1–8. https://doi.org/10.1016/j.mib.2021.08.005
He G-X, Kuroda T, Mima T et al (2004) An H+-coupled multidrug efflux pump, PmpM, a member of the MATE family of transporters, from Pseudomonas aeruginosa. J Bacteriol 186:262–265. https://doi.org/10.1128/JB.186.1.262-265.2004
He X, Szewczyk P, Karyakin A et al (2010) Structure of a cation-bound multidrug and toxic compound extrusion transporter. Nature 467:991–994. https://doi.org/10.1038/nature09408
Hedges RW, Jacob AE (1975) A 98 megadalton R factor of compatibility group C in a Vibrio cholerae El Tor isolate from Southern U.S.S.R. Microbiology 89:383–386. https://doi.org/10.1099/00221287-89-2-383
Heidelberg JF, Eisen JA, Nelson WC et al (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477–483. https://doi.org/10.1038/35020000
Henderson PJ (1990) The homologous glucose transport proteins of prokaryotes and eukaryotes. Res Microbiol 141:316–328. https://doi.org/10.1016/0923-2508(90)90005-b
Henderson PJ (1993) The 12-transmembrane helix transporters. Curr Opin Cell Biol 5:708–721. https://doi.org/10.1016/0955-0674(93)90144-f
Heng S-P, Letchumanan V, Deng C-Y et al (2017) Vibrio vulnificus: an environmental and clinical burden. Front Microbiol. https://doi.org/10.3389/fmicb.2017.00997
Higgins DA, Pomianek ME, Kraml CM et al (2007) The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450:883–886
Hirota D, Sachdev A, Thrupp L et al (2010) Traumatic arm wound infected with Vibrio cholerae in a non-immunocompromised Host. https://www.hmpgloballearningnetwork.com/site/wounds/case-report-and-brief-review/traumatic-arm-wound-infected-vibrio-cholerae-non. Accessed 9 Oct 2023
Hong To TT, Yanagawa H, Khanh Thuan N et al (2020) Prevalence of Vibrio parahaemolyticus causing acute hepatopancreatic necrosis disease of shrimp in shrimp, Molluscan shellfish and water samples in the Mekong Delta, Vietnam. Biology 9:312. https://doi.org/10.3390/biology9100312
HongYou C, LiHong T, Min C et al (2014) Investigation of diversity of Vibrio parahaemolyticus in molluscs. Dis Surveill 29:522–527
Horseman MA, Surani S (2011) A comprehensive review of Vibrio vulnificus: an important cause of severe sepsis and skin and soft-tissue infection. Int J Infect Dis 15:e157–e166. https://doi.org/10.1016/j.ijid.2010.11.003
Hossain S, Wickramanayake MVKS, Dahanayake PS, Heo GJ (2020) Occurrence of virulence and extended-spectrum β-lactamase determinants in Vibrio spp. isolated from marketed hard-shelled mussel (Mytilus coruscus). Microb Drug Resist 26:391–401. https://doi.org/10.1089/mdr.2019.0131
Hou Z, Gangjee A, Matherly LH (2022) The evolving biology of the proton-coupled folate transporter: new insights into regulation, structure, and mechanism. FASEB J 36:e22164. https://doi.org/10.1096/fj.202101704R
Hounmanou YMG, Engberg J, Bjerre KD, et al (2023) Correlation of high seawater temperature with Vibrio and Shewanella infections, Denmark, 2010–2018 - Volume 29, Number 3—March 2023 - Emerg Infect Dis J CDC. https://doi.org/10.3201/eid2903.221568
Huda MN, Chen J, Morita Y et al (2003) Gene cloning and characterization of VcrM, a Na+-coupled multidrug efflux pump, from Vibrio cholerae non-O1. Microbiol Immunol 47:419–427. https://doi.org/10.1111/j.1348-0421.2003.tb03379.x
Huq A, Colwell RR (1996) A microbiological paradox: viable but nonculturable bacteria with special reference to Vibrio cholerae. J Food Prot 59:96–101. https://doi.org/10.4315/0362-028X-59.1.96
Hvorup RN, Winnen B, Chang AB et al (2003) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem 270:799–813
Ichinose Y, Ehara M, Watanabe S et al (1986) The characterization of Vibrio cholerae isolated in Kenya in 1983. J Trop Med Hyg 89:269–276
Ingelbeen B, Hendrickx D, Miwanda B et al (2019) Recurrent cholera outbreaks, Democratic Republic of the Congo, 2008–2017. Emerg Infect Dis 25:856
Jack DL, Yang NM, Saier MH Jr (2001) The drug/metabolite transporter superfamily. Eur J Biochem 268:3620–3639
Jain M, Kumar P, Goel AK (2016) Emergence of tetracycline resistant Vibrio cholerae O1 Biotype El Tor serotype Ogawa with classical ctxB gene from a cholera outbreak in Odisha, Eastern India. J Pathog 2016:1695410. https://doi.org/10.1155/2016/1695410
Jiang D, Zhao Y, Wang X et al (2013) Structure of the YajR transporter suggests a transport mechanism based on the conserved motif A. Proc Natl Acad Sci USA 110:14664–14669. https://doi.org/10.1073/pnas.1308127110
Jin J, Krulwich TA (2002) Site-directed mutagenesis studies of selected motif and charged residues and of cysteines of the multifunctional tetracycline efflux protein Tet(L). J Bacteriol 184:1796–1800. https://doi.org/10.1128/jb.184.6.1796-1800.2002
Jin Y, Nair A, van Veen HW (2014) Multidrug transport protein NorM from Vibrio cholerae simultaneously couples to sodium- and proton-motive force. J Biol Chem 289:14624–14632. https://doi.org/10.1074/jbc.M113.546770
Jones MK, Oliver JD (2009) Vibrio vulnificus: disease and pathogenesis. Infect Immun 77:1723–1733. https://doi.org/10.1128/IAI.01046-08
Kakarla P, Floyd J, Mukherjee M et al (2017) Inhibition of the multidrug efflux pump LmrS from Staphylococcus aureus by cumin spice Cuminum cyminum. Arch Microbiol 199:465–474. https://doi.org/10.1007/s00203-016-1314-5
Kaper JB, Morris JG, Levine MM (1995) Cholera. Clin Microbiol Rev 8:48–86
Kathleen MM, Samuel L, Felecia C, et al (2016) Antibiotic resistance of diverse bacteria from aquaculture in Borneo. Int J Microbiol 2016:2164761. https://www.hindawi.com/journals/ijmicro/2016/2164761/.
