The transcriptional regulation of the horizontally acquired iron uptake system, yersiniabactin and its contribution to oxidative stress tolerance and pathogenicity of globally emerging salmonella strains

References

• Crump JA, Sjolund-Karlsson M, Gordon MA, Parry CM. clinical epidemiology, presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive salmonella infections. Clin Microbiol Rev. 2015;28(4):901–22. doi:10.1128/CMR.00002-15.
   PubMed Web of Science ®Google Scholar
• Gal-Mor O, Boyle EC, Grassl GA. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front Microbiol. 2014;5:391. doi:10.3389/fmicb.2014.00391.
   PubMed Web of Science ®Google Scholar
• House D, Bishop A, Parry C, Dougan G, Wain J. Typhoid fever: pathogenesis and disease. Curr Opin Infect Dis. 2001;14(5):573–578. doi:10.1097/00001432-200110000-00011.
   PubMed Web of Science ®Google Scholar
• Alvarez DM, Barron-Montenegro R, Conejeros J, Rivera D, Undurraga EA, Moreno-Switt AI. A review of the global emergence of multidrug-resistant Salmonella enterica subsp. enterica Serovar Infantis. Int J Food Microbiol. 2023;403:110297. doi:10.1016/j.ijfoodmicro.2023.110297.
   PubMed Web of Science ®Google Scholar
• Aviv G, Tsyba K, Steck N, Salmon-Divon M, Cornelius A, Rahav G, Grassl GA, Gal‐Mor O. A unique megaplasmid contributes to stress tolerance and pathogenicity of an emergent Salmonella enterica serovar Infantis strain. Environ Microbiol. 2014;16(4):977–994. doi:10.1111/1462-2920.12351.
   PubMed Web of Science ®Google Scholar
• Cohen E, Rahav G, Gal-Mor O, Ochman H. Genome sequence of an emerging salmonella enterica serovar infantis and genomic comparison with other S. infantis strains. Genome Biol Evol. 2020;12(3):151–159. doi:10.1093/gbe/evaa048.
   PubMed Web of Science ®Google Scholar
• Gal-Mor O, Valinsky L, Weinberger M, Guy S, Jaffe J, Schorr YI, Raisfeld A, Agmon V, Nissan I. Multidrug-resistant Salmonella enterica serovar Infantis, Israel. Emerg Infect Dis. 2010;16(11):1754–1757. doi:10.3201/eid1611.100100.
   PubMed Web of Science ®Google Scholar
• Aviv G, Rahav G, Gal-Mor O, Davies JE. Horizontal Transfer of the Salmonella enterica serovar infantis resistance and virulence plasmid pESI to the gut microbiota of warm-blooded hosts. mBio. 2016;7(5). doi:10.1128/mBio.01395-16.
   PubMed Web of Science ®Google Scholar
• Franco A, Leekitcharoenphon P, Feltrin F, Alba P, Cordaro G, Iurescia M, Tolli R, D’Incau M, Staffolani M, Di Giannatale E, et al. Emergence of a clonal lineage of multidrug-resistant esbl-producing salmonella infantis transmitted from broilers and broiler meat to humans in Italy between 2011 and 2014. PLOS ONE. 2015;10(12):e0144802. doi:10.1371/journal.pone.0144802.
   PubMed Web of Science ®Google Scholar
• Mughini-Gras L, van Hoek A, Cuperus T, Dam-Deisz C, van Overbeek W, van den Beld M, Wit B, Rapallini M, Wullings B, Franz E, et al. Prevalence, risk factors and genetic traits of Salmonella Infantis in Dutch broiler flocks. Vet Microbiol. 2021;258:109120. doi:10.1016/j.vetmic.2021.109120.
   PubMed Web of Science ®Google Scholar
• Szmolka A, Szabo M, Kiss J, Paszti J, Adrian E, Olasz F, Nagy B. Molecular epidemiology of the endemic multiresistance plasmid pSI54/04 of Salmonella Infantis in broiler and human population in Hungary. Food Microbiol. 2018;71:25–31. doi:10.1016/j.fm.2017.03.011.
   PubMed Web of Science ®Google Scholar
• Bogomazova AN, Gordeeva VD, Krylova EV, Soltynskaya IV, Davydova EE, Ivanova OE, Komarov AA. Mega-plasmid found worldwide confers multiple antimicrobial resistance in Salmonella Infantis of broiler origin in Russia. Int J Food Microbiol. 2020;319:108497. doi:10.1016/j.ijfoodmicro.2019.108497.
