{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T04:11:12Z","timestamp":1789186272218,"version":"build-2803163510"},"reference-count":79,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,5,19]],"date-time":"2021-05-19T00:00:00Z","timestamp":1621382400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R21AI156328, R21AI153752, R01AI116917"],"award-info":[{"award-number":["R21AI156328, R21AI153752, R01AI116917"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>The ability of <jats:italic>Salmonella enterica<\/jats:italic> subspecies <jats:italic>enterica<\/jats:italic> serovar Typhi (<jats:italic>S.<\/jats:italic> Typhi) to cause chronic gallbladder infections is dependent on biofilm growth on cholesterol gallstones. Non-typhoidal <jats:italic>Salmonella<\/jats:italic> (e.g. <jats:italic>S.<\/jats:italic> Typhimurium) also utilize the biofilm state to persist in the host and the environment. How the pathogen maintains recalcitrance to the host response, and oxidative stress in particular, during chronic infection is poorly understood. Previous experiments demonstrated that <jats:italic>S<\/jats:italic>. Typhi and <jats:italic>S<\/jats:italic>. Typhimurium biofilms are tolerant to hydrogen peroxide (H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub>), but that mutations in the biofilm extracellular polymeric substances (EPSs) O antigen capsule, colanic acid, or Vi antigen reduce tolerance. Here, biofilm-mediated tolerance to oxidative stress was investigated using a combination of EPS and catalase mutants, as catalases are important detoxifiers of H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub>. Using co-cultured biofilms of wild-type (WT) bacteria with EPS mutants, it was demonstrated that colanic acid in <jats:italic>S<\/jats:italic>. Typhimurium and Vi antigen in <jats:italic>S<\/jats:italic>. Typhi have a community function and protect all biofilm-resident bacteria rather than to only protect the individual cells producing the EPSs. However, the H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> tolerance deficiency of a O antigen capsule mutant was unable to be compensated for by co-culture with WT bacteria. For curli fimbriae, both WT and mutant strains are tolerant to H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> though unexpectedly, co-cultured WT\/mutant biofilms challenged with H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> resulted in sensitization of both strains, suggesting a more nuanced oxidative resistance alteration in these co-cultures. Three catalase mutant (<jats:italic>katE<\/jats:italic>, <jats:italic>katG<\/jats:italic> and a putative catalase) biofilms were also examined, demonstrating significant reductions in biofilm H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> tolerance for the <jats:italic>katE<\/jats:italic> and <jats:italic>katG<\/jats:italic> mutants. Biofilm co-culture experiments demonstrated that catalases exhibit a community function. We further hypothesized that biofilms are tolerant to H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> because the physical barrier formed by EPSs slows penetration of H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> into the biofilm to a rate that can be mitigated by intra-biofilm catalases. Compared to WT, EPS-deficient biofilms have a heighted response even to low-dose (2.5 mM) H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> challenge, confirming that resident bacteria of EPS-deficient biofilms are under greater stress and have limited protection from H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub>. Thus, these data provide an explanation for how <jats:italic>Salmonella<\/jats:italic> achieves tolerance to H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> by a combination of an EPS-mediated barrier and enzymatic detoxification.