Kazama H, Hamashima H, Sasatsu M, Arai T (1999) Characterization of the antiseptic-resistance gene qacEΔ1 isolated from clinical and environmental isolates of Vibrio parahaemolyticus and Vibrio cholerae non-O1. FEMS Microbiol Lett 174(2):379–384
Kitaoka M, Miyata ST, Unterweger D, Pukatzki S (2011) Antibiotic resistance mechanisms of Vibrio cholerae. J Med Microbiol 60:397–407. https://doi.org/10.1099/jmm.0.023051-0
Konishi S, Iwaki S, Kimura-Someya T, Yamaguchi A (1999) Cysteine-scanning mutagenesis around transmembrane segment VI of Tn10-encoded metal-tetracycline/H(+) antiporter. FEBS Lett 461:315–318. https://doi.org/10.1016/s0014-5793(99)01490-8
Kumar S, He G, Kakarla P et al (2016a) Bacterial multidrug efflux pumps of the major facilitator superfamily as targets for modulation. Infect Disord Drug Targets 16:28–43. https://doi.org/10.2174/1871526516666160407113848
Kumar S, Ranjana K, Sanford LM et al (2016b) Structural and functional roles of two evolutionarily conserved amino acid sequence motifs within solute transporters of the major facilitator superfamily. Trends Cell Mol Biol 11:41–53
Kumar S, Lindquist IE, Sundararajan A et al (2013a) Genome sequence of non-O1 Vibrio cholerae PS15. Genome Announc. https://doi.org/10.1128/genomeA.00227-12
Kumar S, Mukherjee MM, Varela MF (2013b) Modulation of bacterial multidrug resistance efflux pumps of the major facilitator superfamily. Int J Bacteriol 2013:204141. https://doi.org/10.1155/2013/204141
Kumar S, Lekshmi M, Parvathi A et al (2017) Antibiotic resistance in seafood-borne pathogens. In: Foodborne pathogens and antibiotic resistance. Wiley, pp 397–415. https://doi.org/10.1002/9781119139188.ch17
Kumar S, Lekshmi M, Parvathi A et al (2020) Functional and structural roles of the major facilitator superfamily bacterial multidrug efflux pumps. Microorganisms 8:266. https://doi.org/10.3390/microorganisms8020266
Kunkle DE, Bina XR, Bina JE (2017) The Vibrio cholerae VexGH RND efflux system maintains cellular homeostasis by effluxing Vibriobactin. Mbio. https://doi.org/10.1128/mBio.00126-17
Kuroda T, Tsuchiya T (2009) Multidrug efflux transporters in the MATE family. Biochim Biophys Acta 1794(5):763–768. https://doi.org/10.1016/j.bbapap.2008.11.012
Kusakizako T, Miyauchi H, Ishitani R, Nureki O (2020) Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochim Et Biophys Acta BBA Biomembr 1862:183154. https://doi.org/10.1016/j.bbamem.2019.183154
Kuwahara S, Goto S, Kimura M, Abe H (1967) Drug-sensitivity of El Tor vibrio strains isolated in the Philippines in 1964 and 1965. Bull World Health Organ 37:763–771
Lee S, Yeom J-H, Seo S et al (2015) Functional analysis of Vibrio vulnificus RND efflux pumps homologous to Vibrio cholerae VexAB and VexCD, and to Escherichia coli AcrAB. J Microbiol 53:256–261. https://doi.org/10.1007/s12275-015-5037-0
Lee L-H, Ab Mutalib N-S, Law JW-F et al (2018) Discovery on antibiotic resistance patterns of Vibrio parahaemolyticus in selangor reveals carbapenemase producing Vibrio parahaemolyticus in marine and freshwater fish. Front Microbiol 9:2513. https://doi.org/10.3389/fmicb.2018.02513
Lei T, Zhang J, Jiang F et al (2019) First detection of the plasmid-mediated colistin resistance gene mcr-1 in virulent Vibrio parahaemolyticus. Int J Food Microbiol 308:108290. https://doi.org/10.1016/j.ijfoodmicro.2019.108290
Lei T, Jiang F, He M et al (2020) Prevalence, virulence, antimicrobial resistance, and molecular characterization of fluoroquinolone resistance of Vibrio parahaemolyticus from different types of food samples in China. Int J Food Microbiol 317:108461. https://doi.org/10.1016/j.ijfoodmicro.2019.108461
Lekshmi M, Ammini P, Kumar S, Varela MF (2017) The food production environment and the development of antimicrobial resistance in human pathogens of animal origin. Microorganisms. https://doi.org/10.3390/microorganisms5010011
Letchumanan V, Yin W-F, Lee L-H, Chan K-G (2015) Prevalence and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from retail shrimps in Malaysia. Front Microbiol 6:33. https://doi.org/10.3389/fmicb.2015.00033
Li G, Wang M-Y (2020) The role of Vibrio vulnificus virulence factors and regulators in its infection-induced sepsis. Folia Microbiol (praha) 65:265–274. https://doi.org/10.1007/s12223-019-00763-7
Lipp EK, Huq A, Colwell RR (2002) Effects of global climate on infectious disease: the cholera model. Clin Microbiol Rev 15:757–770. https://doi.org/10.1128/CMR.15.4.757-770.2002