   PubMed Web of Science ®Google Scholar
• Mejia L, Medina JL, Bayas R, Salazar CS, Villavicencio F, Zapata S, Matheu J, Wagenaar JA, González-Candelas F, Vinueza-Burgos C, et al. Genomic Epidemiology of Salmonella Infantis in Ecuador: from Poultry Farms to Human Infections. Front Vet Sci. 2020;7:547891. doi:10.3389/fvets.2020.547891.
   PubMedGoogle Scholar
• Donoso A, Paredes N, Retamal P. Detection of antimicrobial resistant salmonella enterica strains in larval and adult forms of lesser mealworm (Alphitobius diaperinus) from industrial poultry farms. Front Vet Sci. 2020;7:577848. doi:10.3389/fvets.2020.577848.
   PubMed Web of Science ®Google Scholar
• Dos Santos AMP, Panzenhagen P, Ferrari RG, Rodrigues GL, Conte-Junior CA. The pESI megaplasmid conferring virulence and multiple-drug resistance is detected in a Salmonella Infantis genome from Brazil. Infect Genet Evol. 2021;95:104934. doi:10.1016/j.meegid.2021.104934.
   PubMed Web of Science ®Google Scholar
• Papic B, Kusar D, Micunovic J, Pirs M, Ocepek M, Avbersek J, Yang X. Clonal Spread of pESI-Positive Multidrug-Resistant ST32 Salmonella enterica Serovar Infantis Isolates among Broilers and Humans in Slovenia. Microbiol Spectr. 2022;10(6):e0248122. doi:10.1128/spectrum.02481-22.
   PubMed Web of Science ®Google Scholar
• Pietsch M, Simon S, Meinen A, Trost E, Banerji S, Pfeifer Y, Flieger A. Third generation cephalosporin resistance in clinical non-typhoidal Salmonella enterica in Germany and emergence of bla CTX-M-harbouring pESI plasmids. Microb Genom. 2021;7(10). doi:10.1099/mgen.0.000698.
   PubMed Web of Science ®Google Scholar
• Lee WWY, Mattock J, Greig DR, Langridge GC, Baker D, Bloomfield S, Mather AE, Wain JR, Edwards AM, Hartman H, et al. Characterization of a pESI-like plasmid and analysis of multidrug-resistant Salmonella enterica Infantis isolates in England and Wales. Microb Genom. 2021;7(10). doi:10.1099/mgen.0.000658.
   Web of Science ®Google Scholar
• Tyson GH, Li C, Harrison LB, Martin G, Hsu CH, Tate H, Tran T-T, Strain E, Zhao S. A multidrug-resistant salmonella infantis clone is spreading and recombining in the United States. Microb Drug Resist. 2021;27(6):792–799. doi:10.1089/mdr.2020.0389.
   PubMed Web of Science ®Google Scholar
• Alba P, Leekitcharoenphon P, Carfora V, Amoruso R, Cordaro G, Di Matteo P, Ianzano A, Iurescia M, Diaconu EL, Study Group EEAN, et al. Molecular epidemiology of Salmonella Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid. Microb Genom. 2020;6(5):6. doi:10.1099/mgen.0.000365.
   Web of Science ®Google Scholar
• Cohen E, Kriger O, Amit S, Davidovich M, Rahav G, Gal-Mor O. The emergence of a multidrug resistant Salmonella Muenchen in Israel is associated with horizontal acquisition of the epidemic pESI plasmid. Clin Microbiol Infect. 2022;28(11):1499 e7–e14. doi:10.1016/j.cmi.2022.05.029.
   PubMed Web of Science ®Google Scholar
• Dos Santos AMP, Panzenhagen P, Ferrari RG, Conte-Junior CA. Large-scale genomic analysis reveals the pESI-like megaplasmid presence in Salmonella Agona, Muenchen, Schwarzengrund, and Senftenberg. Food Microbiol. 2022;108:104112. doi:10.1016/j.fm.2022.104112.
   PubMed Web of Science ®Google Scholar
• Aviv G, Elpers L, Mikhlin S, Cohen H, Vitman Zilber S, Grassl GA, Rahav G, Hensel M, Gal-Mor O. The plasmid-encoded Ipf and Klf fimbriae display different expression and varying roles in the virulence of Salmonella enterica serovar Infantis in mouse vs. avian hosts. PloS Pathog. 2017;13(8):e1006559. doi:10.1371/journal.ppat.1006559.
   PubMed Web of Science ®Google Scholar
• Andrews SC, Robinson AK, Rodriguez-Quinones F. Bacterial iron homeostasis. FEMS Microbiol Rev. 2003;27(2–3):215–237. doi:10.1016/S0168-6445(03)00055-X.
