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Versatile lifestyles of Edwardsiella: Free-living, pathogen, and core bacterium of the aquatic resistome

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 5-18 | Received 02 Sep 2021, Accepted 11 Nov 2021, Published online: 30 Dec 2021

References

  • Buján N, Toranzo A, Magariños B. Edwardsiella piscicida: a significant bacterial pathogen of cultured fish. Dis Aquat Organ. 2018;131:59–71.
  • Reichley SR, Ware C, Steadman J, et al. Comparative phenotypic and genotypic analysis of Edwardsiella isolates from different hosts and geographic origins, with emphasis on isolates formerly classified as E. tarda, and evaluation of diagnostic methods. J Clin Microbiol. 2017;55:3466–3491.
  • Abayneh T, Colquhoun DJ, Sørum H. Edwardsiella piscicida sp. nov., a novel species pathogenic to fish. J Appl Microbiol. 2013;114:644–654.
  • Shao S, Lai Q, Liu Q, et al. Phylogenomics characterization of a highly virulent Edwardsiella strain ET080813T encoding two distinct T3SS and three T6SS gene clusters: propose a novel species as Edwardsiella anguillarum sp. nov. Syst Appl Microbiol. 2015;38:36–47.
  • Mohanty BR, Sahoo PK. Edwardsiellosis in fish: a brief review. J Biosci. 2007;32:1331–1344.
  • Griffin MJ, Reichley SR, Greenway TE, et al. Comparison of Edwardsiella ictaluri isolates from different hosts and geographic origins. J Fish Dis. 2016;39:947–969.
  • Wang K, Liu E, Song S, et al. Characterization of Edwardsiella tarda rpoN: roles in σ70 family regulation, growth, stress adaption and virulence toward fish. Arch Microbiol. 2012;194:493–504.
  • Swain B, Powell CT, Curtiss R. Pathogenicity and immunogenicity of Edwardsiella piscicida ferric uptake regulator (fur) mutations in zebrafish. Fish Shellfish Immunol. 2020;107:497–510.
  • Akgul A, Akgul A, Lawrence ML, et al. Stress-related genes promote Edwardsiella ictaluri pathogenesis. PLoS One. 2018;13:e0194669.
  • Shi Y-J, Fang Q-J, Huang H-Q, et al. HutZ is required for biofilm formation and contributes to the pathogenicity of Edwardsiella piscicida. Vet Res. 2019;50:76.
  • Lee SW, Wendy W. Antibiotic and heavy metal resistance of Aeromonas hydrophila and Edwardsiella tarda isolated from red hybrid tilapia (Oreochromis spp.) coinfected with motile aeromonas septicemia and edwardsiellosis. Vet World. 2017;10:803–807.
  • Leung KY, Wang Q, Yang Z, et al. Edwardsiella piscicida: a versatile emerging pathogen of fish. Virulence. 2019;10:555–567.
  • Liu Y, Gao Y, Liu X, et al. Transposon insertion sequencing reveals T4SS as the major genetic trait for conjugation transfer of multi-drug resistance pEIB202 from Edwardsiella. BMC Microbiol. 2017;17:112.
  • Tekedar HC, Blom J, Kalindamar S, et al. Comparative genomics of the fish pathogens Edwardsiella ictaluri 93-146 and Edwardsiella piscicida C07-087. Microb Genomics. 2020;6:e000322.
  • Thune RL, Fernandez DH, Benoit JL, et al. Signature-tagged mutagenesis of Edwardsiella ictaluri identifies virulence-related genes, including a Salmonella pathogenicity Island 2 class of type III secretion systems. Appl Environ Microbiol. 2007;73:7934–7946.
  • Yu JE, Cho MY, Kim J, et al. Large antibiotic-resistance plasmid of Edwardsiella tarda contributes to virulence in fish. Microb Pathog. 2012;52:259–266.
  • Tan YP, Zheng J, Tung SL, et al. Role of type III secretion in Edwardsiella tarda virulence. Microbiology. 2005;151:2301–2313.
  • Zheng J, Leung KY. Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol. 2007;66:1192–1206.
  • Sun K, Wang H, Zhang M, et al. Genetic mechanisms of multi-antimicrobial resistance in a pathogenic Edwardsiella tarda strain. Aquaculture. 2009;289:134–139.