Liu P, Zhang X, Wang Q et al (2022) Biological and transcriptional studies reveal VmeL is involved in motility, biofilm formation and virulence in Vibrio parahaemolyticus. Front Microbiol 13:976334
Lloyd NA, Nazaret S, Barkay T (2019) Genome-facilitated discovery of RND efflux pump-mediated resistance to cephalosporins in Vibrio spp. isolated from the mummichog fish gut. J Glob Antimicrob Resist 19:294–300
Lo C-C, Lin P-T, Chiang-Ni C et al (2017) Contribution of efflux systems to the detergent resistance, cytotoxicity, and biofilm formation of Vibrio vulnificus. Gene Rep 9:115–122. https://doi.org/10.1016/j.genrep.2017.09.004
Lomovskaya O, Lewis K (1992) Emr, an Escherichia coli locus for multidrug resistance. Proc Natl Acad Sci USA 89:8938–8942. https://doi.org/10.1073/pnas.89.19.8938
Loo KY, Letchumanan V, Law JWF et al (2020) Incidence of antibiotic resistance in Vibrio spp. Rev Aquac 12:2590–2608. https://doi.org/10.1111/raq.12460
Lu M, Symersky J, Radchenko M et al (2013) Structures of a Na+-coupled, substrate-bound MATE multidrug transporter. Proc Natl Acad Sci USA 110:2099–2104. https://doi.org/10.1073/pnas.1219901110
Lu W-J, Lin H-J, Janganan TK et al (2018) ATP-binding cassette transporter VcaM from Vibrio cholerae is dependent on the outer membrane factor family for its function. Int J Mol Sci 19:E1000. https://doi.org/10.3390/ijms19041000
Luo J, Parsons SM (2010) Conformational propensities of peptides mimicking transmembrane Helix 5 and Motif C in wild-type and mutant vesicular acetylcholine transporters. ACS Chem Neurosci 1:381–390. https://doi.org/10.1021/cn900033s
Maddocks SE, Oyston PCF (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology (reading) 154:3609–3623. https://doi.org/10.1099/mic.0.2008/022772-0
Maiden MC, Davis EO, Baldwin SA et al (1987) Mammalian and bacterial sugar transport proteins are homologous. Nature 325:641–643
Mandal A, Sengupta A, Kumar A et al (2017) Molecular epidemiology of extended-spectrum β-lactamase–producing Escherichia coli pathotypes in diarrheal children from low socioeconomic status communities in Bihar, India: emergence of the CTX-M Type. Infect Dis (auckl) 10:1178633617739018. https://doi.org/10.1177/1178633617739018
Manjusha S, Sarita GB (2011) Plasmid associated antibiotic resistance in Vibrios isolated from coastal waters of Kerala. Int Food Res J 18:1171–1181
Marinello S, Marini G, Parisi G et al (2017) Vibrio cholerae non-O1, non-O139 bacteraemia associated with pneumonia, Italy 2016. Infection 45:237–240. https://doi.org/10.1007/s15010-016-0961-4
Martínez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367
Maseda H, Sawada I, Saito K et al (2004) Enhancement of the mexAB-oprM efflux pump expression by a quorum-sensing autoinducer and its cancellation by a regulator, MexT, of the mexEF-oprN efflux pump operon in Pseudomonas aeruginosa. Antimicrob Agents Chemother 48:1320–1328. https://doi.org/10.1128/aac.48.4.1320-1328.2004
Masureel M, Martens C, Stein RA et al (2014) Protonation drives the conformational switch in the multidrug transporter LmrP. Nat Chem Biol 10:149–155. https://doi.org/10.1038/nchembio.1408
Matsumoto C, Okuda J, Ishibashi M et al (2000) Pandemic spread of an O3:K6 clone of Vibrio parahaemolyticus and emergence of related strains evidenced by arbitrarily primed PCR and toxRS sequence analyses. J Clin Microbiol 38:578–585
Matsuo T, Hayashi K, Morita Y et al (2007) VmeAB, an RND-type multidrug efflux transporter in Vibrio parahaemolyticus. Microbiology 153:4129–4137. https://doi.org/10.1099/mic.0.2007/009597-0
Matsuo T, Nakamura K, Kodama T et al (2013) Characterization of all RND-type multidrug efflux transporters in Vibrio parahaemolyticus. MicrobiologyOpen 2:725–742. https://doi.org/10.1002/mbo3.100
McMurry L, Petrucci RE Jr, Levy BS (1980) Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. Proc Natl Acad Sci 77:3974–3977
Meng X, Huang D, Zhou Q et al (2023) The influence of outer membrane protein on ampicillin resistance of Vibrio parahaemolyticus. Can J Infect Dis Med Microbiol 2023:8079091. https://doi.org/10.1155/2023/8079091
Mevada V, Patel R, Dudhagara P et al (2023) Whole genome sequencing and pan-genomic analysis of multidrug-resistant Vibrio cholerae VC01 isolated from a clinical sample. Microorganisms 11:2030. https://doi.org/10.3390/microorganisms11082030
Miyamae S, Ueda O, Yoshimura F, Hwang J, Tanaka Y, Nikaido H (2001) A MATE family multidrug efflux transporter pumps out fluoroquinolones in Bacteroides thetaiotaomicron. Antimicrob Agents Chemother 45(12):3341–3346. https://doi.org/10.1128/aac.45.12.3341-3346.2001