   PubMed Web of Science ®Google Scholar
• Raymond KN, Dertz EA, Kim SS. Enterobactin: an archetype for microbial iron transport. Proc Natl Acad Sci USA. 2003;100(7):3584–3588. doi:10.1073/pnas.0630018100.
   PubMed Web of Science ®Google Scholar
• Weinberg ED. Nutritional immunity. Host’s attempt to withhold iron from microbial invaders. JAMA. 1975;231(1):39–41. doi:10.1001/jama.1975.03240130021018.
   PubMed Web of Science ®Google Scholar
• Cassat JE, Skaar EP. Iron in infection and immunity. Cell Host Microbe. 2013;13(5):509–519. doi:10.1016/j.chom.2013.04.010.
   PubMed Web of Science ®Google Scholar
• Braun V, Braun M. Active transport of iron and siderophore antibiotics. Curr Opin Microbiol. 2002;5(2):194–201. doi:10.1016/S1369-5274(02)00298-9.
   PubMed Web of Science ®Google Scholar
• Muller SI, Valdebenito M, Hantke K. Salmochelin, the long-overlooked catecholate siderophore of Salmonella. Biometals. 2009;22(4):691–695. doi:10.1007/s10534-009-9217-4.
   PubMed Web of Science ®Google Scholar
• Baumler AJ, Norris TL, Lasco T, Voight W, Reissbrodt R, Rabsch W, Heffron F. IroN, a novel outer membrane siderophore receptor characteristic of Salmonella enterica. J Bacteriol. 1998;180(6):1446–1453. doi:10.1128/JB.180.6.1446-1453.1998.
   PubMed Web of Science ®Google Scholar
• Perry RD, Fetherston JD. Yersiniabactin iron uptake: mechanisms and role in Yersinia pestis pathogenesis. Microbes Infect. 2011;13(10):808–817. doi:10.1016/j.micinf.2011.04.008.
   PubMed Web of Science ®Google Scholar
• Carniel E. The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect. 2001;3(7):561–569. doi:10.1016/S1286-4579(01)01412-5.
   PubMed Web of Science ®Google Scholar
• Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA. 2000;97(12):6640–6645. doi:10.1073/pnas.120163297.
   PubMed Web of Science ®Google Scholar
• Serra-Moreno R, Acosta S, Hernalsteens JP, Jofre J, Muniesa M. Use of the lambda Red recombinase system to produce recombinant prophages carrying antibiotic resistance genes. BMC Mol Biol. 2006;7(1):31. doi:10.1186/1471-2199-7-31.
   PubMedGoogle Scholar
• Aviv G, Gal-Mor O. Usage of a bioluminescence reporter system to image promoter activity during host infection. Methods Mol Biol. 2018;1734:33–38.
   PubMedGoogle Scholar
• Boichis E, Ran Sapir S, Herskovits AA. Bone Marrow-Derived Macrophage (BMDM) Infection by Listeria monocytogenes. Methods Mol Biol. 2022;2427:83–93.
   PubMedGoogle Scholar
• Gal-Mor O, Valdez Y, Finlay BB. The temperature-sensing protein TlpA is repressed by PhoP and dispensable for virulence of Salmonella enterica serovar Typhimurium in mice. Microbes Infect. 2006;8(8):2154–2162. doi:10.1016/j.micinf.2006.04.015.
   PubMed Web of Science ®Google Scholar
• Khajanchi BK, Xu J, Grim CJ, Ottesen AR, Ramachandran P, Foley SL. Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions. BMC Genomics. 2019;20(1):490. doi:10.1186/s12864-019-5768-0.
   PubMedGoogle Scholar
• Peralta DR, Adler C, Corbalan NS, Paz Garcia EC, Pomares MF, Vincent PA, Semsey S. Enterobactin as Part of the Oxidative Stress Response Repertoire. PLoS One. 2016;11(6):e0157799. doi:10.1371/journal.pone.0157799.
   PubMed Web of Science ®Google Scholar
• Achard ME, Chen KW, Sweet MJ, Watts RE, Schroder K, Schembri MA, McEwan A. An antioxidant role for catecholate siderophores in Salmonella. Biochem J. 2013;454(3):543–549. doi:10.1042/BJ20121771.
   PubMedGoogle Scholar
• Saha P, Yeoh BS, Olvera RA, Xiao X, Singh V, Awasthi D, Subramanian BC, Chen Q, Dikshit M, Wang Y, et al. Bacterial Siderophores Hijack Neutrophil Functions. J Immunol. 2017;198(11):4293–4303. doi:10.4049/jimmunol.1700261.
