{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T14:55:39Z","timestamp":1787496939087,"version":"build-2736575974"},"reference-count":63,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2023,12,28]],"date-time":"2023-12-28T00:00:00Z","timestamp":1703721600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["2016-67015-24909"],"award-info":[{"award-number":["2016-67015-24909"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Ministry of National Education of Turke"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"\n Edwardsiella ictaluri<\/jats:italic>\n is a Gram-negative facultative intracellular fish pathogen causing enteric septicemia of catfish (ESC). While various secretion systems contribute to\n E<\/jats:italic>\n .\n ictaluri<\/jats:italic>\n virulence, the Type VI secretion system (T6SS) remains poorly understood. In this study, we constructed 13\n E<\/jats:italic>\n .\n ictaluri<\/jats:italic>\n T6SS mutants using splicing by overlap extension PCR and characterized them, assessing their uptake and survival in channel catfish (\n Ictalurus punctatus<\/jats:italic>\n ) peritoneal macrophages, attachment and invasion in channel catfish ovary (CCO) cells, in vitro stress resistance, and virulence and efficacy in channel catfish. Among the mutants,\n Ei<\/jats:italic>\n \u0394\n evpA<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpH<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpM<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpN<\/jats:italic>\n , and\n Ei<\/jats:italic>\n \u0394\n evpO<\/jats:italic>\n exhibited reduced replication inside peritoneal macrophages.\n Ei<\/jats:italic>\n \u0394\n evpM<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpN<\/jats:italic>\n , and\n Ei<\/jats:italic>\n \u0394\n evpO<\/jats:italic>\n showed significantly decreased attachment to CCO cells, while\n Ei<\/jats:italic>\n \u0394\n evpN<\/jats:italic>\n and\n Ei<\/jats:italic>\n \u0394\n evpO<\/jats:italic>\n also displayed reduced invasion of CCO cells (\n p<\/jats:italic>\n < 0.05). Overall, T6SS mutants demonstrated enhanced resistance to oxidative and nitrosative stress in the nutrient-rich medium compared to the minimal medium. However,\n Ei<\/jats:italic>\n \u0394\n evpA<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpH<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpM<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpN<\/jats:italic>\n , and\n Ei<\/jats:italic>\n \u0394\n evpO<\/jats:italic>\n were susceptible to oxidative stress in both nutrient-rich and minimal medium. In fish challenges,\n Ei<\/jats:italic>\n \u0394\n evpD<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpE<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpG<\/jats:italic>\n ,\n Ei<\/jats:italic>\n \u0394\n evpJ<\/jats:italic>\n , and\n Ei<\/jats:italic>\n \u0394\n evpK<\/jats:italic>\n exhibited attenuation and provided effective protection against\n E<\/jats:italic>\n .\n ictaluri<\/jats:italic>\n wild-type (\n Ei<\/jats:italic>\n WT) infection in catfish fingerlings. However, their attenuation and protective efficacy were lower in catfish fry. These findings shed light on the role of the T6SS in\n E<\/jats:italic>\n .\n ictaluri<\/jats:italic>\n pathogenesis, highlighting its significance in intracellular survival, host cell attachment and invasion, stress resistance, and virulence. The attenuated T6SS mutants hold promise as potential candidates for protective immunization strategies in catfish fingerlings.\n <\/jats:p>","DOI":"10.1371\/journal.pone.0296132","type":"journal-article","created":{"date-parts":[[2023,12,28]],"date-time":"2023-12-28T13:23:27Z","timestamp":1703769807000},"page":"e0296132","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":6,"title":["Characterization of Type VI secretion system in Edwardsiella ictaluri"],"prefix":"10.1371","volume":"18","author":[{"given":"Safak","family":"Kalindamar","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hossam","family":"Abdelhamed","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adef O.","family":"Kordon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7678-791X","authenticated-orcid":true,"given":"Hasan