<\/jats:p>","DOI":"10.3389\/fcimb.2021.683081","type":"journal-article","created":{"date-parts":[[2021,5,19]],"date-time":"2021-05-19T13:16:37Z","timestamp":1621430197000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":47,"title":["Salmonella Biofilms Tolerate Hydrogen Peroxide by a Combination of Extracellular Polymeric Substance Barrier Function and Catalase Enzymes"],"prefix":"10.3389","volume":"11","author":[{"given":"Mark M.","family":"Hahn","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan F.","family":"Gonz\u00e1lez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John S.","family":"Gunn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,5,19]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"3243","DOI":"10.1128\/IAI.00532-16[doi","article-title":"Salmonella Extracellular Matrix Components Influence Biofilm Formation and Gallbladder Colonization","volume":"84","author":"Adcox","year":"2016","journal-title":"Infect. Immun."},{"key":"B2","doi-asserted-by":"publisher","first-page":"2839","DOI":"10.1128\/IAI.71.5.2839-2858.2003","article-title":"Pretreatment of Mice With Streptomycin Provides a Salmonella Enterica Serovar Typhimurium Colitis Model That Allows Analysis of Both Pathogen and Host","volume":"71","author":"Barthel","year":"2003","journal-title":"Infect. Immun."},{"key":"B3","doi-asserted-by":"publisher","first-page":"a010041","DOI":"10.1101\/cshperspect.a010041","article-title":"Host Specificity of Bacterial Pathogens","volume":"3","author":"B\u00e4umler","year":"2013","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"B4","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1016\/j.femsre.2004.09.003","article-title":"The Interaction Between Bacteria and Bile","volume":"29","author":"Begley","year":"2005","journal-title":"FEMS Microbiol. Rev."},{"key":"B5","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1016\/j.it.2014.12.003","article-title":"Exploiting Host Immunity: The Salmonella Paradigm","volume":"36","author":"Behnsen","year":"2015","journal-title":"Trends Immunol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1047","DOI":"10.1172\/JCI117750","article-title":"DNA Repair is More Important Than Catalase for Salmonella Virulence in Mice","volume":"95","author":"Buchmeier","year":"1995","journal-title":"J. Clin. Invest."},{"key":"B7","doi-asserted-by":"publisher","first-page":"e00006","DOI":"10.1128\/mSphere.00006-18","article-title":"Conversion of RpoS\u2013 Attenuated Salmonella Enterica Serovar Typhi Vaccine Strains to RpoS+ Improves Their Resistance to Host Defense Barriers","volume":"3","author":"Burda","year":"2018","journal-title":"mSphere"},{"key":"B8","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/0378-1119(95)00193-A","article-title":"Gene Disruption in Escherichia Coli: TcR and KmR Cassettes With the Option of Flp-catalyzed Excision of the Antibiotic-Resistance Determinant","volume":"158","author":"Cherepanov","year":"1995","journal-title":"Gene"},{"key":"B9","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1038\/sj.icb.7100007","article-title":"Salmonella, the Host and Disease: A Brief Review","volume":"85","author":"Coburn","year":"2007","journal-title":"Immunol. Cell Biol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"2981","DOI":"10.1128\/jb.01620-09","article-title":"Flagellated But Not Hyperfimbriated Salmonella Enterica Serovar Typhimurium Attaches to and Forms Biofilms on Cholesterol-Coated Surfaces","volume":"192","author":"Crawford","year":"2010","journal-title":"J. Bacteriol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"4353","DOI":"10.1073\/pnas.1000862107[doi","article-title":"Gallstones Play a Significant Role in Salmonella Spp. Gallbladder Colonization and Carriage","volume":"107","author":"Crawford","year":"2010","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B12","first-page":"346","article-title":"The Global Burden of Typhoid Fever","volume":"82","author":"Crump","year":"2004","journal-title":"Bull. World Health Organ."