   PubMed Web of Science ®Google Scholar
• Wang S, Phillippy AM, Deng K, Rui X, Li Z, Tortorello ML, Zhang W. Transcriptomic responses of Salmonella enterica serovars Enteritidis and Typhimurium to chlorine-based oxidative stress. Appl Environ Microbiol. 2010;76(15):5013–5024. doi:10.1128/AEM.00823-10.
   PubMed Web of Science ®Google Scholar
• Bauer CE, Elsen S, Bird TH. Mechanisms for redox control of gene expression. Annu Rev Microbiol. 1999;53(1):495–523. doi:10.1146/annurev.micro.53.1.495.
   PubMedGoogle Scholar
• Audia JP, Webb CC, Foster JW. Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria. Int J Med Microbiol. 2001;291(2):97–106. doi:10.1078/1438-4221-00106.
   PubMed Web of Science ®Google Scholar
• de Lorenzo V, Wee S, Herrero M, Neilands JB. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol. 1987;169(6):2624–2630. doi:10.1128/jb.169.6.2624-2630.1987.
   PubMed Web of Science ®Google Scholar
• Munch R, Hiller K, Grote A, Scheer M, Klein J, Schobert M, Jahn D. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics. 2005;21(22):4187–4189. doi:10.1093/bioinformatics/bti635.
   PubMed Web of Science ®Google Scholar
• Katumba GL, Tran H, Henderson JP, Gottesman S. The Yersinia High-Pathogenicity Island Encodes a Siderophore-Dependent Copper Response System in Uropathogenic Escherichia coli. mBio. 2022;13(1):e0239121. doi:10.1128/mBio.02391-21.
   PubMed Web of Science ®Google Scholar
• Anisimov R, Brem D, Heesemann J, Rakin A. Transcriptional regulation of high pathogenicity island iron uptake genes by YbtA. Int J Med Microbiol. 2005;295(1):19–28. doi:10.1016/j.ijmm.2004.11.007.
   PubMed Web of Science ®Google Scholar
• Fetherston JD, Bearden SW, Perry RD. YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor. Mol Microbiol. 1996;22(2):315–325. doi:10.1046/j.1365-2958.1996.00118.x.
   PubMed Web of Science ®Google Scholar
• Paauw A, Leverstein-van Hall MA, van Kessel Kp, Verhoef J, Fluit AC, van Kessel KPM. Yersiniabactin reduces the respiratory oxidative stress response of innate immune cells. PLOS ONE. 2009;4(12):e8240. doi:10.1371/journal.pone.0008240.
   PubMed Web of Science ®Google Scholar
• Brumell JH, Rosenberger CM, Gotto GT, Marcus SL, Finlay BB. SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell Microbiol. 2001;3(2):75–84. doi:10.1046/j.1462-5822.2001.00087.x.
   PubMed Web of Science ®Google Scholar
• Bearden SW, Staggs TM, Perry RD. An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J Bacteriol. 1998;180(5):1135–1147. doi:10.1128/JB.180.5.1135-1147.1998.
   PubMed Web of Science ®Google Scholar
• Lawlor MS, O’Connor C, Miller VL. Yersiniabactin is a virulence factor for Klebsiella pneumoniae during pulmonary infection. Infect Immun. 2007;75(3):1463–1472. doi:10.1128/IAI.00372-06.
   PubMed Web of Science ®Google Scholar
• Schubert S, Picard B, Gouriou S, Heesemann J, Denamur E. Yersinia high-pathogenicity island contributes to virulence in Escherichia coli causing extraintestinal infections. Infect Immun. 2002;70(9):5335–5337. doi:10.1128/IAI.70.9.5335-5337.2002.
   PubMed Web of Science ®Google Scholar
• Riveros M, Garcia W, Garcia C, Durand D, Mercado E, Ruiz J, García C. Molecular and Phenotypic Characterization of Diarrheagenic Escherichia coli Strains Isolated from Bacteremic Children. Am J Trop Med Hyg. 2017;97(5):1329–1336. doi:10.4269/ajtmh.17-0066.
   PubMed Web of Science ®Google Scholar
• Pustam A, Jayaraman J, Ramsubhag A, Shastry RP. Comparative genomics and virulome analysis reveal unique features associated with clinical strains of Klebsiella pneumoniae and Klebsiella quasipneumoniae from Trinidad, West Indies. PLoS One. 2023;18(7):e0283583. doi:10.1371/journal.pone.0283583.
