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Abstract

Non-typhoidal are extremely diverse and different serovars can exhibit varied phenotypes, including host adaptation and the ability to cause clinical illness in animals and humans. In the USA, serovar Kentucky is infrequently found to cause human illness, despite being the top serovar isolated from broiler chickens. Conversely, in Europe, this serovar falls in the top 10 serovars linked to human salmonellosis. Serovar Kentucky is polyphyletic and has two lineages, Kentucky-I and Kentucky-II; isolates belonging to Kentucky-I are frequently isolated from poultry in the USA, while Kentucky-II isolates tend to be associated with human illness. In this study, we analysed whole-genome sequences and associated metadata deposited in public databases between 2017 and 2021 by federal agencies to determine serovar Kentucky incidence across different animal and human sources. Of 5151 genomes, 90.3 % were from isolates that came from broilers, while 5.9 % were from humans and 3.0 % were from cattle. Kentucky-I isolates were associated with broilers, while isolates belonging to Kentucky-II and a new lineage, Kentucky-III, were more commonly associated with cattle and humans. Very few serovar Kentucky isolates were associated with turkey and swine sources. Phylogenetic analyses showed that Kentucky-III genomes were more closely related to Kentucky-I, and this was confirmed by CRISPR-typing and multilocus sequence typing (MLST). In a macrophage assay, serovar Kentucky-II isolates were able to replicate over eight times better than Kentucky-I isolates. Analysis of virulence factors showed unique patterns across these three groups, and these differences may be linked to their association with different hosts.

Keyword(s): polyphyly , Salmonella Kentucky and WGS
Funding
This study was supported by the:
  • National Institute of Food and Agriculture (Award 2020-67017-30792)
    • Principle Award Recipient: NikkiW. Shariat
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-09-26
2024-05-21
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References

  1. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010; 50:882–889 [View Article] [PubMed]
    [Google Scholar]
  2. Tack DM, Ray L, Griffin PM, Cieslak PR, Dunn J et al. Preliminary incidence and trends of infections with pathogens transmitted commonly through food – foodborne diseases active surveillance network, 10 U.S. sites, 2016–2019. Morb Mortal Wkly Rep 2020; 69:509–514 [View Article] [PubMed]
    [Google Scholar]
  3. Grimont PAD, Weill FX. Antigenic Formulae of the Salmonella Serovars, 9th edn Paris: WHO Collaborating Centre for Reference and Research on Salmonella; 2007
    [Google Scholar]
  4. CDC National Enteric Disease Surveillance: Salmonella Annual Summary Atlanta, GA: Centers for Disease Control and Prevention; 2016
    [Google Scholar]
  5. Yoshida CE, Kruczkiewicz P, Laing CR, Lingohr EJ, Gannon VPJ et al. The Salmonella in silico typing resource (SISTR): an open web-accessible tool for rapidly typing and subtyping draft Salmonella genome assemblies. PLoS One 2016; 11:e0147101 [View Article] [PubMed]
    [Google Scholar]
  6. Zhang S, den Bakker HC, Li S, Chen J, Dinsmore BA et al. SeqSero2: rapid and improved Salmonella serotype determination using whole-genome sequencing data. Appl Environ Microbiol 2019; 85:e01746-19 [View Article] [PubMed]
    [Google Scholar]
  7. Tanner JR, Kingsley RA. Evolution of Salmonella within hosts. Trends Microbiol 2018; 26:986–998 [View Article] [PubMed]
    [Google Scholar]
  8. Cheng RA, Wiedmann M. Recent advances in our understanding of the diversity and roles of chaperone-usher fimbriae in facilitating Salmonella host and tissue tropism. Front Cell Infect Microbiol 2021; 10:628043 [View Article] [PubMed]
    [Google Scholar]
  9. Silva CA, Blondel CJ, Quezada CP, Porwollik S, Andrews-Polymenis HL et al. Infection of mice by Salmonella enterica serovar Enteritidis involves additional genes that are absent in the genome of serovar Typhimurium. Infect Immun 2012; 80:839–849 [View Article] [PubMed]
    [Google Scholar]
  10. Cheng RA, Eade CR, Wiedmann M. Embracing diversity: differences in virulence mechanisms, disease severity, and host adaptations contribute to the success of nontyphoidal Salmonella as a foodborne pathogen. Front Microbiol 2019; 10:1368 [View Article] [PubMed]
    [Google Scholar]
