{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T14:07:25Z","timestamp":1740146845639,"version":"3.37.3"},"reference-count":46,"publisher":"Public Library of Science (PLoS)","issue":"2","license":[{"start":{"date-parts":[[2023,2,23]],"date-time":"2023-02-23T00:00:00Z","timestamp":1677110400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012309","name":"Royal Golden Jubilee (RGJ) Ph.D. Programme","doi-asserted-by":"publisher","award":["PHD\/0070\/2559"],"award-info":[{"award-number":["PHD\/0070\/2559"]}],"id":[{"id":"10.13039\/501100012309","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Siriraj Grant for Research and Development, Faculty of Medicine Siriraj Hospital, Mahidol University."},{"name":"Siriraj Grant for Research and Development, Faculty of Medicine Siriraj Hospital, Mahidol University."},{"name":"Siriraj Grant for Research and Development, Faculty of Medicine Siriraj Hospital, Mahidol University."},{"name":"Biotechnology & Biological Sciences Research Council of the United Kingdom","award":["BBS\/E\/D\/20002173"],"award-info":[{"award-number":["BBS\/E\/D\/20002173"]}]},{"name":"Biotechnology & Biological Sciences Research Council of the United Kingdom","award":["BBS\/E\/D\/20002173"],"award-info":[{"award-number":["BBS\/E\/D\/20002173"]}]},{"name":"Biotechnology & Biological Sciences Research Council of the United Kingdom","award":["BBS\/E\/D\/20002173"],"award-info":[{"award-number":["BBS\/E\/D\/20002173"]}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p><jats:italic>Burkholderia pseudomallei<\/jats:italic> is a facultative intracellular bacterial pathogen that causes melioidosis, a severe invasive disease of humans. We previously reported that the stress-related catecholamine hormone epinephrine enhances motility of <jats:italic>B<\/jats:italic>. <jats:italic>pseudomallei<\/jats:italic>, transcription of flagellar genes and the production of flagellin. It has been reported that the QseBC two-component sensory system regulates motility and virulence-associated genes in other Gram-negative bacteria in response to stress-related catecholamines, albeit disparities between studies exist. We constructed and whole-genome sequenced a mutant of <jats:italic>B<\/jats:italic>. <jats:italic>pseudomallei<\/jats:italic> with a deletion spanning the predicted <jats:italic>qseBC<\/jats:italic> homologues (<jats:italic>bpsl0806<\/jats:italic> and <jats:italic>bpsl0807<\/jats:italic>). The \u0394<jats:italic>qseBC<\/jats:italic> mutant exhibited significantly reduced swimming and swarming motility and reduced transcription of <jats:italic>fliC<\/jats:italic>. It also exhibited a defect in biofilm formation and net intracellular survival in J774A.1 murine macrophage-like cells. While epinephrine enhanced bacterial motility and <jats:italic>fliC<\/jats:italic> transcription, no further reduction in these phenotypes was observed with the \u0394<jats:italic>qseBC<\/jats:italic> mutant in the presence of epinephrine. Plasmid-mediated expression of <jats:italic>qseBC<\/jats:italic> suppressed bacterial growth, complicating attempts to <jats:italic>trans<\/jats:italic>-complement mutant phenotypes. Our data support a role for QseBC in motility, biofilm formation and net intracellular survival of <jats:italic>B<\/jats:italic>. <jats:italic>pseudomallei<\/jats:italic>, but indicate that it is not essential for epinephrine-induced motility <jats:italic>per se<\/jats:italic>.