Genomic Approaches for Understanding the Characteristics of Salmonella enterica subsp. enterica Serovar Typhimurium ST1120, Isolated from Swine Feces in Korea

Seongok  Kim; Eunsuk  Kim; Soyeon  Park; Tae-Wook  Hahn; Hyunjin  Yoon

doi:10.4014/jmb.1708.08027

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Research article

Food Microbiology and Biotechnology (FMB) | Probiotics and Foodborne Microorganisms

Genomic Approaches for Understanding the Characteristics of Salmonella enterica subsp. enterica Serovar Typhimurium ST1120, Isolated from Swine Feces in Korea

Seongok Kim ¹, Eunsuk Kim ¹, Soyeon Park ², Tae-Wook Hahn ² and Hyunjin Yoon ^{1, 3*}

¹Department of Molecular Science and Technology, Ajou University, Suwon 16499, Republic of Korea, ²College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University, Chuncheon 24341, Republic of Korea, ³Department of Applied Chemistry and Biological Engineering, Ajou University, Suwon 16499, Republic of Korea

Received: August 11, 2017; Accepted: September 17, 2017

J. Microbiol. Biotechnol. 2017; 27(11): 1983-1993

Published November 28, 2017 https://doi.org/10.4014/jmb.1708.08027

Abstract

Salmonella enterica subsp. enterica serovar Typhimurium, one of the most common foodborne pathogens, is transmitted mainly through contaminated food derived from infected animals. In this study, S. Typhimurium ST1120, an isolate from pig feces in Korea, was subjected to whole-genome analysis to understand its genomic features associated with virulence. The genome of ST1120 was found to have a circular chromosome of 4,855,001 bp (GC content 52.2%) and a plasmid of 6,863 bp (GC content 46.0%). This chromosome was predicted to have 4,558 open reading frames (ORFs), 17 pseudogenes, 22 rRNA genes, and 86 tRNA genes. Its plasmid was predicted to have three ORFs. Comparative genome analysis revealed that ST1120 was phylogenetically close to S. Typhimurium U288, a critical isolate in piggery farms and food chains in Europe. In silico functional analysis predicted that the ST1120 genome harbored multiple genes associated with virulence and stress resistance, including Salmonella pathogenicity islands (SPIs containing SPI-1 to SPI-5, SPI-13, and SPI-14), C63PI locus, ST104 prophage locus, and various antibiotic resistance genes. In accordance with these analysis results, ST1120 showed competence in invasion and survival abilities when it was added to host cells. It also exhibited robust resistance against antibiotics in comparison with other S. Typhimurium strains. This is the first report of the complete genome sequence of S. Typhimurium isolated from swine in Korea. Comparative genome analysis between ST1120 and other Salmonella strains would provide fruitful information toward understanding Salmonella host specificity and developing control measures against S. Typhimurium infection.

Keywords

Salmonella Typhimurium ST1120, piggery, genome, comparative analysis, virulence, antibiotic resistance