Mohanty P, Patel A, Bhardwaj AK (2012) Role of H- and D- MATE-type transporters from multidrug resistant clinical isolates of Vibrio fluvialis in conferring fluoroquinolone resistance. PLoS ONE 7:e35752. https://doi.org/10.1371/journal.pone.0035752
Mohanty P, Shah A, Bhardwaj AK (2021) Functional insights of two MATE transporters from Vibrio fluvialis. bioRxiv 49:949
Mok JS, Ryu A, Kwon JY et al (2019) Abundance, antimicrobial resistance, and virulence of pathogenic Vibrio strains from molluscan shellfish farms along the Korean coast. Mar Pollut Bull 149:110559. https://doi.org/10.1016/j.marpolbul.2019.110559
Molina-Aja A, García-Gasca A, Abreu-Grobois A et al (2002) Plasmid profiling and antibiotic resistance of Vibrio strains isolated from cultured penaeid shrimp. FEMS Microbiol Lett 213:7–12. https://doi.org/10.1016/S0378-1097(02)00791-7
Moorthy S, Watnick PI (2005) Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol Microbiol 57:1623–1635. https://doi.org/10.1111/j.1365-2958.2005.04797.x
Morita Y, Kataoka A, Shiota S et al (2000) NorM of vibrio parahaemolyticus is an Na(+)-driven multidrug efflux pump. J Bacteriol 182:6694–6697. https://doi.org/10.1128/JB.182.23.6694-6697.2000
Morita D, Takahashi E, Morita M et al (2020) Genomic characterization of antibiotic resistance-encoding genes in clinical isolates of Vibrio cholerae non-O1/non-O139 strains from Kolkata, India: generation of novel types of genomic islands containing plural antibiotic resistance genes. Microbiol Immunol 64:435–444. https://doi.org/10.1111/1348-0421.12790
Morita Y, Li X-Z (2016) Antimicrobial resistance and drug efflux pumps in Vibrio and Legionella. In: Li XZ, Elkins C, Zgurskaya H (eds) Efflux-mediated antimicrobial resistance in bacteria. Adis, Cham, p 307–328
Morris JG (2003) Cholera and other types of vibriosis: a story of human pandemics and oysters on the half shell. Clin Infect Dis 37:272–280. https://doi.org/10.1086/375600
Morris RD (2007) The blue death : disease, disaster, and the water we drink, 1st edn. HarperCollins, New York
Motes ML, DePaola A, Cook DW et al (1998) Influence of water temperature and salinity on Vibrio vulnificus in Northern Gulf and Atlantic Coast oysters (Crassostrea virginica). Appl Environ Microbiol 64:1459–1465. https://doi.org/10.1128/AEM.64.4.1459-1465.1998
Mukherjee M, Kakarla P, Kumar S et al (2014) Comparative genome analysis of non-toxigenic non-O1 versus toxigenic O1 Vibrio cholerae. Genom Discov 2:1–15. https://doi.org/10.7243/2052-7993-2-1
Mukhopadhyay AK, Takeda Y, Balakrish Nair G (2014) Cholera outbreaks in the El Tor Biotype era and the impact of the new El Tor variants. In: Nair GB, Takeda Y (eds) Cholera outbreaks. Springer, Berlin, pp 17–47
Nair GB, Ramamurthy T, Bhattacharya SK et al (1994) Spread of Vibrio cholerae O139 Bengal in India. J Infect Dis 169:1029–1034. https://doi.org/10.1093/infdis/169.5.1029
Nakayama T, Yamaguchi T, Jinnai M et al (2023) ESBL-producing Vibrio vulnificus and V. alginolyticus harbour a plasmid encoding ISEc9 upstream of blaCTX-M-55 and qnrS2 isolated from imported seafood. Arch Microbiol 205:241. https://doi.org/10.1007/s00203-023-03569-x
Ndraha N, Hsiao H-I (2019) The risk assessment of Vibrio parahaemolyticus in raw oysters in Taiwan under the seasonal variations, time horizons, and climate scenarios. Food Control 102:188–196. https://doi.org/10.1016/j.foodcont.2019.03.020
Nelson ML, Levy SB (2011) The history of the tetracyclines. Ann N Y Acad Sci 1241:17–32. https://doi.org/10.1111/j.1749-6632.2011.06354.x
Neogi SB, Chowdhury N, Awasthi SP et al (2019) Novel cholera toxin variant and ToxT regulon in environmental Vibrio mimicus isolates: potential resources for the evolution of Vibrio cholerae hybrid strains. Appl Environ Microbiol 85:e01977-e2018. https://doi.org/10.1128/AEM.01977-18
Nikaido H (1994) Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264:382–388. https://doi.org/10.1126/science.8153625
Nikaido H (1998) Antibiotic resistance caused by gram-negative multidrug efflux pumps. Clin Infect Dis 27:S32–S41. https://doi.org/10.1086/514920
Nikaido H (2011) Structure and mechanism of RND-type multidrug efflux pumps. Adv Enzymol Relat Areas Mol Biol 77:1–60. https://doi.org/10.1002/9780470920541.ch1