<\/jats:p>","DOI":"10.1371\/journal.pone.0282098","type":"journal-article","created":{"date-parts":[[2023,2,23]],"date-time":"2023-02-23T18:35:02Z","timestamp":1677177302000},"page":"e0282098","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Analysis of the role of the QseBC two-component sensory system in epinephrine-induced motility and intracellular replication of Burkholderia\u00a0pseudomallei"],"prefix":"10.1371","volume":"18","author":[{"given":"Chatruthai","family":"Meethai","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Muthita","family":"Vanaporn","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Narin","family":"Intarak","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Varintip","family":"Lerdsittikul","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Patoo","family":"Withatanung","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sujintana","family":"Janesomboon","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paiboon","family":"Vattanaviboon","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sorujsiri","family":"Chareonsudjai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Toby","family":"Wilkinson","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark P.","family":"Stevens","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joanne M.","family":"Stevens","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4732-0733","authenticated-orcid":true,"given":"Sunee","family":"Korbsrisate","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2023,2,23]]},"reference":[{"key":"pone.0282098.ref001","doi-asserted-by":"crossref","first-page":"17107","DOI":"10.1038\/nrdp.2017.107","article-title":"Melioidosis.","volume":"4","author":"WJ Wiersinga","year":"2018","journal-title":"Nat Rev Dis Primers"},{"issue":"1","key":"pone.0282098.ref002","doi-asserted-by":"crossref","DOI":"10.1038\/nmicrobiol.2015.8","article-title":"Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis","volume":"1","author":"D Limmathurotsakul","year":"2016","journal-title":"Nat Microbiol"},{"issue":"2","key":"pone.0282098.ref003","doi-asserted-by":"crossref","DOI":"10.1128\/CMR.00006-19","article-title":"Human melioidosis.","volume":"33","author":"I Gassiep","year":"2020","journal-title":"Clin Microbiol Rev"},{"key":"pone.0282098.ref004","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1146\/annurev.micro.112408.134030","article-title":"Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis","volume":"64","author":"EE Galyov","year":"2010","journal-title":"Annu Rev Microbiol"},{"key":"pone.0282098.ref005","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.mib.2015.11.007","article-title":"Intracellular replication of the well-armed pathogen Burkholderia pseudomallei","volume":"29","author":"SJ Willcocks","year":"2016","journal-title":"Curr Opin Microbiol"},{"issue":"3","key":"pone.0282098.ref006","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1046\/j.1365-2958.2002.03190.x","article-title":"An Inv\/Mxi-Spa-like type III protein secretion system in Burkholderia pseudomallei modulates intracellular behaviour of the pathogen","volume":"46","author":"MP Stevens","year":"2002","journal-title":"Mol Microbiol"},{"issue":"7","key":"pone.0282098.ref007","doi-asserted-by":"crossref","DOI":"10.1128\/IAI.00927-19","article-title":"Regulation of virulence by two-component systems in pathogenic Burkholderia","volume":"88","author":"MM Schaefers","year":"2020","journal-title":"Infect Immun"},{"key":"pone.0282098.ref008","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1186\/s12864-016-2668-4","article-title":"Perturbation of the two-component signal transduction system, BprRS, results in attenuated virulence and motility defects in Burkholderia pseudomallei","volume":"17","author":"NR Lazar Adler","year":"2016","journal-title":"BMC Genomics"},{"issue":"5","key":"pone.0282098.ref009","doi-asserted-by":"crossref","first-page":"2079","DOI":"10.1128\/IAI.01233-10","article-title":"Dictyostelium discoideum as a model system for identification of Burkholderia pseudomallei virulence factors","volume":"79","author":"BM Hasselbring","year":"2011","journal-title":"Infect Immun"},{"issue":"1","key":"pone.0282098.ref010","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.chom.2015.06.002","article-title":"Host cytosolic glutathione sensing by a membrane histidine kinase activates the type VI secretion system in an intracellular bacterium","volume":"18","author":"J