},{"key":"B13","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1093\/molbev\/msj036","article-title":"The \u201cDomino Theory\u201d of Gene Death: Gradual and Mass Gene Extinction Events in Three Lineages of Obligate Symbiotic Bacterial Pathogens","volume":"23","author":"Dagan","year":"2006","journal-title":"Mol. Biol. Evol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"6640","DOI":"10.1073\/pnas.120163297[doi","article-title":"One-Step Inactivation of Chromosomal Genes in Escherichia Coli K-12 Using PCR Products","volume":"97","author":"Datsenko","year":"2000","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B15","doi-asserted-by":"publisher","first-page":"11978","DOI":"10.1073\/pnas.89.24.11978","article-title":"The Alternative Sigma Factor katF (rpoS) Regulates Salmonella Virulence","volume":"89","author":"Fang","year":"1992","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1128\/MR.55.4.561-585.1991","article-title":"Oxidative Stress Responses in Escherichia Coli and Salmonella Typhimurium","volume":"55","author":"Farr","year":"1991","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"B17","doi-asserted-by":"publisher","first-page":"5741","DOI":"10.4049\/jimmunol.166.9.5741","article-title":"Salmonella Pathogenicity Island 2-Encoded Type III Secretion System Mediates Exclusion of NADPH Oxidase Assembly From the Phagosomal Membrane","volume":"166","author":"Gallois","year":"2001","journal-title":"J. Immunol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"7722","DOI":"10.1128\/JB.00809-06","article-title":"Salmonella Produces an O-antigen Capsule Regulated by AgfD and Important for Environmental Persistence","volume":"188","author":"Gibson","year":"2006","journal-title":"J. Bacteriol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1038\/s41598-017-18516-2","article-title":"Biofilm Formation Protects Salmonella From the Antibiotic Ciprofloxacin In Vitro and In Vivo in the Mouse Model of Chronic Carriage","volume":"8","author":"Gonz\u00e1lez","year":"2018","journal-title":"Sci. Rep."},{"key":"B20","doi-asserted-by":"publisher","first-page":"2920","DOI":"10.1128\/IAI.00258-13","article-title":"Gallbladder Epithelium as a Niche for Chronic Salmonella Carriage","volume":"81","author":"Gonzalez-Escobedo","year":"2013","journal-title":"Infect. Immun."},{"key":"B21","doi-asserted-by":"publisher","first-page":"nrmicro2490","DOI":"10.1038\/nrmicro2490","article-title":"Chronic and Acute Infection of the Gall Bladder by Salmonella Typhi: Understanding the Carrier State","volume":"9","author":"Gonzalez-Escobedo","year":"2010","journal-title":"Nat. Rev. Microbiol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"e02262","DOI":"10.1128\/mBio.02262-19","article-title":"Establishment of Chronic Typhoid Infection in a Mouse Carriage Model Involves a Type 2 Immune Shift and T and B Cell Recruitment to the Gallbladder","volume":"10","author":"Gonz\u00e1lez","year":"2019","journal-title":"mBio"},{"key":"B23","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1016\/j.jinf.2008.03.012","article-title":"Salmonella Infections in Immunocompromised Adults","volume":"56","author":"Gordon","year":"2008","journal-title":"J.\u00a0Infect."},{"key":"B24","doi-asserted-by":"publisher","first-page":"953","DOI":"10.1086\/651080","article-title":"Invasive non-Typhoid Salmonellae Establish Systemic Intracellular Infection in HIV-infected Adults: An Emerging Disease Pathogenesis","volume":"50","author":"Gordon","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"B25","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1016\/S1286-4579(00)00392-0","article-title":"Mechanisms of Bacterial Resistance and Response to Bile","volume":"2","author":"Gunn","year":"2000","journal-title":"Microbes Infect."},{"key":"B26","doi-asserted-by":"publisher","first-page":"12538","DOI":"10.1074\/jbc.R115.707547[doi","article-title":"What\u2019s on the Outside Matters: The Role of the Extracellular Polymeric Substance of Gram-negative Biofilms in Evading Host Immunity and as a Target for Therapeutic Intervention","volume":"291","author":"Gunn","year":"2016","journal-title":"J. Biol. Chem."