  11. Worley J, Meng J, Allard MW, Brown EW, Timme RE. Salmonella enterica phylogeny based on whole-genome sequencing reveals two new clades and novel patterns of horizontally acquired genetic elements. mBio 2018; 9:e02303-18 [View Article] [PubMed]
    [Google Scholar]
  12. Sangal V, Harbottle H, Mazzoni CJ, Helmuth R, Guerra B et al. Evolution and population structure of Salmonella enterica serovar Newport. J Bacteriol 2010; 192:6465–6476 [View Article] [PubMed]
    [Google Scholar]
  13. Cao G, Meng J, Strain E, Stones R, Pettengill J et al. Phylogenetics and differentiation of Salmonella Newport lineages by whole genome sequencing. PLoS One 2013; 8:e55687 [View Article] [PubMed]
    [Google Scholar]
  14. de Moraes MH, Soto EB, Salas González I, Desai P, Chu W et al. Genome-wide comparative functional analyses reveal adaptations of Salmonella sv. Newport to a plant colonization lifestyle. Front Microbiol 2018; 9:877 [View Article] [PubMed]
    [Google Scholar]
  15. Zheng J, Luo Y, Reed E, Bell R, Brown EW et al. Whole-genome comparative analysis of Salmonella enterica serovar Newport strains reveals lineage-specific divergence. Genome Biol Evol 2017; 9:1047–1050 [View Article] [PubMed]
    [Google Scholar]
  16. Nguyen SV, Harhay DM, Bono JL, Smith TPL, Fields PI et al. Comparative genomics of Salmonella enterica serovar Montevideo reveals lineage-specific gene differences that may influence ecological niche association. Microb Genom 2018; 4:e000202 [View Article] [PubMed]
    [Google Scholar]
  17. Zou W, Lin WJ, Foley SL, Chen CH, Nayak R et al. Evaluation of pulsed-field gel electrophoresis profiles for identification of Salmonella serotypes. J Clin Microbiol 2010; 48:3122–3126 [View Article] [PubMed]
    [Google Scholar]
  18. Timme RE, Pettengill JB, Allard MW, Strain E, Barrangou R et al. Phylogenetic diversity of the enteric pathogen Salmonella enterica subsp. enterica inferred from genome-wide reference-free SNP characters. Genome Biol Evol 2013; 5:2109–2123 [View Article] [PubMed]
    [Google Scholar]
  19. Achtman M, Wain J, Weill F-X, Nair S, Zhou Z et al. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog 2012; 8:e1002776 [View Article]
    [Google Scholar]
  20. Shariat N, Kirchner MK, Sandt CH, Trees E, Barrangou R et al. Subtyping of Salmonella enterica serovar Newport outbreak isolates by CRISPR-MVLST and determination of the relationship between CRISPR-MVLST and PFGE results. J Clin Microbiol 2013; 51:2328–2336 [View Article] [PubMed]
    [Google Scholar]
  21. Yin Z, Liu J, Du B, Ruan H-H, Huo Y-X et al. Whole-genome-based survey for polyphyletic serovars of Salmonella enterica subsp. enterica provides new insights into public health surveillance. Int J Mol Sci 2020; 21:5226 [View Article] [PubMed]
    [Google Scholar]
  22. Xi M, Zheng J, Zhao S, Brown EW, Meng J. An enhanced discriminatory pulsed-field gel electrophoresis scheme for subtyping Salmonella serotypes Heidelberg, Kentucky, SaintPaul, and Hadar. J Food Prot 2008; 71:2067–2072 [View Article] [PubMed]
    [Google Scholar]
  23. Vosik D, Tewari D, Dettinger L, M’ikanatha NM, Shariat NW. CRISPR typing and antibiotic resistance correlates with polyphyletic distribution in human isolates of Salmonella Kentucky. Foodborne Pathog Dis 2018; 15:101–108 [View Article] [PubMed]
    [Google Scholar]
  24. Haley BJ, Kim SW, Pettengill J, Luo Y, Karns JS et al. Genomic and evolutionary analysis of two Salmonella enterica serovar Kentucky sequence types isolated from bovine and poultry sources in North America. PLoS One 2016; 11:e0161225 [View Article] [PubMed]
    [Google Scholar]
  25. Le Hello S, Bekhit A, Granier SA, Barua H, Beutlich J et al. The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Front Microbiol 2013; 4:395 [View Article] [PubMed]
    [Google Scholar]
  26. Sukhnanand S, Alcaine S, Warnick LD, Su W-L, Hof J et al. DNA sequence-based subtyping and evolutionary analysis of selected Salmonella enterica serotypes. J Clin Microbiol 2005; 43:3688–3698 [View Article] [PubMed]
    [Google Scholar]
  27. Rauch HE, Vosik D, Kariyawasam S, M’ikanatha N, Shariat NW. Prevalence of group I Salmonella Kentucky in domestic food animals from Pennsylvania and overlap with human clinical CRISPR sequence types. Zoonoses Public Health 2018; 65:831–837 [View Article] [PubMed]
    [Google Scholar]
  28. Siceloff AT, Waltman D, Shariat NW. Regional Salmonella differences in United States broiler production from 2016 to 2020 and the contribution of multiserovar populations to Salmonella surveillance. Appl Environ Microbiol 2022; 88:e0020422 [View Article] [PubMed]