Nishibuchi M, Ishibashi M, Takeda Y, Kaper JB (1985) Detection of the thermostable direct hemolysin gene and related DNA sequences in Vibrio parahaemolyticus and other vibrio species by the DNA colony hybridization test. Infect Immun 49:481–486. https://doi.org/10.1128/IAI.49.3.481-486.1985
Nishibuchi M, Taniguchi T, Misawa T et al (1989) Cloning and nucleotide sequence of the gene (trh) encoding the hemolysin related to the thermostable direct hemolysin of Vibrio parahaemolyticus. Infect Immun 57:2691–2697. https://doi.org/10.1128/IAI.57.9.2691-2697.1989
Ogawa W, Minato Y, Dodan H et al (2015) Characterization of MATE-type multidrug efflux pumps from Klebsiella pneumoniae MGH78578. PLoS ONE 10:e0121619. https://doi.org/10.1371/journal.pone.0121619
Oh EG, Son KT, Yu H et al (2011) Antimicrobial resistance of Vibrio parahaemolyticus and Vibrio alginolyticus strains isolated from farmed fish in Korea from 2005 through 2007. J Food Prot 74:380–386. https://doi.org/10.4315/0362-028X.JFP-10-307
Okoh AI, Igbinosa EO (2010) Antibiotic susceptibility profiles of some Vibrio strains isolated from wastewater final effluents in a rural community of the Eastern Cape Province of South Africa. BMC Microbiol 10:143. https://doi.org/10.1186/1471-2180-10-143
Okuda J, Ishibashi M, Hayakawa E et al (1997) Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus in Calcutta, India, and isolation of strains from the same clonal group from Southeast Asian travelers arriving in Japan. J Clin Microbiol 35:3150–3155
Okura M, Osawa R, Iguchi A et al (2003) Genotypic analyses of Vibrio parahaemolyticus and development of a pandemic group-specific multiplex PCR assay. J Clin Microbiol 41:4676–4682
Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415–425. https://doi.org/10.1111/j.1574-6976.2009.00200.x
Oliver JD, Pruzzo C, Vezzulli L, Kaper JB (2012) Vibrio species. Food microbiology. John Wiley & Sons Ltd, pp 401–439
Otsuka M, Yasuda M, Morita Y et al (2005) Identification of essential amino acid residues of the NorM Na+/multidrug antiporter in Vibrio parahaemolyticus. J Bacteriol 187:1552–1558. https://doi.org/10.1128/JB.187.5.1552-1558.2005
Ottaviani D, Bacchiocchi I, Masini L et al (2001) Antimicrobial susceptibility of potentially pathogenic halophilic vibrios isolated from seafood. Int J Antimicrob Agents 18:135–140. https://doi.org/10.1016/S0924-8579(01)00358-2
Ottaviani D, Leoni F, Rocchegiani E et al (2011) Unusual case of necrotizing fasciitis caused by Vibrio cholerae O137. J Clin Microbiol 49:757–759. https://doi.org/10.1128/JCM.02257-10
Ouellette M, Gerbaud G, Courvalin P (1988) Genetic, biochemical and molecular characterization of strains of Vibrio cholerae multiresistant to antibiotics. Ann Inst Pasteur Microbiol 139:105–113
Oyelade AA, Adelowo OO, Fagade OE (2018) blaNDM-1-producing Vibrio parahaemolyticus and V. vulnificus isolated from recreational beaches in Lagos Nigeria. Environ Sci Pollut Res Int 25:33538–33547. https://doi.org/10.1007/s11356-018-3306-2
Pao SS, Paulsen IT, Saier MH Jr (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34
Parthasarathy S, Das SC, Kumar A et al (2021) Molecular characterization and antibiotic resistance of Vibrio parahaemolyticus from Indian oyster and their probable implication in food chain. World J Microbiol Biotechnol 37:145. https://doi.org/10.1007/s11274-021-03113-3
Parvathi A, Kumar HS, Karunasagar I, Karunasagar I (2004) Detection and enumeration of Vibrio vulnificus in oysters from two estuaries along the southwest coast of India, using molecular methods. Appl Environ Microbiol 70:6909–6913. https://doi.org/10.1128/AEM.70.11.6909-6913.2004
Pasrija R, Banerjee D, Prasad R (2007) Structure and function analysis of CaMdr1p, a major facilitator superfamily antifungal efflux transporter protein of Candida albicans: identification of amino acid residues critical for drug/H+ transport. Eukaryot Cell 6:443–453. https://doi.org/10.1128/EC.00315-06
Pérez-Acosta JA, Martínez-Porchas M, Elizalde-Contreras JM et al (2018) Proteomic profiling of integral membrane proteins associated to pathogenicity in Vibrio parahaemolyticus strains. Microbiol Immunol 62:14–23. https://doi.org/10.1111/1348-0421.12556
Piddock LJ (2006) Multidrug-resistance efflux pumps—not just for resistance. Nat Rev Microbiol 4:629–636
Prescott LM, Datta A, Datta GC (1968) R-factors in Calcutta strains of Vibrio cholerae and members of the enterobacteriaceae. Bull World Health Organ 39:971–973
Rahal K, Gerbaud GR, Chabbert YA (1973) Properties of a transferable resistance factor in Vibrio cholerae Biotype El Tor. Ann Microbiol (Paris) 124:283–294