References

Timme RE, Pettengill JB, Allard MW, Strain E, Barrangou R, Wehnes C, et al. 2013. Phylogenetic diversity of the enteric pathogen Salmonella enterica subsp. enterica inferred from genome-wide reference-free SNP characters. Genome Biol. Evol. 5: 2109-2123.
CDC. 2007. Bacterial foodborne and diarrheal disease national case surveillance, annual report, 2005. CDC, Atlanta, GA.
Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, et al. 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50: 882-889.
Gal-Mor O, Boyle EC, Grassl GA. 2014. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front. Microbiol. 5: 391.
Kim HB, Yoon M, Lee SJ, Jang YH, Choe NH. 2014. Prevalence and antibiotic resistance characteristics of Salmonella spp. isolated from food-producing animals and meat products in Korea. J. Preventive Vet. Med. 38: 85-93.
Letellier A, Messier S, Quessy S. 1999. Prevalence of Salmonella spp. and Yersinia enterocolitica in finishing swine at Canadian abattoirs. J. Food Prot. 62: 22-25.
Wood RL, Rose R. 1992. Populations of Salmonella typhimurium in internal organs of experimentally infected carrier swine. Am. J. Vet. Res. 53: 653-658.
De Busser EV, Maes D, Houf K, Dewulf J, Imberechts H, Bertrand S, De Zutter L. 2011. Detection and characterization of Salmonella in lairage, on pig carcasses and intestines in five slaughterhouses. Int. J. Food Microbiol. 145: 279-286.
Berends BR, Van Knapen F, Snijders JM, Mossel DA. 1997. Identification and quantification of risk factors regarding Salmonella spp. on pork carcasses. Int. J. Food Microbiol. 36: 199-206.
Aarestrup FM. 2005. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin. Pharmacol. Toxicol. 96: 271-281.
Zhao EY, Bao HX, Tang L, Zou QH, Liu WQ, Zhu DL, et al. 2013. Genomic comparison of Salmonella typhimurium DT104 with non-DT104 strains. Mol. Genet. Genomics 288: 549-557.
Meunier D, Boyd D, Mulvey MR, Baucheron S, Mammina C, Nastasi A, et al. 2002. Salmonella enterica serotype Typhimurium DT 104 antibiotic resistance genomic island I in serotype paratyphi B. Emerg. Infect. Dis. 8: 430-433.
Ju MS, Kang ZW, Jung JH, Cho SB, Kim SH, Lee YJ, et al. 2011. Genotyping, phage typing, and antimicrobial resistance of Salmonella Typhimurium isolated from pigs, cattle, and humans. Korean J. Food Sci. Anim. Resour. 31: 47-53.
Bruun T, Sorensen G, Forshell LP, Jensen T, Nygard K, Kapperud G, et al. 2009. An outbreak of Salmonella Typhimurium infections in Denmark, Norway and Sweden, 2008. Euro Surveill. 14: 19147.
Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, et al. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10: 563-569.
Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30: 2068-2069.
Lukashin AV, Borodovsky M. 1998. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26: 1107-1115.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35: 3100-3108.
Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. 2009. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120.
Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. 2016. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32: 929-931.
Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, et al. 2015. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31: 3691-3693.
Sullivan MJ, Petty NK, Beatson SA. 2011. Easyfig: a genome comparison visualizer. Bioinformatics 27: 1009-1010.
Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the artemis comparison tool. Bioinformatics 21: 3422-3423.
Roer L, Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, Kaas RS, Hasman H, et al. 2016. Is the evolution of Salmonella enterica subsp. enterica linked to restriction-modification systems? mSystems. 1: e00009-e00016.
Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q. 2005. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. 33: D325-D328.
Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. 2017. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 45: D566-D573.
Brumell JH, Rosenberger CM, Gotto GT, Marcus SL, Finlay BB. 2001. SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell. Microbiol. 3: 75-84.
Kim E, Lee S-H, Lee S-J, Kwon O-P, Yoon H. 2017. New antibacterial-core structures based on styryl quinolinium. Food Sci. Biotechnol. 26: 521-529.
Bowe F, Lipps CJ, Tsolis RM, Groisman E, Heffron F, Kusters JG. 1998. At least four percent of the Salmonella typhimurium genome is required for fatal infection of mice. Infect. Immun. 66: 3372-3377.
Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. 2000. Salmonella pathogenicity islands: big virulence in small packages. Microb. Infect. 2: 145-156.
Addwebi TM, Call DR, Shah DH. 2014. Contribution of Salmonella Enteritidis virulence factors to intestinal colonization and systemic dissemination in 1-day-old chickens. Poult. Sci. 93: 871-881.
Elder JR, Chiok KL, Paul NC, Haldorson G, Guard J, Shah DH. 2016. The Salmonella pathogenicity island 13 contributes to pathogenesis in streptomycin pre-treated mice but not in day-old chickens. Gut Pathog. 8: 16.
Boyer E, Bergevin I, Malo D, Gros P, Cellier MF. 2002. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 70: 6032-6042.
Tsolis RM, Baumler AJ, Heffron F. 1995. Role of Salmonella typhimurium Mn-superoxide dismutase (SodA) in protection against early killing by J774 macrophages. Infect. Immun. 63: 1739-1744.
Kehres DG, Janakiraman A, Slauch JM, Maguire ME. 2002. Regulation of Salmonella enterica serovar Typhimurium mntH transcription by H2O2, Fe2+, and Mn2+. J. Bacteriol. 184: 3151-3158.
Horsburgh MJ, Wharton SJ, Karavolos M, Foster SJ. 2002. Manganese: elemental defence for a life with oxygen. Trends Microbiol. 10: 496-501.
Althouse C, Patterson S, Fedorka-Cray P, Isaacson RE. 2003. Type 1 fimbriae of Salmonella enterica serovar Typhimurium bind to enterocytes and contribute to colonization of swine in vivo. Infect. Immun. 71: 6446-6452.
Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, et al. 2015. Secretion systems in gramnegative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13: 343-359.
Baumler AJ, Tsolis RM, Heffron F. 1996. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer’s patches. Proc. Natl. Acad. Sci. USA 93: 279-283.
Brodsky IE, Ghori N, Falkow S, Monack D. 2005. Mig-14 is an inner membrane-associated protein that promotes Salmonella typhimurium resistance to CRAMP, survival within activated macrophages and persistent infection. Mol. Microbiol. 55: 954-972.
Hapfelmeier S, Stecher B, Barthel M, Kremer M, Muller AJ, Heikenwalder M, et al. 2005. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar Typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174: 1675-1685.
Swords WE, Cannon BM, Benjamin WH Jr. 1997. Avirulence of L T2 s trains of Salmonella typhimurium results from a defective rpoS gene. Infect. Immun. 65: 2451-2453.
Wilmes-Riesenberg MR, Foster JW, Curtiss R 3rd. 1997. An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect. Immun. 65: 203-210.
De E, Basle A, Jaquinod M, Saint N, Mallea M, Molle G, et al. 2001. A new mechanism of antibiotic resistance in Enterobacteriaceae induced by a structural modification of the major porin. Mol. Microbiol. 41: 189-198.
Sievers F , Wilm A , Dineen D , Gibson T J, K arplus K , L i W, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7: 539.
Petkau A, Stuart-Edwards M, Stothard P, Van Domselaar G. 2010. Interactive microbial genome visualization with GView. Bioinformatics 26: 3125-3126.
Tanaka K, Nishimori K, Makino S, Nishimori T, Kanno T, Ishihara R, et al. 2004. Molecular characterization of a prophage of Salmonella enterica serotype Typhimurium DT104. J. Clin. Microbiol. 42: 1807-1812.
Reiter WD, Palm P, Yeats S. 1989. Transfer RNA genes frequently serve as integration sites for prokaryotic genetic elements. Nucleic Acids Res. 17: 1907-1914.
Brussow H, Canchaya C, Hardt WD. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68: 560-602.
Allison GE, Verma NK. 2000. Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol. 8: 17-23.
Kim M, Ryu S. 2012. Spontaneous and transient defence against bacteriophage by phase-variable glucosylation of O-antigen in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 86: 411-425.
Duerr CU, Zenk SF, Chassin C, Pott J, Gutle D, Hensel M, et al. 2009. O-Antigen delays lipopolysaccharide recognition and impairs antibacterial host defense in murine intestinal epithelial cells. PLoS Pathog. 5: e1000567.
Reeves P. 1995. Role of O-antigen variation in the immune response. Trends Microbiol. 3: 381-386.
Anjum MF, Choudhary S, Morrison V, Snow LC, Mafura M, Slickers P, et al. 2011. Identifying antimicrobial resistance genes of human clinical relevance within Salmonella isolated from food animals in Great Britain. J. Antimicrob. Chemother. 66: 550-559.
Patterson SK, Borewicz K, Johnson T, Xu W, Isaacson RE. 2012. Characterization and differential gene expression between two phenotypic phase variants in Salmonella enterica serovar Typhimurium. PLoS One 7: e43592.
Fortier LC, Sekulovic O. 2013. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4: 354-365.