},{"key":"B27","doi-asserted-by":"publisher","first-page":"648","DOI":"10.1016\/j.tim.2014.06.007","article-title":"Salmonella Chronic Carriage: Epidemiology, Diagnosis, and Gallbladder Persistence","volume":"22","author":"Gunn","year":"2014","journal-title":"Trends Microbiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"253","DOI":"10.3390\/microorganisms8020253","article-title":"Salmonella Extracellular Polymeric Substances Modulate Innate Phagocyte Activity and Enhance Tolerance of Biofilm-Associated Bacteria to Oxidative Stress","volume":"8","author":"Hahn","year":"2020","journal-title":"Microorganisms"},{"key":"B29","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1016\/j.tibs.2006.07.005","article-title":"Phagocyte-Derived Reactive Species: Salvation or Suicide","volume":"31","author":"Halliwell","year":"2006","journal-title":"Trends Biochem. Sci."},{"key":"B30","first-page":"43","article-title":"In Sickness and in Health: The Relationships Between Bacteria and Bile in the Human Gut","volume-title":"Advances in Applied Microbiology","author":"Hay","year":"2016"},{"key":"B31","doi-asserted-by":"publisher","first-page":"4605","DOI":"10.1128\/JB.00144-09","article-title":"Redundant Hydrogen Peroxide Scavengers Contribute to Salmonella Virulence and Oxidative Stress Resistance","volume":"191","author":"H\u00e9brard","year":"2009","journal-title":"J. Bacteriol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1046\/j.1365-2958.1998.01047.x","article-title":"Genes Encoding Putative Effector Proteins of the Type III Secretion System of Salmonella Pathogenicity Island 2 are Required for Bacterial Virulence and Proliferation in Macrophages","volume":"30","author":"Hensel","year":"1998","journal-title":"Mol. Microbiol."},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1002459","article-title":"Adaptation and Preadaptation of Salmonella Enterica to Bile","volume":"8","author":"Hern\u00e1ndez","year":"2012","journal-title":"PloS Genet."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1787","DOI":"10.1016\/j.celrep.2018.01.016","article-title":"Mechanisms to Evade the Phagocyte Respiratory Burst Arose by Convergent Evolution in Typhoidal Salmonella Serovars","volume":"22","author":"Hiyoshi","year":"2018","journal-title":"Cell Rep."},{"key":"B35","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1034\/j.1600-0854.2002.030301.x","article-title":"Trafficking of the Salmonella Vacuole in Macrophages","volume":"3","author":"Holden","year":"2002","journal-title":"Traffic"},{"key":"B36","doi-asserted-by":"publisher","first-page":"2929","DOI":"10.1128\/JB.01652-09","article-title":"Thiol Peroxidase Protects Salmonella Enterica From Hydrogen Peroxide Stress In Vitro and Facilitates Intracellular Growth","volume":"192","author":"Horst","year":"2010","journal-title":"J. Bacteriol."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2014.00481","article-title":"Salmonella\u2013Host Interactions\u2013Modulation of the Host Innate Immune System","volume":"5","author":"Hurley","year":"2014","journal-title":"Front. Immunol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"5749","DOI":"10.1128\/JB.182.20.5749-5756.2000","article-title":"Identification of RpoS (\u03c2S)-Regulated Genes inSalmonella Enterica Serovar Typhimurium","volume":"182","author":"Ibanez-Ruiz","year":"2000","journal-title":"J. Bacteriol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"1579","DOI":"10.1111\/j.1462-5822.2009.01368.x","article-title":"Salmonella\u2013the Ultimate Insider. Salmonella Virulence Factors That Modulate Intracellular Survival","volume":"11","author":"Ibarra","year":"2009","journal-title":"Cell. Microbiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1146\/annurev.micro.57.030502.090938","article-title":"Pathways of Oxidative Damage","volume":"57","author":"Imlay","year":"2003","journal-title":"Annu. Rev. Microbiol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1016\/S1286-4579(03)00069-8","article-title":"Responses to Reactive Oxygen Intermediates and Virulence of Salmonella Typhimurium","volume":"5","author":"Janssen","year":"2003","journal-title":"Microbes Infect."