C.","family":"Tekedar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lesya","family":"Pinchuk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6845-3346","authenticated-orcid":true,"given":"Attila","family":"Karsi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,12,28]]},"reference":[{"key":"pone.0296132.ref001","doi-asserted-by":"crossref","first-page":"1508","DOI":"10.1139\/f79-219","article-title":"A bacterium associated with disease of pond cultured channel catfish, Ictalurus punctatus","volume":"36","author":"JP Hawke","year":"1979","journal-title":"Journal of the Fisheries Research Board of Canada"},{"issue":"4","key":"pone.0296132.ref002","doi-asserted-by":"crossref","DOI":"10.1099\/00207713-31-4-396","article-title":"Edwardsiella ictaluri sp. nov., the Causative Agent of Enteric Septicemia of Catfish","volume":"31","author":"JP Hawke","year":"1981","journal-title":"International Journal of Systematic Bacteriology"},{"key":"pone.0296132.ref003","first-page":"405","volume-title":"Infectious diseases in channel catfish culture","author":"JR MacMillan","year":"1985"},{"key":"pone.0296132.ref004","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1111\/j.1365-2761.1989.tb00322.x","article-title":"Pathology of experimental enteric septicemia in channel catfish, Ictalurus punctatus (Rafinesque), following immersion-exposure to Edwardsiella ictaluri","volume":"12","author":"JC Newton","year":"1989","journal-title":"Journal of Fish Disease"},{"issue":"1","key":"pone.0296132.ref005","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1139\/f86-005","article-title":"Pathogenesis of Experimental Edwardsiella ictaluri Infections in Channel Catfish (Icta lurus punctatus)","volume":"43","author":"EB Shotts","year":"1986","journal-title":"Canadian Journal of Fisheries and Aquatic Sciences"},{"issue":"4","key":"pone.0296132.ref006","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1111\/j.1365-2761.1985.tb00961.x","article-title":"Histopathology of Edwardsiella ictaluri in channel catfish, Ictalurus punctatus (Rafinesque)","volume":"8","author":"T Miyazaki","year":"1985","journal-title":"Journal of Fish Diseases"},{"issue":"3","key":"pone.0296132.ref007","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1577\/1548-8667(1993)005<0189:POESOC>2.3.CO;2","article-title":"Pathogenesis of Enteric Septicemia of Channel Catfish, Caused by Edwardsiella ictaluri: Bacteriologic and Light and Electron Microscopic Findings","volume":"5","author":"TJ Baldwin","year":"1993","journal-title":"Journal of Aquatic Animal Health"},{"key":"pone.0296132.ref008","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1577\/H05-025.1","article-title":"Intracellular replication of Edwardsiella ictaluri in channel catfish macrophages","volume":"18","author":"NJ Booth","year":"2006","journal-title":"Journal of Aquatic Animal Health"},{"issue":"2","key":"pone.0296132.ref009","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/S0165-2427(97)00026-3","article-title":"Killing of Edwardsiella ictaluri by macrophages from channel catfish immune and susceptible to enteric septicemia of catfish","volume":"58","author":"CA Shoemaker","year":"1997","journal-title":"Veterinary immunology and immunopathology"},{"issue":"2","key":"pone.0296132.ref010","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/0145-305X(90)90091-R","article-title":"Differences in the phagocytosis of four bacteria by channel catfish neutrophils","volume":"14","author":"AJ Ainsworth","year":"1990","journal-title":"Developmental and comparative immunology"},{"issue":"13","key":"pone.0296132.ref011","doi-asserted-by":"crossref","first-page":"4293","DOI":"10.1128\/AEM.00195-11","article-title":"Regulation of the Edwardsiella ictaluri type III secretion system by pH and phosphate concentration through EsrA, EsrB, and EsrC","volume":"77","author":"ML Rogge","year":"2011","journal-title":"Applied and environmental microbiology"},{"issue":"1\u20132","key":"pone.0296132.ref012","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.vetmic.2013.05.023","article-title":"Roles