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(11): 1983-1993

Published online November 28, 2017 https://doi.org/10.4014/jmb.1708.08027

Genomic Approaches for Understanding the Characteristics of Salmonella enterica subsp. enterica Serovar Typhimurium ST1120, Isolated from Swine Feces in Korea

Seongok Kim ¹, Eunsuk Kim ¹, Soyeon Park ², Tae-Wook Hahn ² and Hyunjin Yoon ^{1, 3*}

¹Department of Molecular Science and Technology, Ajou University, Suwon 16499, Republic of Korea, ²College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University, Chuncheon 24341, Republic of Korea, ³Department of Applied Chemistry and Biological Engineering, Ajou University, Suwon 16499, Republic of Korea

Received: August 11, 2017; Accepted: September 17, 2017

Abstract

Salmonella enterica subsp. enterica serovar Typhimurium, one of the most common foodborne
pathogens, is transmitted mainly through contaminated food derived from infected animals.
In this study, S. Typhimurium ST1120, an isolate from pig feces in Korea, was subjected to
whole-genome analysis to understand its genomic features associated with virulence. The
genome of ST1120 was found to have a circular chromosome of 4,855,001 bp (GC content
52.2%) and a plasmid of 6,863 bp (GC content 46.0%). This chromosome was predicted to have
4,558 open reading frames (ORFs), 17 pseudogenes, 22 rRNA genes, and 86 tRNA genes. Its
plasmid was predicted to have three ORFs. Comparative genome analysis revealed that
ST1120 was phylogenetically close to S. Typhimurium U288, a critical isolate in piggery farms
and food chains in Europe. In silico functional analysis predicted that the ST1120 genome
harbored multiple genes associated with virulence and stress resistance, including Salmonella
pathogenicity islands (SPIs containing SPI-1 to SPI-5, SPI-13, and SPI-14), C63PI locus, ST104
prophage locus, and various antibiotic resistance genes. In accordance with these analysis
results, ST1120 showed competence in invasion and survival abilities when it was added to
host cells. It also exhibited robust resistance against antibiotics in comparison with other
S. Typhimurium strains. This is the first report of the complete genome sequence of
S. Typhimurium isolated from swine in Korea. Comparative genome analysis between ST1120
and other Salmonella strains would provide fruitful information toward understanding
Salmonella host specificity and developing control measures against S. Typhimurium infection.

Keywords: Salmonella Typhimurium ST1120, piggery, genome, comparative analysis, virulence, antibiotic resistance