Rahman MM, Matsuo T, Ogawa W et al (2007) Molecular cloning and characterization of all RND-type efflux transporters in Vibrio cholerae non-O1. Microbiol Immunol 51:1061–1070. https://doi.org/10.1111/j.1348-0421.2007.tb04001.x
Rahmati S, Yang S, Davidson AL, Zechiedrich EL (2002) Control of the AcrAB multidrug efflux pump by quorum-sensing regulator SdiA. Mol Microbiol 43:677–685
Ramamurthy T, Garg S, Sharma R et al (1993) Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India. Lancet 341:703–704. https://doi.org/10.1016/0140-6736(93)90480-5
Ramamurthy T, Ghosh A (2021) A re-look at cholera pandemics from early times to now in the current era of epidemiology. J Disast Res 16:110–117. https://doi.org/10.20965/jdr.2021.p0110
Ranaweera I, Shrestha U, Ranjana K et al (2015) Structural comparison of bacterial multidrug efflux pumps of the major facilitator superfamily. Trends Cell Mol Biol 10:131
Reguera G, Kolter R (2005) Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on Chitin. J Bacteriol 187:3551–3555. https://doi.org/10.1128/jb.187.10.3551-3555.2005
Reidl J, Klose KE (2002) Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol Rev 26:125–139. https://doi.org/10.1111/j.1574-6976.2002.tb00605.x
Reyhanath PV, Ranjeet K (2014) Incidence of multidrug resistant Vibrio parahaemolyticus isolated from Ponnani, South India. Iran J Microbiol 6:60–67
Rouch DA, Cram DS, DiBerardino D et al (1990) Efflux-mediated antiseptic resistance gene qacA from Staphylococcus aureus: common ancestry with tetracycline- and sugar-transport proteins. Mol Microbiol 4:2051–2062. https://doi.org/10.1111/j.1365-2958.1990.tb00565.x
Rouquette-Loughlin C, Dunham SA, Kuhn M et al (2003) The NorM efflux pump of Neisseria gonorrhoeae and Neisseria meningitidis recognizes antimicrobial cationic compounds. J Bacteriol 185:1101–1106. https://doi.org/10.1128/JB.185.3.1101-1106.2003
Rubin DHF, Zingl FG, Leitner DR et al (2022) Reemergence of cholera in Haiti. N Engl J Med 387:2387–2389. https://doi.org/10.1056/NEJMc2213908
Saha GK, Ganguly NK (2021) Spread and endemicity of cholera in india: factors beyond the numbers. J Infect Dis 224:S710–S716. https://doi.org/10.1093/infdis/jiab436
Saier MH Jr, Beatty JT, Goffeau A et al (1999) The major facilitator superfamily. J Mol Microbiol Biotechnol 1:257–279
Saier MH, Reddy VS, Moreno-Hagelsieb G et al (2021) The transporter classification database (TCDB): 2021 update. Nucleic Acids Res 49:D461–D467. https://doi.org/10.1093/nar/gkaa1004
Saraswathi K, Deodhar LP (1990) A study of V. cholerae strains isolated in Bombay. J Postgrad Med 36:128–130
Shannon JD, Kimbrough RC (2006) Pulmonary cholera due to infection with a non-O1 Vibrio cholerae strain. J Clin Microbiol 44:3459–3460. https://doi.org/10.1128/jcm.02343-05
Sharma C, Thungapathra M, Ghosh A et al (1998) Molecular analysis of non-O1, non-O139 Vibrio cholerae associated with an unusual upsurge in the incidence of cholera-like disease in Calcutta, India. J Clin Microbiol 36:756–763. https://doi.org/10.1128/jcm.36.3.756-763.1998
Sherman I (2007) Cholera. Twelve diseases that changed our world. John Wiley & Sons Ltd, pp 33–49
Silva IP, de Carneiro CS, Saraiva MAF et al (2018) Antimicrobial resistance and potential virulence of Vibrio parahaemolyticus isolated from water and bivalve mollusks from Bahia, Brazil. Mar Pollut Bull 131:757–762. https://doi.org/10.1016/j.marpolbul.2018.05.007
Silvester R, Pires J, Van Boeckel TP et al (2019) Occurrence of β-lactam resistance genes and plasmid-mediated resistance among vibrios isolated from Southwest Coast of India. Microb Drug Resist 25:1306–1315. https://doi.org/10.1089/mdr.2019.0031
Smith KP, Kumar S, Varela MF (2009) Identification, cloning, and functional characterization of EmrD-3, a putative multidrug efflux pump of the major facilitator superfamily from Vibrio cholerae O395. Arch Microbiol 191:903–911
Someya Y, Kimura-Someya T, Yamaguchi A (2000) Role of the charge interaction between Arg(70) and Asp(120) in the Tn10-encoded metal-tetracycline/H(+) antiporter of Escherichia coli. J Biol Chem 275:210–214. https://doi.org/10.1074/jbc.275.1.210
Stein WD (1986) CHAPTER 6 - primary active transport systems: chemiosmosis. In: Stein WD (ed) Transport and diffusion across cell membranes. Academic Press, pp 475–612
Stein W (2012) Transport and diffusion across cell membranes. Elsevier