of plasmid-encoded proteins, EseH, EseI and EscD in invasion, replication and virulence of Edwardsiella ictaluri","volume":"166","author":"LJ Zhao","year":"2013","journal-title":"Veterinary microbiology"},{"issue":"3","key":"pone.0296132.ref013","doi-asserted-by":"crossref","DOI":"10.1128\/mSphere.00039-16","article-title":"Identification and Characterization of Putative Translocated Effector Proteins of the Edwardsiella ictaluri Type III Secretion System","volume":"1","author":"LP Dubytska","year":"2016","journal-title":"mSphere"},{"issue":"24","key":"pone.0296132.ref014","doi-asserted-by":"crossref","first-page":"7934","DOI":"10.1128\/AEM.01115-07","article-title":"Signature-tagged mutagenesis of Edwardsiella ictaluri identifies virulence-related genes, including a salmonella pathogenicity island 2 class of type III secretion systems","volume":"73","author":"RL Thune","year":"2007","journal-title":"Applied and environmental microbiology"},{"issue":"7","key":"pone.0296132.ref015","doi-asserted-by":"crossref","first-page":"2166","DOI":"10.1128\/AEM.02449-08","article-title":"High-throughput bioluminescence-based mutant screening strategy for identification of bacterial virulence genes","volume":"75","author":"A Karsi","year":"2009","journal-title":"Applied and environmental microbiology"},{"issue":"5","key":"pone.0296132.ref016","doi-asserted-by":"crossref","first-page":"1528","DOI":"10.1073\/pnas.0510322103","article-title":"Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system","volume":"103","author":"S Pukatzki","year":"2006","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"11","key":"pone.0296132.ref017","doi-asserted-by":"crossref","first-page":"4067","DOI":"10.1073\/pnas.0901205106","article-title":"Structural similarity of tailed phages and pathogenic bacterial secretion systems","volume":"106","author":"S. Kanamaru","year":"2009","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"5","key":"pone.0296132.ref018","doi-asserted-by":"crossref","first-page":"1192","DOI":"10.1111\/j.1365-2958.2007.05993.x","article-title":"Dissection of a type VI secretion system in Edwardsiella tarda","volume":"66","author":"J Zheng","year":"2007","journal-title":"Molecular microbiology"},{"issue":"2","key":"pone.0296132.ref019","article-title":"Comparative genomics of the fish pathogens Edwardsiella ictaluri 93\u2013146 and Edwardsiella piscicida C07-087","volume":"6","author":"HC Tekedar","year":"2020","journal-title":"Microb Genom"},{"key":"pone.0296132.ref020","doi-asserted-by":"crossref","first-page":"1819","DOI":"10.3389\/fmicb.2018.01819","article-title":"Development and Characterization of a Novel Live Attenuated Vaccine Against Enteric Septicemia of Catfish","volume":"9","author":"H Abdelhamed","year":"2018","journal-title":"Front Microbiol"},{"issue":"8","key":"pone.0296132.ref021","doi-asserted-by":"crossref","first-page":"1664","DOI":"10.1016\/j.bbamcr.2014.03.018","article-title":"Architecture and assembly of the Type VI secretion system","volume":"1843","author":"A Zoued","year":"2014","journal-title":"Biochim Biophys Acta"},{"issue":"2","key":"pone.0296132.ref022","doi-asserted-by":"crossref","first-page":"93","DOI":"10.3354\/dao052093","article-title":"Cloning and characterization of Edwardsiella ictaluri proteins expressed and recognized by the channel catfish Ictalurus punctatus immune response during infection","volume":"52","author":"MM Moore","year":"2002","journal-title":"Diseases of aquatic organisms"},{"issue":"8","key":"pone.0296132.ref023","doi-asserted-by":"crossref","first-page":"2689","DOI":"10.1128\/IAI.00013-12","article-title":"Fur-regulated iron uptake system of Edwardsiella ictaluri and its influence on pathogenesis and immunogenicity in the catfish host","volume":"80","author":"J Santander","year":"2012","journal-title":"Infection and immunity"},{"key":"pone.0296132.ref024","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.mib.2015.11.006","article-title":"Type VI secretion and anti-host effectors","volume":"29","author":"A Hachani","year":"2016","journal-title":"Current opinion in