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/ncomms12748","article-title":"Inhibition of ROS and Upregulation of Inflammatory Cytokines by FoxO3a Promotes Survival Against Salmonella Typhimurium","volume":"7","author":"Joseph","year":"2016","journal-title":"Nat. Commun."},{"key":"B43","doi-asserted-by":"publisher","first-page":"e1001921","DOI":"10.1371\/journal.pmed.1001921","article-title":"World Health Organization Estimates of the Global and Regional Disease Burden of 22 Foodborne Bacterial, Protozoal, and Viral Diseases 2010: A Data Synthesis","volume":"12","author":"Kirk","year":"2015","journal-title":"PloS Med."},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a010306[doi","article-title":"Bacterial Biofilms: Development, Dispersal, and Therapeutic Strategies in the Dawn of the Postantibiotic Era","volume":"3","author":"Kostakioti","year":"2013","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"B45","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1016\/j.imlet.2017.07.006","article-title":"Salmonella Infection: Interplay Between the Bacteria and Host Immune System","volume":"190","author":"Kurtz","year":"2017","journal-title":"Immunol. Lett."},{"key":"B46","doi-asserted-by":"publisher","first-page":"863","DOI":"10.1073\/pnas.1416707112","article-title":"Patterns of Genome Evolution That Have Accompanied Host Adaptation in Salmonella","volume":"112","author":"Langridge","year":"2015","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B47","first-page":"66","article-title":"Bacterial Biofilms Resist Key Host Defenses","volume":"4","author":"Leid","year":"2009","journal-title":"Microbe"},{"key":"B48","doi-asserted-by":"publisher","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\u2013 \u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"B49","doi-asserted-by":"publisher","first-page":"e89243","DOI":"10.1371\/journal.pone.0089243","article-title":"Visualization of Extracellular Matrix Components Within Sectioned Salmonella Biofilms on the Surface of Human Gallstones","volume":"9","author":"Marshall","year":"2014","journal-title":"PloS One"},{"key":"B50","doi-asserted-by":"publisher","first-page":"3946","DOI":"10.1128\/IAI.00634-15[doi","article-title":"The O-Antigen Capsule of Salmonella Enterica Serovar Typhimurium Facilitates Serum Resistance and Surface Expression of Flic","volume":"83","author":"Marshall","year":"2015","journal-title":"Infect. Immun."},{"key":"B51","doi-asserted-by":"publisher","first-page":"1533","DOI":"10.1099\/jmm.0.014092-0","article-title":"Effect of Bile Salts on the DNA and Membrane Integrity of Enteric Bacteria","volume":"58","author":"Merritt","year":"2009","journal-title":"J. Med. Microbiol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/j.ijfoodmicro.2018.05.011","article-title":"Predicting Adhesion and Biofilm Formation Boundaries on Stainless Steel Surfaces by Five Salmonella Enterica Strains Belonging to Different Serovars as a Function of pH, Temperature and NaCl Concentration","volume":"281","author":"Moraes","year":"2018","journal-title":"Int. J. Food Microbiol."},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.00929-14","article-title":"Comparative Analysis of Salmonella Genomes Identifies a Metabolic Network for Escalating Growth in the Inflamed Gut","volume":"5","author":"Nuccio","year":"2014","journal-title":"MBio"},{"key":"B54","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.meegid.2016.08.029","article-title":"Lose to Win: Mart Pseudogenization in Salmonella Enterica Serovar Typhi Contributed to the surV-dependent Survival to H2O2, and Inside Human Macrophage-Like Cells","volume":"45","author":"Ortega","year":"2016","journal-title":"Infect. Genet. Evol."