  • Xiao J, Chen T, Liu B, et al. Edwardsiella tarda mutant disrupted in type III secretion system and chorismic acid synthesis and cured of a plasmid as a live attenuated vaccine in turbot. Fish Shellfish Immunol. 2013;35:632–641.
  • Chen H, Yang D, Han F, et al. The bacterial T6SS effector EvpP prevents NLRP3 inflammasome activation by inhibiting the Ca2+ -Dependent MAPK-Jnk pathway. Cell Host Microbe. 2017;21:47–58.
  • Leung KY, Siame BA, Tenkink BJ, et al. Edwardsiella tarda – virulence mechanisms of an emerging gastroenteritis pathogen. Microbes Infect. 2012;14:26–34.
  • Yin K, Guan Y, Ma R, et al. Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida. PLOS Pathog. 2018;14:e1007272.
  • Roy R, Tiwari M, Donelli G, et al. Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence. 2018;9:522–554.
  • Logares R, Bråte J, Bertilsson S, et al. Infrequent marine–freshwater transitions in the microbial world. Trends Microbiol. 2009;17:414–422.
  • Gołębiewski M, Całkiewicz J, Creer S, et al. Tideless estuaries in brackish seas as possible freshwater-marine transition zones for bacteria: the case study of the Vistula river estuary. Environ Microbiol Rep. 2017;9:129–143.
  • Cabello-Yeves PJ, Rodriguez-Valera F. Marine-freshwater prokaryotic transitions require extensive changes in the predicted proteome. Microbiome. 2019;7:117.
  • Xu T, Zhang X-H. Edwardsiella tarda: an intriguing problem in aquaculture. Aquaculture. 2014;431:129–135.
  • Wang Y, Wang Q, Yang M, et al. Proteomic analysis of a twin-arginine translocation-deficient mutant unravel its functions involved in stress adaptation and virulence in fish pathogen Edwardsiella tarda. FEMS Microbiol Lett. 2013;343:145–155.
  • Xu L, Wang Q, Xiao J, et al. Characterization of Edwardsiella tarda waaL: roles in lipopolysaccharide biosynthesis, stress adaptation, and virulence toward fish. Arch Microbiol. 2010;192:1039–1047.
  • Akgul A, Nho SW, Kalindamar S, et al. Universal stress proteins contribute Edwardsiella ictaluri virulence in catfish. Front Microbiol. 2018;9:2931.
  • Wang B, Huang H, Li S, et al. Thioredoxin H (TrxH) contributes to adversity adaptation and pathogenicity of Edwardsiella piscicida. Vet Res. 2019;50:26.
  • Rogge ML, Thune RL. Regulation of the Edwardsiella ictaluri type III secretion system by pH and phosphate concentration through EsrA, EsrB, and EsrC. Appl Environ Microbiol. 2011;77:4293–4302.
  • Du M, Chen J, Zhang X, et al. Retention of virulence in a viable but nonculturable Edwardsiella tarda isolate. Appl Environ Microbiol. 2007;73:1349–1354.
  • Wei L, Wu Y, Yang G, et al. Genome- wide identification of fitness factors in seawater for Edwardsiella piscicida. Appl Environ Microbiol. 2019;85:e00233–19.
  • Liu Y, Zhao L, Yang M, et al. Transcriptomic dissection of the horizontally acquired response regulator EsrB reveals its global regulatory roles in the physiological adaptation and activation of T3SS and the cognate effector repertoire in Edwardsiella piscicida during infection toward. Virulence. 2017;8:1355–1377.
  • Yin K, Wang Q, Xiao J, et al. Comparative proteomic analysis unravels a role for EsrB in the regulation of reactive oxygen species stress responses in Edwardsiella piscicida. FEMS Microbiol Lett. 2017;364:fnw269.
  • Guan Y, Yin K, Zhou M, et al. EsrB negatively regulates expression of the glutamine sythetase GlnA in the fish pathogen Edwardsiella piscicida. FEMS Microbiol Lett. 2018;365:fny007.
  • Kingsley RA, Langridge G, Smith SE, et al. Functional analysis of Salmonella Typhi adaptation to survival in water. Environ Microbiol. 2018;20:4079–4090.
  • Lange W. Limiting nutrient elements in filtered Lake Erie water. Water Res. 1971;5:1031–1048.
  • Parry R. Agricultural phosphorus and water quality: a U.S. Environmental Protection Agency perspective. J Environ Qual. 1998;27:258–261.