Wong","year":"2015","journal-title":"Cell Host Microbe"},{"issue":"3","key":"pone.0282098.ref011","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1046\/j.1365-2958.2002.02803.x","article-title":"Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli","volume":"43","author":"V Sperandio","year":"2002","journal-title":"Mol Microbiol"},{"issue":"27","key":"pone.0282098.ref012","doi-asserted-by":"crossref","first-page":"10420","DOI":"10.1073\/pnas.0604343103","article-title":"The QseC sensor kinase: a bacterial adrenergic receptor","volume":"103","author":"MB Clarke","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"8","key":"pone.0282098.ref013","doi-asserted-by":"crossref","first-page":"e1000553","DOI":"10.1371\/journal.ppat.1000553","article-title":"The QseC adrenergic signaling cascade in Enterohemorrhagic E. coli (EHEC).","volume":"5","author":"DT Hughes","year":"2009","journal-title":"PLoS Pathog"},{"issue":"1","key":"pone.0282098.ref014","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1007\/s12013-014-9924-5","article-title":"The role of the qseC quorum-sensing sensor kinase in epinephrine-enhanced motility and biofilm formation by Escherichia coli","volume":"70","author":"K Yang","year":"2014","journal-title":"Cell Biochem Biophys"},{"key":"pone.0282098.ref015","doi-asserted-by":"crossref","first-page":"e8833","DOI":"10.7717\/peerj.8833","article-title":"QseBC is involved in the biofilm formation and antibiotic resistance in Escherichia coli isolated from bovine mastitis","volume":"8","author":"W Li","year":"2020","journal-title":"PeerJ"},{"issue":"6","key":"pone.0282098.ref016","doi-asserted-by":"crossref","first-page":"1882","DOI":"10.1128\/AEM.03198-13","article-title":"Escherichia coli O157:H7 lacking the qseBC-encoded quorum-sensing system outcompetes the parental strain in colonization of cattle intestines","volume":"80","author":"VK Sharma","year":"2014","journal-title":"Appl Environ Microbiol"},{"key":"pone.0282098.ref017","article-title":"Characterisation of the E. coli and Salmonella qseC and qseE mutants reveals a metabolic rather than adrenergic receptor role","author":"A Hamed","year":"2022","journal-title":"FEMS Microbiol Lett"},{"issue":"4","key":"pone.0282098.ref018","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/j.micpath.2007.10.001","article-title":"The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium","volume":"44","author":"BL Bearson","year":"2008","journal-title":"Microb Pathog"},{"issue":"12","key":"pone.0282098.ref019","doi-asserted-by":"crossref","first-page":"4344","DOI":"10.1128\/IAI.00803-12","article-title":"Interplay between the qseC and qseE bacterial adrenergic sensor kinases in Salmonella enterica serovar Typhimurium pathogenesis","volume":"80","author":"CG Moreira","year":"2012","journal-title":"Infect Immun"},{"issue":"3","key":"pone.0282098.ref020","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1128\/IAI.01038-09","article-title":"QseC mediates Salmonella enterica serovar Typhimurium virulence in vitro and in vivo","volume":"78","author":"CG Moreira","year":"2010","journal-title":"Infect Immun"},{"issue":"1","key":"pone.0282098.ref021","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1128\/IAI.01203-09","article-title":"Norepinephrine augments Salmonella enterica-induced enteritis in a manner associated with increased net replication but independent of the putative adrenergic sensor kinases qseC and qseE","volume":"78","author":"GD Pullinger","year":"2010","journal-title":"Infect Immun"},{"issue":"1","key":"pone.0282098.ref022","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1111\/2049-632X.12181","article-title":"Growth, motility and resistance to oxidative stress of the melioidosis pathogen Burkholderia pseudomallei are enhanced by epinephrine","volume":"72","author":"N Intarak","year":"2014","journal-title":"Pathog