Abstract

References

Timme RE, Pettengill JB, Allard MW, Strain E, Barrangou R, Wehnes C, et al. 2013. Phylogenetic diversity of the enteric pathogen Salmonella enterica subsp. enterica inferred from genome-wide reference-free SNP characters. Genome Biol. Evol. 5: 2109-2123.
CDC. 2007. Bacterial foodborne and diarrheal disease national case surveillance, annual report, 2005. CDC, Atlanta, GA.
Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, et al. 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50: 882-889.
Gal-Mor O, Boyle EC, Grassl GA. 2014. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front. Microbiol. 5: 391.
Kim HB, Yoon M, Lee SJ, Jang YH, Choe NH. 2014. Prevalence and antibiotic resistance characteristics of Salmonella spp. isolated from food-producing animals and meat products in Korea. J. Preventive Vet. Med. 38: 85-93.
Letellier A, Messier S, Quessy S. 1999. Prevalence of Salmonella spp. and Yersinia enterocolitica in finishing swine at Canadian abattoirs. J. Food Prot. 62: 22-25.
Wood RL, Rose R. 1992. Populations of Salmonella typhimurium in internal organs of experimentally infected carrier swine. Am. J. Vet. Res. 53: 653-658.
De Busser EV, Maes D, Houf K, Dewulf J, Imberechts H, Bertrand S, De Zutter L. 2011. Detection and characterization of Salmonella in lairage, on pig carcasses and intestines in five slaughterhouses. Int. J. Food Microbiol. 145: 279-286.
Berends BR, Van Knapen F, Snijders JM, Mossel DA. 1997. Identification and quantification of risk factors regarding Salmonella spp. on pork carcasses. Int. J. Food Microbiol. 36: 199-206.
Aarestrup FM. 2005. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin. Pharmacol. Toxicol. 96: 271-281.
Zhao EY, Bao HX, Tang L, Zou QH, Liu WQ, Zhu DL, et al. 2013. Genomic comparison of Salmonella typhimurium DT104 with non-DT104 strains. Mol. Genet. Genomics 288: 549-557.
Meunier D, Boyd D, Mulvey MR, Baucheron S, Mammina C, Nastasi A, et al. 2002. Salmonella enterica serotype Typhimurium DT 104 antibiotic resistance genomic island I in serotype paratyphi B. Emerg. Infect. Dis. 8: 430-433.
Ju MS, Kang ZW, Jung JH, Cho SB, Kim SH, Lee YJ, et al. 2011. Genotyping, phage typing, and antimicrobial resistance of Salmonella Typhimurium isolated from pigs, cattle, and humans. Korean J. Food Sci. Anim. Resour. 31: 47-53.
Bruun T, Sorensen G, Forshell LP, Jensen T, Nygard K, Kapperud G, et al. 2009. An outbreak of Salmonella Typhimurium infections in Denmark, Norway and Sweden, 2008. Euro Surveill. 14: 19147.
Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, et al. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10: 563-569.
Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30: 2068-2069.
Lukashin AV, Borodovsky M. 1998. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26: 1107-1115.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35: 3100-3108.
Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. 2009. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120.
Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. 2016. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32: 929-931.
Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, et al. 2015. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31: 3691-3693.
Sullivan MJ, Petty NK, Beatson SA. 2011. Easyfig: a genome comparison visualizer. Bioinformatics 27: 1009-1010.
Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the artemis comparison tool. Bioinformatics 21: 3422-3423.
Roer L, Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, Kaas RS, Hasman H, et al. 2016. Is the evolution of Salmonella enterica subsp. enterica linked to restriction-modification systems? mSystems. 1: e00009-e00016.
Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q. 2005. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. 33: D325-D328.
Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. 2017. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 45: D566-D573.
Brumell JH, Rosenberger CM, Gotto GT, Marcus SL, Finlay BB. 2001. SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell. Microbiol. 3: 75-84.
Kim E, Lee S-H, Lee S-J, Kwon O-P, Yoon H. 2017. New antibacterial-core structures based on styryl quinolinium. Food Sci. Biotechnol. 26: 521-529.
Bowe F, Lipps CJ, Tsolis RM, Groisman E, Heffron F, Kusters JG. 1998. At least four percent of the Salmonella typhimurium genome is required for fatal infection of mice. Infect. Immun. 66: 3372-3377.
Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. 2000. Salmonella pathogenicity islands: big virulence in small packages. Microb. Infect. 2: 145-156.
Addwebi TM, Call DR, Shah DH. 2014. Contribution of Salmonella Enteritidis virulence factors to intestinal colonization and systemic dissemination in 1-day-old chickens. Poult. Sci. 93: 871-881.
Elder JR, Chiok KL, Paul NC, Haldorson G, Guard J, Shah DH. 2016. The Salmonella pathogenicity island 13 contributes to pathogenesis in streptomycin pre-treated mice but not in day-old chickens. Gut Pathog. 8: 16.
Boyer E, Bergevin I, Malo D, Gros P, Cellier MF. 2002. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 70: 6032-6042.
Tsolis RM, Baumler AJ, Heffron F. 1995. Role of Salmonella typhimurium Mn-superoxide dismutase (SodA) in protection against early killing by J774 macrophages. Infect. Immun. 63: 1739-1744.
Kehres DG, Janakiraman A, Slauch JM, Maguire ME. 2002. Regulation of Salmonella enterica serovar Typhimurium mntH transcription by H2O2, Fe2+, and Mn2+. J. Bacteriol. 184: 3151-3158.
Horsburgh MJ, Wharton SJ, Karavolos M, Foster SJ. 2002. Manganese: elemental defence for a life with oxygen. Trends Microbiol. 10: 496-501.
Althouse C, Patterson S, Fedorka-Cray P, Isaacson RE. 2003. Type 1 fimbriae of Salmonella enterica serovar Typhimurium bind to enterocytes and contribute to colonization of swine in vivo. Infect. Immun. 71: 6446-6452.
Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, et al. 2015. Secretion systems in gramnegative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13: 343-359.
Baumler AJ, Tsolis RM, Heffron F. 1996. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer’s patches. Proc. Natl. Acad. Sci. USA 93: 279-283.
Brodsky IE, Ghori N, Falkow S, Monack D. 2005. Mig-14 is an inner membrane-associated protein that promotes Salmonella typhimurium resistance to CRAMP, survival within activated macrophages and persistent infection. Mol. Microbiol. 55: 954-972.
Hapfelmeier S, Stecher B, Barthel M, Kremer M, Muller AJ, Heikenwalder M, et al. 2005. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar Typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174: 1675-1685.
Swords WE, Cannon BM, Benjamin WH Jr. 1997. Avirulence of L T2 s trains of Salmonella typhimurium results from a defective rpoS gene. Infect. Immun. 65: 2451-2453.
Wilmes-Riesenberg MR, Foster JW, Curtiss R 3rd. 1997. An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect. Immun. 65: 203-210.
De E, Basle A, Jaquinod M, Saint N, Mallea M, Molle G, et al. 2001. A new mechanism of antibiotic resistance in Enterobacteriaceae induced by a structural modification of the major porin. Mol. Microbiol. 41: 189-198.
Sievers F , Wilm A , Dineen D , Gibson T J, K arplus K , L i W, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7: 539.
Petkau A, Stuart-Edwards M, Stothard P, Van Domselaar G. 2010. Interactive microbial genome visualization with GView. Bioinformatics 26: 3125-3126.
Tanaka K, Nishimori K, Makino S, Nishimori T, Kanno T, Ishihara R, et al. 2004. Molecular characterization of a prophage of Salmonella enterica serotype Typhimurium DT104. J. Clin. Microbiol. 42: 1807-1812.
Reiter WD, Palm P, Yeats S. 1989. Transfer RNA genes frequently serve as integration sites for prokaryotic genetic elements. Nucleic Acids Res. 17: 1907-1914.
Brussow H, Canchaya C, Hardt WD. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68: 560-602.
Allison GE, Verma NK. 2000. Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol. 8: 17-23.
Kim M, Ryu S. 2012. Spontaneous and transient defence against bacteriophage by phase-variable glucosylation of O-antigen in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 86: 411-425.
Duerr CU, Zenk SF, Chassin C, Pott J, Gutle D, Hensel M, et al. 2009. O-Antigen delays lipopolysaccharide recognition and impairs antibacterial host defense in murine intestinal epithelial cells. PLoS Pathog. 5: e1000567.
Reeves P. 1995. Role of O-antigen variation in the immune response. Trends Microbiol. 3: 381-386.
Anjum MF, Choudhary S, Morrison V, Snow LC, Mafura M, Slickers P, et al. 2011. Identifying antimicrobial resistance genes of human clinical relevance within Salmonella isolated from food animals in Great Britain. J. Antimicrob. Chemother. 66: 550-559.
Patterson SK, Borewicz K, Johnson T, Xu W, Isaacson RE. 2012. Characterization and differential gene expression between two phenotypic phase variants in Salmonella enterica serovar Typhimurium. PLoS One 7: e43592.
Fortier LC, Sekulovic O. 2013. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4: 354-365.