  • Hu Y, Sun L. The global regulatory effect of Edwardsiella tarda Fur on iron acquisition, stress resistance, and host infection: a proteomics-based interpretation. J Proteomics. 2016;140:100–110.
  • Chakraborty S, Sivaraman J, Leung KY, et al. Two-component PhoB-PhoR regulatory system and ferric uptake regulator sense phosphate and iron to control virulence genes in type III and VI secretion systems of Edwardsiella tarda. J Biol Chem. 2011;286:39417–39430.
  • Rabin N, Zheng Y, Opoku-Temeng C, et al. Biofilm formation mechanisms and targets for developing antibiofilm agents. Future Med Chem. 2015;7:493–512.
  • Yan J, Bassler BL. Surviving as a community: antibiotic tolerance and persistence in bacterial biofilms. Cell Host Microbe. 2019;26:15–21.
  • Hall CW, Mah T-F. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev. 2017;41:276–301.
  • Venkatesan N, Perumal G, Doble M. Bacterial resistance in biofilm-associated bacteria. Future Microbiol. 2015;10:1743–1750.
  • Santander J, Martin T, Loh A, et al. Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence. Microbiology. 2013;159:1471–1486.
  • Mo Z-L, Li J, G-y L, et al. Phenotypic characterization, virulence, and immunogenicity of Edwardsiella tarda LSE40 aroA mutant. Appl Microbiol Biotechnol. 2013;97:6325–6335.
  • Xu T, Su Y, Xu Y, et al. Mutations of flagellar genes fliC12, fliA and flhDC of Edwardsiella tarda attenuated bacterial motility, biofilm formation and virulence to fish. J Appl Microbiol. 2014;116:236–244.
  • Wang C, Hu Y, Chi H, et al. The major fimbrial subunit protein of Edwardsiella tarda: vaccine potential, adjuvant effect, and involvement in host infection. Fish Shellfish Immunol. 2013;35:858–865.
  • Hu Y, Li Y, Sun L. Edwardsiella tarda Hfq: impact on host infection and global protein expression. Vet Res. 2014;45:23.
  • Hassan HA, Ding X, Zhang X, et al. Fish borne Edwardsiella tarda eha involved in the bacterial biofilm formation, hemolytic activity, adhesion capability and pathogenicity. Arch Microbiol. 2020;202:835–842.
  • Xu Y, Xu T, Wang B, et al. A mutation in rcsB, a gene encoding the core component of the Rcs cascade, enhances the virulence of Edwardsiella tarda. Res Microbiol. 2014;165:226–232.
  • Xiao J, Wang Q, Liu Q, et al. Characterization of Edwardsiella tarda rpoS: effect on serum resistance, chondroitinase activity, biofilm formation, and autoinducer synthetases expression. Appl Microbiol Biotechnol. 2009;83:151–160.
  • Zheng J, Tung SL, Leung KY. Regulation of a type III and a putative secretion system in Edwardsiella tarda by EsrC is under the control of a two-component system, EsrA-EsrB. Infect Immun. 2005;73:4127–4137.
  • Sun Y, Li Y, Luo Q, et al. LuxS/AI-2 quorum sensing system in Edwardsiella piscicida promotes biofilm formation and pathogenicity. Infect Immun. 2020;88:e00907–19.
  • Dong X, Fan X, Wang B, et al. Invasin of Edwardsiella tarda is essential for its haemolytic activity, biofilm formation and virulence towards fish. J Appl Microbiol. 2013;115:12–19.
  • Hu Y, Zhou H, Jin Q, et al. The serine protease autotransporter Tsh contributes to the virulence of Edwardsiella tarda. Vet Microbiol. 2016;189:68–74.
  • Srinivasa Rao PS, Yamada Y, Tan YP, et al. Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol Microbiol. 2004;53:573–586.
  • Gao ZP, Nie P, Lu JF, et al. Type III secretion system translocon component EseB forms filaments on and mediates autoaggregation of and biofilm formation by Edwardsiella tarda. Appl Environ Microbiol. 2015;81:6078–6087.
  • Okocha RC, Olatoye IO, Adedeji OB. Food safety impacts of antimicrobial use and their residues in aquaculture. Public Health Rev. 2018;39:21.
  • Henriksson PJG, Rico A, Troell M, et al. Unpacking factors influencing antimicrobial use in global aquaculture and their implication for management: a review from a systems perspective. Sustain Sci. 2018;13:1105–1120.