Dis"},{"issue":"39","key":"pone.0282098.ref023","doi-asserted-by":"crossref","first-page":"14240","DOI":"10.1073\/pnas.0403302101","article-title":"Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei","volume":"101","author":"MT Holden","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"20","key":"pone.0282098.ref024","doi-asserted-by":"crossref","first-page":"6496","DOI":"10.1128\/AEM.01669-09","article-title":"Versatile dual-technology system for markerless allele replacement in Burkholderia pseudomallei","volume":"75","author":"CM Lopez","year":"2009","journal-title":"Appl Environ Microbiol"},{"article-title":"FastQC: a quality control tool for high throughput 550 sequence data babraham bioinformatics","year":"2010","author":"S. Andrews","key":"pone.0282098.ref025"},{"issue":"11","key":"pone.0282098.ref026","doi-asserted-by":"crossref","first-page":"e112963","DOI":"10.1371\/journal.pone.0112963","article-title":"Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement","volume":"9","author":"BJ Walker","year":"2014","journal-title":"PLoS One"},{"issue":"2","key":"pone.0282098.ref027","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.plasmid.2013.04.001","article-title":"Improvement of pBBR1MCS plasmids, a very useful series of broad-host-range cloning vectors","volume":"70","author":"S Obranic","year":"2013","journal-title":"Plasmid"},{"issue":"4","key":"pone.0282098.ref028","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1128\/JB.183.4.1195-1204.2001","article-title":"Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities","volume":"183","author":"E Deziel","year":"2001","journal-title":"J Bacteriol"},{"key":"pone.0282098.ref029","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1007\/978-1-4939-2854-5_5","article-title":"A microplate-based system as in vitro model of biofilm growth and quantification","volume":"1333","author":"I Vandecandelaere","year":"2016","journal-title":"Methods Mol Biol"},{"issue":"4","key":"pone.0282098.ref030","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"KJ Livak","year":"2001","journal-title":"Methods"},{"issue":"8","key":"pone.0282098.ref031","doi-asserted-by":"crossref","DOI":"10.1128\/JB.00861-16","article-title":"Genetic and mechanistic analyses of the periplasmic domain of the enterohemorrhagic Escherichia coli qseC Histidine Sensor Kinase","volume":"199","author":"CT Parker","year":"2017","journal-title":"J Bacteriol"},{"issue":"9","key":"pone.0282098.ref032","doi-asserted-by":"crossref","first-page":"e1003795","DOI":"10.1371\/journal.pgen.1003795","article-title":"The condition-dependent transcriptional landscape of Burkholderia pseudomallei","volume":"9","author":"WF Ooi","year":"2013","journal-title":"PLoS Genet"},{"issue":"17","key":"pone.0282098.ref033","doi-asserted-by":"crossref","first-page":"5301","DOI":"10.1128\/JB.185.17.5301-5305.2003","article-title":"High-frequency secondary mutations after suicide-driven allelic exchange mutagenesis in extraintestinal pathogenic Escherichia coli","volume":"185","author":"JR Johnson","year":"2003","journal-title":"J Bacteriol"},{"issue":"3","key":"pone.0282098.ref034","doi-asserted-by":"crossref","first-page":"e0121052","DOI":"10.1371\/journal.pone.0121052","article-title":"Genomic characterization of Burkholderia pseudomallei isolates selected for medical countermeasures testing: comparative genomics associated with differential virulence","volume":"10","author":"JW Sahl","year":"2015","journal-title":"PLoS One"},{"issue":"9","key":"pone.0282098.ref035","doi-asserted-by":"crossref","DOI":"10.1128\/MRA.01529-18","article-title":"Genome resequencing of laboratory stocks of Burkholderia pseudomallei K96243","volume":"8","author":"S Wagley","year":"2019","journal-title":"Microbiol Resour Announc"},{"key":"pone.0282098.ref036","doi-asserted-by":"crossref","first-page":"145374","DOI":"10.1016\/j.gene.2020.145374","article-title":"The Escherichia coli qseB\/qseC signaling is required for correct timing of replication initiation and cell motility","volume":"773","author":"D