Sten-Knudsen O (1978) Passive transport processes. In: Tosteson DC (ed) Concepts and models. Springer, Berlin, pp 5–113
Stephen J, Lekshmi M, Ammini P et al (2022) Membrane efflux pumps of pathogenic vibrio species: role in antimicrobial resistance and virulence. Microorganisms 10:382. https://doi.org/10.3390/microorganisms10020382
Stephen J, Salam F, Lekshmi M et al (2023) The major facilitator superfamily and antimicrobial resistance efflux pumps of the ESKAPEE pathogen Staphylococcus aureus. Antibiotics 12:343. https://doi.org/10.3390/antibiotics12020343
Stratev D, Fasulkova R, Krumova-Valcheva G (2023) Incidence, virulence genes and antimicrobial resistance of Vibrio parahaemolyticus isolated from seafood. Microb Pathog 177:106050. https://doi.org/10.1016/j.micpath.2023.106050
Su X-Z, Chen J, Mizushima T et al (2005) AbeM, an H+-coupled Acinetobacter baumannii multidrug efflux pump belonging to the MATE family of transporters. Antimicrob Agents Chemother 49:4362–4364. https://doi.org/10.1128/AAC.49.10.4362-4364.2005
Symmons MF, Marshall RL, Bavro VN (2015) Architecture and roles of periplasmic adaptor proteins in tripartite efflux assemblies. Front Microbiol 6:513. https://doi.org/10.3389/fmicb.2015.00513
Tabtieng R, Wattanasri S, Echeverria P et al (1989) An epidemic of Vibrio cholerae El Tor Inaba resistant to several antibiotics with a conjugative group C plasmid coding for type II dihydrofolate reductase in Thailand. Am J Trop Med Hyg 41:680–686. https://doi.org/10.4269/ajtmh.1989.41.680
Tan CW, Rukayadi Y, Hasan H et al (2020) Prevalence and antibiotic resistance patterns of Vibrio parahaemolyticus isolated from different types of seafood in Selangor, Malaysia. Saudi J Biol Sci 27:1602–1608. https://doi.org/10.1016/j.sjbs.2020.01.002
Tanabe T, Funahashi T, Nakao H et al (2003) Identification and characterization of genes required for biosynthesis and transport of the siderophore vibrioferrin in Vibrio parahaemolyticus. J Bacteriol 185:6938–6949. https://doi.org/10.1128/JB.185.23.6938-6949.2003
Tanabe T, Nakao H, Kuroda T et al (2006) Involvement of the Vibrio parahaemolyticus pvsC gene in export of the siderophore vibrioferrin. Microbiol Immunol 50:871–876
Tanaka Y, Hipolito CJ, Maturana AD et al (2013) Structural basis for the drug extrusion mechanism by a MATE multidrug transporter. Nature 496:247–251. https://doi.org/10.1038/nature12014
Taylor DL, Bina XR, Bina JE (2012) Vibrio cholerae vexH encodes a multiple drug efflux pump that contributes to the production of cholera toxin and the toxin co-regulated pilus. PLoS ONE 7:e38208
Threlfall EJ, Rowe B, Huq I (1980) Plasmid-encoded multiple antibiotic resistance in Vibrio cholerae El Tor from Bangladesh. Lancet 1:1247–1248. https://doi.org/10.1016/s0140-6736(80)91701-8
Towner KJ, Pearson NJ, Mhalu FS, O’Grady F (1980) Resistance to antimicrobial agents of Vibrio cholerae E1 Tor strains isolated during the fourth cholera epidemic in the United Republic of Tanzania. Bull World Health Organ 58:747–751
Tseng TT, Gratwick KS, Kollman J et al (1999) The rnd permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol 1:107–125
Upadhyay N, Kar D, Deepak Mahajan B et al (2019) The multitasking abilities of MATE 1285 transporters in plants. J Exp Bot 70:4643–4656. https://doi.org/10.1093/jxb/erz246
Varela MF, Griffith JK (1993) Nucleotide and deduced protein sequences of the class D tetracycline resistance determinant: relationship to other antimicrobial transport proteins. Antimicrob Agents Chemother 37:1253–1258. https://doi.org/10.1128/aac.37.6.1253
Varela MF, Kumar S (2019) Strategies for discovery of new molecular targets for anti-infective drugs. Curr Opin Pharmacol 48:57–68. https://doi.org/10.1016/j.coph.2019.04.015
Varela MF, Wilson TH (1996) Molecular biology of the lactose carrier of Escherichia coli. Biochem Biophys Acta 1276:21–34. https://doi.org/10.1016/0005-2728(96)00030-8
Varela MF, Sansom CE, Griffith JK (1995) Mutational analysis and molecular modelling of an amino acid sequence motif conserved in antiporters but not symporters in a transporter superfamily. Mol Membr Biol 12:313–319. https://doi.org/10.3109/09687689509072433
Verma J, Bag S, Saha B et al (2019) Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae. Proc Natl Acad Sci 116:6226–6231. https://doi.org/10.1073/pnas.1900141116
Vezzulli L, Baker-Austin C, Kirschner A et al (2020) Global emergence of environmental non-O1/O139 Vibrio cholerae infections linked with climate change: a neglected research field? Environ Microbiol 22:4342–4355. https://doi.org/10.1111/1462-2920.15040