},{"key":"B55","doi-asserted-by":"crossref","DOI":"10.1128\/mBio.00808-17","volume-title":"The Rcs-regulated Colanic Acid Capsule Maintains Membrane Potential in Salmonella Enterica Serovar Typhimurium","author":"Pando","year":"2017"},{"key":"B56","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0203497","article-title":"The ArcAB Two-Component Regulatory System Promotes Resistance to Reactive Oxygen Species and Systemic Infection by Salmonella Typhimurium","volume":"13","author":"Pardo-Est\u00e9","year":"2018","journal-title":"PloS One"},{"key":"B57","doi-asserted-by":"publisher","first-page":"1770","DOI":"10.1056\/NEJMra020201","article-title":"Typhoid Fever","volume":"347","author":"Parry","year":"2002","journal-title":"N. Engl. J. Med."},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0099820","article-title":"Defined Single-Gene and Multi-Gene Deletion Mutant Collections in Salmonella Enterica Sv Typhimurium","volume":"9","author":"Porwollik","year":"2014","journal-title":"PloS One"},{"key":"B59","doi-asserted-by":"publisher","first-page":"775","DOI":"10.1099\/mic.0.26769-0","article-title":"Bile-Salt-Mediated Induction of Antimicrobial and Bile Resistance in Salmonella Typhimurium","volume":"150","author":"Prouty","year":"2004","journal-title":"Microbiology"},{"key":"B60","doi-asserted-by":"publisher","first-page":"3367","DOI":"10.1128\/IAI.73.6.3367-3374.2005","article-title":"The Vi Capsular Antigen of Salmonella Enterica Serotype Typhi Reduces Toll-like Receptor-Dependent Interleukin-8 Expression in the Intestinal Mucosa","volume":"73","author":"Raffatellu","year":"2005","journal-title":"Infect. Immun."},{"key":"B61","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1159\/000496370","article-title":"Salmonella and Reactive Oxygen Species: A Love-Hate Relationship","volume":"11","author":"Rhen","year":"2019","journal-title":"J. Innate Immun."},{"key":"B62","doi-asserted-by":"publisher","first-page":"4352","DOI":"10.1128\/AEM.69.8.4352-4358.2003","article-title":"Characterization of the RpoS Status of Clinical Isolates of Salmonella Enterica","volume":"69","author":"Robbe-Saule","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"B63","doi-asserted-by":"publisher","first-page":"1533","DOI":"10.1046\/j.1365-2958.2001.02340.x","article-title":"Identification of a non-Haem Catalase in Salmonella and its Regulation by RpoS (\u03c3S)","volume":"39","author":"Robbe-Saule","year":"2001","journal-title":"Mol. Microbiol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"600","DOI":"10.1111\/j.1574-6976.2012.00332.x","article-title":"Salmonella\u2019s Long-Term Relationship With its Host","volume":"36","author":"Ruby","year":"2012","journal-title":"FEMS Microbiol. Rev."},{"key":"B65","doi-asserted-by":"publisher","first-page":"108806","DOI":"10.1016\/j.foodres.2019.108806","article-title":"Exploitation of Plant Extracts and Phytochemicals Against Resistant Salmonella Spp. in Biofilms","volume":"128","author":"Sakarikou","year":"2020","journal-title":"Food Res. Int."},{"key":"B66","doi-asserted-by":"publisher","first-page":"1382","DOI":"10.1128\/IAI.00888-06","article-title":"Role of RpoS in Fine-Tuning the Synthesis of Vi Capsular Polysaccharide in Salmonella Enterica Serotype Typhi","volume":"75","author":"Santander","year":"2007","journal-title":"Infect. Immun."},{"key":"B67","doi-asserted-by":"publisher","first-page":"1163","DOI":"10.1128\/AEM.71.3.1163-1168.2005","article-title":"Effect of Heat, Acidification, and Chlorination on Salmonella Enterica Serovar Typhimurium Cells in a Biofilm Formed at the Air-Liquid Interface","volume":"71","author":"Scher","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"B68","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 Years of Image Analysis","volume":"9","author":"Schneider","year":"2012","journal-title":"Nat. Methods"},{"key":"B69","doi-asserted-by":"publisher","first-page":"7173","DOI":"10.1128\/JB.183.24.7173-7181.2001","article-title":"Alkyl Hydroperoxide Reductase is the Primary Scavenger of Endogenous Hydrogen Peroxide in Escherichia Coli","volume":"183","author":"Seaver","year":"2001","journal-title":"J.