Wu","year":"2021","journal-title":"Gene"},{"issue":"2","key":"pone.0282098.ref037","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1111\/j.1365-2958.2008.06170.x","article-title":"FliL is essential for swarming: motor rotation in absence of fliL fractures the flagellar rod in swarmer cells of Salmonella enterica","volume":"68","author":"U Attmannspacher","year":"2008","journal-title":"Mol Microbiol"},{"issue":"2","key":"pone.0282098.ref038","article-title":"Bacterial biofilm and its role in the pathogenesis of disease","volume":"9","author":"LK Vestby","year":"2020","journal-title":"Antibiotics (Basel)."},{"issue":"6","key":"pone.0282098.ref039","doi-asserted-by":"crossref","first-page":"e0005689","DOI":"10.1371\/journal.pntd.0005689","article-title":"Genome-scale analysis of the genes that contribute to Burkholderia pseudomallei biofilm formation identifies a crucial exopolysaccharide biosynthesis gene cluster","volume":"11","author":"GI Borlee","year":"2017","journal-title":"PLoS Negl Trop Dis"},{"key":"pone.0282098.ref040","doi-asserted-by":"crossref","first-page":"212","DOI":"10.3389\/fmicb.2018.00212","article-title":"QseC mediates osmotic stress resistance and biofilm formation in Haemophilus parasuis.","volume":"9","author":"L He","year":"2018","journal-title":"Front Microbiol"},{"issue":"7","key":"pone.0282098.ref041","doi-asserted-by":"crossref","first-page":"2919","DOI":"10.1128\/IAI.01376-09","article-title":"Autoinducer-2 and qseC control biofilm formation and in vivo virulence of Aggregatibacter actinomycetemcomitans","volume":"78","author":"EA Novak","year":"2010","journal-title":"Infect Immun"},{"key":"pone.0282098.ref042","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.micpath.2017.01.010","article-title":"QseB mediates biofilm formation and invasion in Salmonella enterica serovar Typhi","volume":"104","author":"Y Ji","year":"2017","journal-title":"Microb Pathog"},{"key":"pone.0282098.ref043","doi-asserted-by":"crossref","first-page":"108603","DOI":"10.1016\/j.vetmic.2020.108603","article-title":"Disruption of the Burkholderia pseudomallei two-component signal transduction system BbeR-BbeS leads to increased extracellular DNA secretion and altered biofilm formation","volume":"242","author":"PA Alwis","year":"2020","journal-title":"Vet Microbiol"},{"issue":"4","key":"pone.0282098.ref044","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1038\/nrmicro1385","article-title":"Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei","volume":"4","author":"WJ Wiersinga","year":"2006","journal-title":"Nat Rev Microbiol"},{"issue":"12","key":"pone.0282098.ref045","doi-asserted-by":"crossref","first-page":"e0143916","DOI":"10.1371\/journal.pone.0143916","article-title":"The Burkholderia pseudomallei proteins BapA and BapC are secreted TTSS3 effectors and BapB levels modulate expression of bopE","volume":"10","author":"P Treerat","year":"2015","journal-title":"PLoS One"},{"issue":"3","key":"pone.0282098.ref046","doi-asserted-by":"crossref","first-page":"944","DOI":"10.1016\/j.fsi.2011.01.019","article-title":"QseBC controls flagellar motility, fimbrial hemagglutination and intracellular virulence in fish pathogen Edwardsiella tarda","volume":"30","author":"X Wang","year":"2011","journal-title":"Fish Shellfish Immunol"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0282098","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,23]],"date-time":"2023-02-23T18:35:41Z","timestamp":1677177341000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0282098"}},"subtitle":[],"editor":[{"given":"Christopher","family":"Rao","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2023,2,23]]},"references-count":46,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2,23]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0282098","relation":{},"ISSN":["1932-6203"],"issn-type":[{"type":"electronic","value":"1932-6203"}],"subject":[],"published":{"date-parts":[[2023,2,23]]}}}