  • Zhuang M, Achmon Y, Cao Y, et al. Distribution of antibiotic resistance genes in the environment. Environ Pollut. 2021;285:117402.
  • Lerminiaux NA, Cameron ADS. Horizontal transfer of antibiotic resistance genes in clinical environments. Can J Microbiol. 2019;65:34–44.
  • Resende JA, Silva VL, Fontes CO, et al. Multidrug-resistance and toxic metal tolerance of medically important bacteria isolated from an aquaculture system. Microbes Environ. 2012;27:449–455.
  • Yuan K, Wang X, Chen X, et al. Occurrence of antibiotic resistance genes in extracellular and intracellular DNA from sediments collected from two types of aquaculture farms. Chemosphere. 2019;234:520–527.
  • Dos Santos DFK, Istvan P, Quirino BF, et al. Functional metagenomics as a tool for identification of new antibiotic resistance genes from natural environments. Microb Ecol. 2017;73:479–491.
  • Munita JM, and Arias CA. Mechanisms of antibiotic resistance. In: Kudva, I.T., and Cornick, N.A.(eds)., Virulence mechanisms of bacterial pathogens. Washington, DC, USA: ASM Press; 2016. p. 481–511.
  • Mao D, Yu S, Rysz M, et al. Prevalence and proliferation of antibiotic resistance genes in two municipal wastewater treatment plants. Water Res. 2015;85:458–466.
  • Kim SY, Kuppusamy S, Kim JH, et al. Occurrence and diversity of tetracycline resistance genes in the agricultural soils of South Korea. Environ Sci Pollut Res. 2016;23:22190–22196.
  • Peng B, Su Y, Li H, et al. Exogenous alanine and/or glucose plus kanamycin kills antibiotic-resistant bacteria. Cell Metab. 2015;21:249–262.
  • Allison KR, Brynildsen MP, Collins JJ. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature. 2011;473:216–220.
  • Su Y, Kuang S, Peng X, et al. The depressed P cycle contributes to the acquisition of ampicillin resistance in Edwardsiella piscicida. J Proteomics. 2020;212:103562.
  • Peng B, Wang C, Li H, et al. Outer membrane proteins form specific patterns in antibiotic-resistant Edwardsiella tarda. Front Microbiol. 2017;8:69.
  • Yu Z, Gunn L, Wall P, et al. Antimicrobial resistance and its association with tolerance to heavy metals in agriculture production. Food Microbiol. 2017;64:23–32.
  • Bengtsson-Palme J, Kristiansson E, Larsson DGJ. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol Rev. 2018;42:fux053.
  • Sultan I, Rahman S, Jan AT, et al. Antibiotics, resistome and resistance mechanisms: a bacterial perspective. Front Microbiol. 2018;9:2066.
  • Wang Q, Yang M, Xiao J, et al. Genome sequence of the versatile fish pathogen Edwardsiella tarda provides insights into its adaptation to broad host ranges and intracellular niches. PLoS One. 2009;4:e7646.
  • Lo DY, Lee YJ, Wang JH, et al. Antimicrobial susceptibility and genetic characterisation of oxytetracycline-resistant Edwardsiella tarda isolated from diseased eels. Vet Rec. 2014;175:203.
  • Cabezón E, Ripoll-Rozada J, Peña A, et al. Towards an integrated model of bacterial conjugation. FEMS Microbiol Rev. 2014;39:81–95.
  • Graf FE, Palm M, Warringer J, et al. Inhibiting conjugation as a tool in the fight against antibiotic resistance. Drug Dev Res. 2019;80:19–23.
  • Muniesa M, Colomer-Lluch M, Jofre J. Could bacteriophages transfer antibiotic resistance genes from environmental bacteria to human-body associated bacterial populations? Mob Genet Elements. 2013;3:e25847.
  • Touchon M, Moura de Sousa JA, Rocha EP. Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Curr Opin Microbiol. 2017;38:66–73.
  • Zhou S, Zhu Y, Yan Y, et al. Deciphering extracellular antibiotic resistance genes (eARGs) in activated sludge by metagenome. Water Res. 2019;161:610–620.
  • Zhao Z, Zhang K, Wu N, et al. Estuarine sediments are key hotspots of intracellular and extracellular antibiotic resistance genes: a high-throughput analysis in Haihe Estuary in China. Environ Int. 2020;135:105385.