Vu TTT, Hoang TTH, Fleischmann S et al (2022) Quantification and antimicrobial resistance of Vibrio parahaemolyticus in retail seafood in Hanoi, Vietnam. J Food Prot 85:786–791. https://doi.org/10.4315/JFP-21-444
Wade BM (2022) The blue death: cholera and reimagined community in nineteenth-century Havana. In: Venkatesan S, Chatterjee A, Lewis AD, Callender B (eds) Pandemics and epidemics in cultural representation. Springer Nature, Singapore, pp 81–103
Waldor MK, Tschäpe H, Mekalanos JJ (1996) A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J Bacteriol 178:4157–4165. https://doi.org/10.1128/jb.178.14.4157-4165.1996
Wei Y, Perez LJ, Ng W-L et al (2011) Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem Biol 6:356–365
Weng Y, Fields EG, Bina TF et al (2021) Vibrio cholerae TolC is required for expression of the ToxR regulon. Infect Immunity. https://doi.org/10.1128/iai.00242-21
West IC (1980) Energy coupling in secondary active transport. Biochem Biophys Acta 604:91–126. https://doi.org/10.1016/0005-2736(80)90586-6
WHO (2022) WHO fact sheet. https://www.who.int/news-room/fact-sheets/detail/food-safety. Accessed 14 Jan 2023
Woolley RC, Vediyappan G, Anderson M et al (2005) Characterization of the Vibrio cholerae vceCAB multiple-drug resistance efflux operon in Escherichia coli. J Bacteriol 187:5500–5503. https://doi.org/10.1128/JB.187.15.5500-5503.2005
Wu C, Zhao Z, Liu Y et al (2020) Type III secretion 1 effector gene diversity among vibrio isolates from coastal areas in China. Front Cell Infect Microbiol. https://doi.org/10.3389/fcimb.2020.00301
Yaffe D, Radestock S, Shuster Y et al (2013) Identification of molecular hinge points mediating alternating access in the vesicular monoamine transporter VMAT2. Proc Natl Acad Sci 110:E1332–E1341
Yamaguchi A, Someya Y, Sawai T (1992) Metal-tetracycline/H+ antiporter of Escherichia coli encoded by transposon Tn10. The role of a conserved sequence motif, GXXXXRXGRR, in a putative cytoplasmic loop between helices 2 and 3. J Biol Chem 267:19155–19162
Ye L, Zheng Z, Xu Y et al (2023) Prevalence and genetic basis of tetracycline resistance in Vibrio parahaemolyticus isolates recovered from food products in Shenzhen, China during 2013 to 2021. Sci Total Environ 902:166026. https://doi.org/10.1016/j.scitotenv.2023.166026
UNHCR Yemen flooding escalates spread of cholera (2023). In: UNHCR Hong Kong. https://www.unhcr.org/hk/en/23296-yemen-flooding-escalates-spread-of-cholera.html. Accessed 8 Oct 2023
Yokota T, Kuwahara S (1977) Temperature-sensitive R plasmid obtained from naturally isolated drug-resistant Vibrio cholerae (Biotype El Tor). Antimicrob Agents Chemother 11:13–20. https://doi.org/10.1128/AAC.11.1.13
Yuan Y, Feng Z, Wang J (2020) Vibrio vulnificus Hemolysin: biological activity, regulation of vvhA expression, and role in pathogenesis. Front Immunol 11:599439. https://doi.org/10.3389/fimmu.2020.599439
Zaidenstein R, Sadik C, Lerner L et al (2008) Clinical characteristics and molecular subtyping of Vibrio vulnificus illnesses, Israel. Emerg Infect Dis 14:1875–1882. https://doi.org/10.3201/eid1412.080499
Zanetti S, Spanu T, Deriu A et al (2001) In vitro susceptibility of Vibrio spp. isolated from the environment. Int J Antimicrob Agents 17:407–409. https://doi.org/10.1016/S0924-8579(01)00307-7
Zhang G, Sun K, Ai G et al (2019) A novel family of intrinsic chloramphenicol acetyltransferase CATC in Vibrio parahaemolyticus: naturally occurring variants reveal diverse resistance levels against chloramphenicol. Int J Antimicrob Agents 54:75–79. https://doi.org/10.1016/j.ijantimicag.2019.03.012
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The research studies reported from our laboratories and reflected in this publication were supported by Faculty Research and Instructional Development grants by ENMU and the National Institute of the General Medical Sciences (P20GM103451) awarded by the National Institutes of Health, plus the HSI-STEM program from the U.S. Department of Education (P031C110114).
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Kumar, S., Lekshmi, M., Stephen, J. et al. Dynamics of efflux pumps in antimicrobial resistance, persistence, and community living of Vibrionaceae. Arch Microbiol 206, 7 (2024). https://doi.org/10.1007/s00203-023-03731-5
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DOI: https://doi.org/10.1007/s00203-023-03731-5