   PubMed Web of Science ®Google Scholar
• Di Pilato V, Henrici De Angelis L, Aiezza N, Baccani I, Niccolai C, Parisio EM, Giordano C, Camarlinghi G, Barnini S, Forni S. et al. Resistome and virulome accretion in an NDM-1-producing ST147 sublineage of Klebsiella pneumoniae associated with an outbreak in Tuscany, Italy: a genotypic and phenotypic characterisation. null null. 2022;3(3):e224–e34. doi:10.1016/S2666-5247(21)00268-8.
   Google Scholar
• Paauw A, Caspers MPM, Leverstein-van Hall MA, Schuren FHJ, Montijn RC, Verhoef J, Fluit AC. Identification of resistance and virulence factors in an epidemic Enterobacter hormaechei outbreak strain. Microbiol (Null). 2009;155(5):1478–1488. doi:10.1099/mic.0.024828-0.
   PubMedGoogle Scholar
• Li Y, Liu Y, Chew SC, Tay M, Salido MM, Teo J, Lauro FM, Givskov M, Yang L. Complete Genome Sequence and Transcriptomic Analysis of the Novel Pathogen Elizabethkingia anophelis in Response to Oxidative Stress. Genome Biol Evol. 2015;7(6):1676–1685. doi:10.1093/gbe/evv101.
   PubMed Web of Science ®Google Scholar
• Anisimov R, Brem D, Heesemann J, Rakin A. Molecular mechanism of YbtA-mediated transcriptional regulation of divergent overlapping promoters ybtA and irp6 of Yersinia enterocolitica. FEMS Microbiol Lett. 2005;250(1):27–32. doi:10.1016/j.femsle.2005.06.040.
   PubMed Web of Science ®Google Scholar
• Gao H, Zhou D, Li Y, Guo Z, Han Y, Song Y, Zhai J, Du Z, Wang X, Lu J, et al. The iron-responsive Fur regulon in Yersinia pestis. J Bacteriol. 2008;190(8):3063–3075. doi:10.1128/JB.01910-07.
   PubMed Web of Science ®Google Scholar
• Rakin A, Noelting C, Schubert S, Heesemann J, Tuomanen EI. Common and specific characteristics of the high-pathogenicity island of Yersinia enterocolitica. Infect Immun. 1999;67(10):5265–5274. doi:10.1128/IAI.67.10.5265-5274.1999.
   PubMed Web of Science ®Google Scholar
• Farr SB, Kogoma T. Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev. 1991;55(4):561–585. doi:10.1128/mr.55.4.561-585.1991.
   PubMedGoogle Scholar
• Troxell B, Hassan HM. Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol. 2013;3:59. doi:10.3389/fcimb.2013.00059.
   PubMed Web of Science ®Google Scholar
• Crouch ML, Castor M, Karlinsey JE, Kalhorn T, Fang FC. Biosynthesis and IroC-dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium. Mol Microbiol. 2008;67(5):971–983. doi:10.1111/j.1365-2958.2007.06089.x.
   PubMed Web of Science ®Google Scholar
• Rabsch W, Methner U, Voigt W, Tschape H, Reissbrodt R, Williams PH. Role of receptor proteins for enterobactin and 2,3-dihydroxybenzoylserine in virulence of Salmonella enterica. Infect Immun. 2003;71(12):6953–6961. doi:10.1128/IAI.71.12.6953-6961.2003.
   PubMed Web of Science ®Google Scholar
• Yancey RJ, Breeding SA, Lankford CE. Enterochelin (enterobactin): virulence factor for Salmonella typhimurium. Infect Immun. 1979;24(1):174–180. doi:10.1128/iai.24.1.174-180.1979.
   PubMed Web of Science ®Google Scholar
• Nagy TA, Moreland SM, Andrews-Polymenis H, Detweiler CS, Payne SM. The ferric enterobactin transporter Fep is required for persistent Salmonella enterica serovar typhimurium infection. Infect Immun. 2013;81(11):4063–4070. doi:10.1128/IAI.00412-13.
   PubMed Web of Science ®Google Scholar
• Furman M, Fica A, Saxena M, Di Fabio JL, Cabello FC. Salmonella typhi iron uptake mutants are attenuated in mice. Infect Immun. 1994;62(9):4091–4094. doi:10.1128/iai.62.9.4091-4094.1994.
   PubMed Web of Science ®Google Scholar
• Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 2010;467(7314):426–429. doi:10.1038/nature09415.
   PubMed Web of Science ®Google Scholar
• Garcia EC, Brumbaugh AR, Mobley HL, Payne SM. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect Immun. 2011;79(3):1225–1235. doi:10.1128/IAI.01222-10.
   PubMed Web of Science ®Google Scholar