\u00a0Bacteriol."},{"key":"B70","doi-asserted-by":"publisher","first-page":"17492","DOI":"10.1073\/pnas.0407536101","article-title":"Vi Polysaccharide of Salmonella Typhi Targets the Prohibitin Family of Molecules in Intestinal Epithelial Cells and Suppresses Early Inflammatory Responses","volume":"101","author":"Sharma","year":"2004","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B71","doi-asserted-by":"publisher","first-page":"580","DOI":"10.1111\/j.1365-2958.2011.07612.x","article-title":"How Does the Oxidative Burst of Macrophages Kill Bacteria? Still an Open Question","volume":"80","author":"Slauch","year":"2011","journal-title":"Mol. Microbiol."},{"key":"B72","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1016\/S1473-3099(18)30685-6","article-title":"The Global Burden of Typhoid and Paratyphoid Fevers: A Systematic Analysis for the Global Burden of Disease Study 2017","volume":"19","author":"Stanaway","year":"2019","journal-title":"Lancet Infect. Dis."},{"key":"B73","doi-asserted-by":"publisher","first-page":"1739","DOI":"10.1128\/IAI.63.5.1739-1744.1995","article-title":"Role of Salmonella Typhimurium Mn-superoxide Dismutase (SodA) in Protection Against Early Killing by J774 Macrophages","volume":"63","author":"Tsolis","year":"1995","journal-title":"Infect. Immun."},{"key":"B74","doi-asserted-by":"publisher","first-page":"560","DOI":"10.1073\/pnas.1414569112","article-title":"Direct Measurement of Oxidative and Nitrosative Stress Dynamics in Salmonella Inside Macrophages","volume":"112","author":"van der Heijden","year":"2015","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B75","doi-asserted-by":"publisher","first-page":"1655","DOI":"10.1126\/science.287.5458.1655","article-title":"Salmonella Pathogenicity Island 2-Dependent Evasion of the Phagocyte NADPH Oxidase","volume":"287","author":"Vazquez-Torres","year":"2000","journal-title":"Science"},{"key":"B76","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/S1473-3099(02)00225-6","article-title":"Unlocking the Genome of the Human Typhoid Bacillus","volume":"2","author":"Wain","year":"2002","journal-title":"Lancet Infect. Dis."},{"key":"B77","doi-asserted-by":"publisher","first-page":"ftw090","DOI":"10.1093\/femspd\/ftw090","article-title":"Response of Salmonella Typhi to Bile-Generated Oxidative Stress: Implication of Quorum Sensing and Persister Cell Populations","volume":"74","author":"Walawalkar","year":"2016","journal-title":"Pathog. Dis."},{"key":"B78","doi-asserted-by":"publisher","first-page":"39860","DOI":"10.1074\/jbc.M605898200","article-title":"Modeling the Reactions of Superoxide and Myeloperoxidase in the Neutrophil Phagosome Implications for Microbial Killing","volume":"281","author":"Winterbourn","year":"2006","journal-title":"J. Biol. Chem."},{"key":"B79","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1111\/j.1462-5822.2007.01037.x","article-title":"The Salmonella Enterica Serotype Typhi Regulator TviA Reduces Interleukin-8 Production in Intestinal Epithelial Cells by Repressing Flagellin Secretion","volume":"10","author":"Winter","year":"2008","journal-title":"Cell. Microbiol."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2021.683081\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,19]],"date-time":"2021-05-19T13:16:44Z","timestamp":1621430204000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2021.683081\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,19]]},"references-count":79,"alternative-id":["10.3389\/fcimb.2021.683081"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2021.683081","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,19]]},"article-number":"683081"}}