microbiology"},{"issue":"2","key":"pone.0296132.ref025","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1111\/j.1365-2958.2004.04123.x","article-title":"Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis","volume":"53","author":"PS Rao","year":"2004","journal-title":"Molecular microbiology"},{"issue":"11","key":"pone.0296132.ref026","doi-asserted-by":"crossref","first-page":"e110810","DOI":"10.1371\/journal.pone.0110810","article-title":"A disordered region in the EvpP protein from the type VI secretion system of Edwardsiella tarda is essential for EvpC binding","volume":"9","author":"W Hu","year":"2014","journal-title":"PloS one"},{"issue":"1","key":"pone.0296132.ref027","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.chom.2016.12.004","article-title":"The Bacterial T6SS Effector EvpP Prevents NLRP3 Inflammasome Activation by Inhibiting the Ca2+-Dependent MAPK-Jnk Pathway","volume":"21","author":"H Chen","year":"2017","journal-title":"Cell Host Microbe"},{"issue":"3","key":"pone.0296132.ref028","doi-asserted-by":"crossref","first-page":"e13135","DOI":"10.1111\/cmi.13135","article-title":"Edwardsiella ictaluri evpP is required for colonisation of channel catfish ovary cells and necrosis in anterior kidney macrophages","volume":"22","author":"S Kalindamar","year":"2020","journal-title":"Cell Microbiol"},{"issue":"50","key":"pone.0296132.ref029","doi-asserted-by":"crossref","first-page":"38876","DOI":"10.1074\/jbc.M110.179150","article-title":"Temperature and Mg2+ sensing by a novel PhoP-PhoQ two-component system for regulation of virulence in Edwardsiella tarda","volume":"285","author":"S Chakraborty","year":"2010","journal-title":"The Journal of biological chemistry"},{"issue":"45","key":"pone.0296132.ref030","doi-asserted-by":"crossref","first-page":"39417","DOI":"10.1074\/jbc.M111.295188","article-title":"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","volume":"286","author":"S Chakraborty","year":"2011","journal-title":"The Journal of biological chemistry"},{"key":"pone.0296132.ref031","doi-asserted-by":"crossref","first-page":"681609","DOI":"10.3389\/fvets.2021.681609","article-title":"Hemolysin Co-regulated Family Proteins Hcp1 and Hcp2 Contribute to Edwardsiella ictaluri Pathogenesis","volume":"8","author":"S Kalindamar","year":"2021","journal-title":"Front Vet Sci"},{"issue":"3","key":"pone.0296132.ref032","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1128\/JB.06522-11","article-title":"Genome sequence of Edwardsiella ictaluri 93\u2013146, a strain associated with a natural channel catfish outbreak of enteric septicemia of catfish","volume":"194","author":"ML Williams","year":"2012","journal-title":"J Bacteriol"},{"issue":"1","key":"pone.0296132.ref033","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/0378-1119(89)90359-4","article-title":"Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension","volume":"77","author":"RM Horton","year":"1989","journal-title":"Gene"},{"issue":"3","key":"pone.0296132.ref034","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.plasmid.2006.11.002","article-title":"Broad host range fluorescence and bioluminescence expression vectors for Gram-negative bacteria","volume":"57","author":"A Karsi","year":"2007","journal-title":"Plasmid"},{"issue":"21","key":"pone.0296132.ref035","doi-asserted-by":"crossref","first-page":"6712","DOI":"10.1128\/AEM.01670-09","article-title":"Edwardsiella ictaluri encodes an acid-activated urease that is required for intracellular replication in channel catfish (Ictalurus punctatus) macrophages","volume":"75","author":"NJ Booth","year":"2009","journal-title":"Applied and environmental microbiology"},{"issue":"3","key":"pone.0296132.ref036","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/j.fsi.2009.02.011","article-title":"In vitro and in vivo interaction of macrophages from vaccinated and non-vaccinated channel catfish (Ictalurus punctatus) to Edwardsiella ictaluri","volume":"26","author":"R Russo","year":"2009","journal-title":"Fish & shellfish immunology"},{"issue":"2638","key":"pone.0296132.ref037","article-title":"Phagocytic and Bactericidal Properties of Channel Catfish Peritoneal