  • Dong P, Wang H, Fang T, et al. Assessment of extracellular antibiotic resistance genes (eARGs) in typical environmental samples and the transforming ability of eARG. Environ Int. 2019;125:90–96.
  • Pietramellara G, Ascher J, Borgogni F, et al. Extracellular DNA in soil and sediment: fate and ecological relevance. Biol Fertil Soils. 2009;45:219–235.
  • Liu -S-S, Qu H-M, Yang D, et al. Chlorine disinfection increases both intracellular and extracellular antibiotic resistance genes in a full-scale wastewater treatment plant. Water Res. 2018;136:131–136.
  • Wei L, Qiao H, Sit B, et al. A bacterial pathogen senses host mannose to coordinate virulence. iSicence. 2019;20:310–323.
  • Yang G, Billings G, Hubbard TP, et al. Time-resolved transposon insertion sequencing reveals genome-wide fitness dynamics during infection. MBio. 2017;8:e01581–17.
  • Lan MZ, Peng X, Xiang MY, et al. Construction and characterization of a live, attenuated esrB mutant of Edwardsiella tarda and its potential as a vaccine against the haemorrhagic septicaemia in turbot, Scophthamus maximus (L.). Fish Shellfish Immunol. 2007;23:521–530.
  • Li J, Mo Z, Li G, et al. Generation and evaluation of virulence attenuated mutants of Edwardsiella tarda as vaccine candidates to combat edwardsiellosis in flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 2015;43:175–180.
  • Li M, Sun L. Edwardsiella tarda Sip2: a serum-induced protein that is essential to serum survival, acid resistance, intracellular replication, and host infection. Front Microbiol. 2018;9:1084.
  • Ma R, Yang G, Xu R, et al. Pattern analysis of conditional essentiality (PACE)-based heuristic identification of an in vivo colonization determinant as a novel target for the construction of a live attenuated vaccine against Edwardsiella piscicida. Fish Shellfish Immunol. 2019;90:65–72.
  • Trigui H, Dudyk P, Oh J, et al. A regulatory feedback loop between RpoS and SpoT supports the survival of Legionella pneumophila in water. Appl Environ Microbiol. 2015;81:918–928.
  • Desai SK, Winardhi RS, Periasamy S, et al. The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing. Elife. 2016;5:e10747.
  • Ferenci T. Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol Microbiol. 2005;57:1–8.
  • Dumpala PR, Peterson BC, Lawrence ML, et al. Identification of differentially abundant proteins of Edwardsiella ictaluri during iron restriction. PLoS One. 2015;10:e0132504.
  • Dung TT, Haesebrouck F, Sorgeloos P, et al. IncK plasmid-mediated tetracycline resistance in Edwardsiella ictaluri isolates from diseased freshwater catfish in Vietnam. Aquaculture. 2009;295:157–159.
  • Welch TJ, Evenhuis J, White DG, et al. IncA/C Plasmid-mediated florfenicol resistance in the catfish pathogen Edwardsiella ictaluri. Antimicrob Agents Chemother. 2009;53:845–846.
  • Abdelhamed H, Ramachandran R, Ozdemir O, et al. Characterization of a novel conjugative plasmid in Edwardsiella piscicida strain MS-18-199. Front Cell Infect Microbiol. 2019;9:404.
  • Kim A, Lim Y, Kim N, et al. A comparison of genotypic and phenotypic methods for analyzing the susceptibility to sulfamethoxazole and trimethoprim in Edwardsiella piscicida. Microb Drug Resist. 2018;24:1226–1235.
  • Aoki T, Takahashi A. Class D tetracycline resistance determinants of R plasmids from the fish pathogens Aeromonas hydrophila, Edwardsiella tarda, and Pasteurella piscicida. Antimicrob Agents Chemother. 1987;31:1278–1280.
  • Tee LW, Najiah M. Antibiogram and heavy metal tolerance of bullfrog bacteria in Malaysia. Open Vet J. 2011;1:39–45.
  • Nikapitiya C, Chandrarathna HPSU, Dananjaya SHS, et al. Isolation and characterization of phage (ETP-1) specific to multidrug resistant pathogenic Edwardsiella tarda and its in vivo biocontrol efficacy in zebrafish (Danio rerio). Biologicals. 2020;63:14–23.