Macrophages Exposed to Edwardsiella ictaluri Live Attenuated Vaccine and Wild-Type Strains","volume":"8","author":"AO Kordon","year":"2018","journal-title":"Frontiers in Microbiology"},{"issue":"Pt 7","key":"pone.0296132.ref038","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1099\/mic.0.066639-0","article-title":"Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence","volume":"159","author":"J Santander","year":"2013","journal-title":"Microbiology"},{"issue":"3","key":"pone.0296132.ref039","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1128\/aem.62.3.848-852.1996","article-title":"Development of a Defined Minimal Medium for the Growth of Edwardsiella ictaluri","volume":"62","author":"LA Collins","year":"1996","journal-title":"Applied and environmental microbiology"},{"key":"pone.0296132.ref040","first-page":"168","article-title":"Presence and absence of type VI secretion systems in bacteria","author":"R Unni","year":"2022","journal-title":"Microbiology (Reading)"},{"issue":"10","key":"pone.0296132.ref041","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0140743","article-title":"Type Six Secretion System of Bordetella bronchiseptica and Adaptive Immune Components Limit Intracellular Survival During Infection","volume":"10","author":"L Bendor","year":"2015","journal-title":"PloS one"},{"issue":"7","key":"pone.0296132.ref042","doi-asserted-by":"crossref","first-page":"4338","DOI":"10.1128\/IAI.73.7.4338-4345.2005","article-title":"sciS, an icmF homolog in Salmonella enterica serovar Typhimurium, limits intracellular replication and decreases virulence","volume":"73","author":"DA Parsons","year":"2005","journal-title":"Infection and immunity"},{"issue":"1","key":"pone.0296132.ref043","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1128\/IAI.00985-09","article-title":"Burkholderia mallei cluster 1 type VI secretion mutants exhibit growth and actin polymerization defects in RAW 264.7 murine macrophages","volume":"78","author":"MN Burtnick","year":"2010","journal-title":"Infection and immunity"},{"issue":"Pt 10","key":"pone.0296132.ref044","doi-asserted-by":"crossref","first-page":"2954","DOI":"10.1099\/mic.0.050005-0","article-title":"Characterization of IcmF of the type VI secretion system in an avian pathogenic Escherichia coli (APEC) strain","volume":"157","author":"F de Pace","year":"2011","journal-title":"Microbiology"},{"issue":"4","key":"pone.0296132.ref045","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1128\/IAI.01165-12","article-title":"The type VI secretion system encoded in Salmonella pathogenicity island 19 is required for Salmonella enterica serotype Gallinarum survival within infected macrophages","volume":"81","author":"CJ Blondel","year":"2013","journal-title":"Infection and immunity"},{"issue":"6","key":"pone.0296132.ref046","doi-asserted-by":"crossref","first-page":"1996","DOI":"10.1128\/IAI.06205-11","article-title":"Type VI secretion system-associated gene clusters contribute to pathogenesis of Salmonella enterica serovar Typhimurium","volume":"80","author":"DT Mulder","year":"2012","journal-title":"Infection and immunity"},{"issue":"8","key":"pone.0296132.ref047","doi-asserted-by":"crossref","first-page":"e42842","DOI":"10.1371\/journal.pone.0042842","article-title":"Campylobacter jejuni type VI secretion system: roles in adaptation to deoxycholic acid, host cell adherence, invasion, and in vivo colonization","volume":"7","author":"K Lertpiriyapong","year":"2012","journal-title":"PloS one"},{"issue":"10","key":"pone.0296132.ref048","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1007\/s00203-012-0816-z","article-title":"Putative type VI secretion systems of Vibrio parahaemolyticus contribute to adhesion to cultured cell monolayers","volume":"194","author":"Y Yu","year":"2012","journal-title":"Arch Microbiol"},{"issue":"4","key":"pone.0296132.ref049","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.chom.2010.03.004","article-title":"A pathobiont of the microbiota balances host colonization and intestinal inflammation","volume":"7","author":"J Chow","year":"2010","journal-title":"Cell Host Microbe"},{"issue":"9","key":"pone.0296132.ref050","doi-asserted-by":"crossref","first-page":"3867","DOI":"10.1128\/IAI.01769-14","article-title":"Two functional type VI secretion systems in avian pathogenic Escherichia coli are involved in different pathogenic pathways","volume":"82","author":"J Ma","year":"2014","journal-title":"Infection and immunity"},{"key":"pone.0296132.ref051","doi-asserted-by":"crossref","first-page":"32950","DOI":"10.1038\/srep32950","article-title":"Involvement of type VI secretion system in secretion of iron chelator pyoverdine in Pseudomonas taiwanensis","volume":"6","author":"WJ Chen","year":"2016","journal-title":"Sci Rep"},{"issue":"11","key":"pone.0296132.ref052","first-page":"E2233","article-title":"Manganese scavenging and oxidative stress response mediated by type VI secretion system in Burkholderia thailandensis","volume":"114","author":"M Si","year":"2017","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"1","key":"pone.0296132.ref053","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.chom.2013.12.006","article-title":"Disparate impact of oxidative host defenses determines the fate of Salmonella during systemic infection in mice","volume":"15","author":"NA Burton","year":"2014","journal-title":"Cell Host Microbe"},{"issue":"6","key":"pone.0296132.ref054","doi-asserted-by":"crossref","first-page":"2329","DOI":"10.1128\/IAI.01616-13","article-title":"Modulation of Vacuolar pH Is Required for Replication of Edwardsiella ictaluri in Channel Catfish Macrophages","volume":"82","author":"WA Baumgartner","year":"2014","journal-title":"Infection and immunity"},{"issue":"4","key":"pone.0296132.ref055","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.micpath.2007.10.005","article-title":"Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila","volume":"44","author":"G Suarez","year":"2008","journal-title":"Microb Pathog"},{"issue":"9","key":"pone.0296132.ref056","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0138265","article-title":"Differential Role of the T6SS in Acinetobacter baumannii Virulence","volume":"10","author":"GD Repizo","year":"2015","journal-title":"PloS one"},{"issue":"1\u20132","key":"pone.0296132.ref057","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/S0165-2427(01)00331-2","article-title":"Ontogeny of channel catfish lymphoid organs","volume":"81","author":"L Petrie-Hanson","year":"2001","journal-title":"Veterinary immunology and immunopathology"},{"issue":"11","key":"pone.0296132.ref058","doi-asserted-by":"crossref","first-page":"4642","DOI":"10.1128\/iai.65.11.4642-4651.1997","article-title":"Attenuation, persistence, and vaccine potential of an Edwardsiella ictaluri purA mutant","volume":"65","author":"ML Lawrence","year":"1997","journal-title":"Infection and immunity"},{"issue":"11","key":"pone.0296132.ref059","doi-asserted-by":"crossref","first-page":"6557","DOI":"10.1128\/jb.172.11.6557-6567.1990","article-title":"Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gram-negative bacteria","volume":"172","author":"M Herrero","year":"1990","journal-title":"J Bacteriol"},{"issue":"6","key":"pone.0296132.ref060","doi-asserted-by":"crossref","first-page":"2575","DOI":"10.1128\/jb.170.6.2575-2583.1988","article-title":"A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR","volume":"170","author":"VL Miller","year":"1988","journal-title":"J Bacteriol"},{"issue":"1\u20132","key":"pone.0296132.ref061","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0378-1119(94)90776-5","article-title":"Use of the rep technique for allele replacement to construct new Escherichia coli hosts for maintenance of R6K gamma origin plasmids at different copy numbers","volume":"138","author":"WW Metcalf","year":"1994","journal-title":"Gene"},{"issue":"7","key":"pone.0296132.ref062","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1093\/nar\/21.7.1677","article-title":"E. coli host strains significantly affect the quality of small scale plasmid DNA preparations used for sequencing","volume":"21","author":"RG Taylor","year":"1993","journal-title":"Nucleic Acids 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