    [Google Scholar]
  29. USDA-FSIS Serotypes Profile of Salmonella Isolates from Meat and Poultry Products January 1998 through December 2014 Washington, DC: United States Department of Agriculture–Food Safety and Inspection Service; 2014
    [Google Scholar]
  30. Interagency Food Safety Analytics Collaboration (IFSAC) Foodborne Illness Source Attribution Estimates for 2019 for Salmonella, Escherichia coli O157, Listeria monocytogenes, and Campylobacter Using Multi-Year Outbreak Surveillance Data Atlanta, GA, Washington, DC: CDC, FDA, USDA-FSIS; 2021
    [Google Scholar]
  31. Soltys RC, Sakomoto CK, Oltean HN, Guard J, Haley BJ et al. High-resolution comparative genomics of Salmonella Kentucky aids source tracing and detection of ST198 and ST152 lineage-specific mutations. Front Sustain Food Syst 2021; 5:6953368 [View Article]
    [Google Scholar]
  32. Xiong Z, Wang S, Huang Y, Gao Y, Shen H et al. Ciprofloxacin-resistant Salmonella enterica serovar Kentucky ST198 in broiler chicken supply chain and patients, China, 2010–2016. Microorganisms 2020; 8:140 [View Article] [PubMed]
    [Google Scholar]
  33. Hawkey J, Le Hello S, Doublet B, Granier SA, Hendriksen RS et al. Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198. Microb Genom 2019; 5:e000269 [View Article] [PubMed]
    [Google Scholar]
  34. Le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D et al. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis 2013; 13:672–679 [View Article] [PubMed]
    [Google Scholar]
  35. European Food Safety Authority The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J 2018; 16:e05500 [View Article] [PubMed]
    [Google Scholar]
  36. Seiffert SN, Perreten V, Johannes S, Droz S, Bodmer T et al. OXA-48 carbapenemase-producing Salmonella enterica serovar Kentucky isolate of sequence type 198 in a patient transferred from Libya to Switzerland. Antimicrob Agents Chemother 2014; 58:2446–2449 [View Article] [PubMed]
    [Google Scholar]
  37. Haley BJ, Kim SW, Haendiges J, Keller E, Torpey D et al. Salmonella enterica serovar Kentucky recovered from human clinical cases in Maryland, USA (2011–2015). Zoonoses Public Health 2019; 66:382–392 [View Article] [PubMed]
    [Google Scholar]
  38. Tang S, Orsi RH, Luo H, Ge C, Zhang G et al. Assessment and comparison of molecular subtyping and characterization methods for Salmonella. Front Microbiol 2019; 10:1591 [View Article] [PubMed]
    [Google Scholar]
  39. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  40. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article] [PubMed]
    [Google Scholar]
  41. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  42. Gardner SN, Hall BG, Tang H. When whole-genome alignments just won’t work: kSNP v2 software for alignment-free SNP discovery and phylogenetics of hundreds of microbial genomes. PLoS One 2013; 8:e81760 [View Article] [PubMed]
    [Google Scholar]
  43. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
    [Google Scholar]
  44. Letunic I, Bork P. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  45. Chernomor O, Minh BQ, Forest F, Klaere S, Ingram T et al. Split diversity in constrained conservation prioritization using integer linear programming. Methods Ecol Evol 2015; 6:83–91 [View Article] [PubMed]
    [Google Scholar]
  46. Alikhan N-F, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet 2018; 14:e1007261 [View Article] [PubMed]
    [Google Scholar]
  47. Zhou Z, Alikhan NF, Mohamed K, Fan Y, Achtman M. The EnteroBase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res 2020; 30:138–152 [View Article]
    [Google Scholar]
  48. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  49. Nethery MA, Barrangou R. CRISPR Visualizer: rapid identification and visualization of CRISPR loci via an automated high-throughput processing pipeline. RNA Biol 2019; 16:577–584 [View Article] [PubMed]
    [Google Scholar]
  50. Horvath P, Romero DA, Coûté-Monvoisin A-C, Richards M, Deveau H et al. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 2008; 190:1401–1412 [View Article] [PubMed]
    [Google Scholar]
  51. Richards AK, Hopkins BA, Shariat NW. Conserved CRISPR arrays in Salmonella enterica serovar Infantis can serve as qPCR targets to detect Infantis in mixed serovar populations. Lett Appl Microbiol 2020; 71:138–145 [View Article] [PubMed]
    [Google Scholar]
  52. Chen L, Yang J, Yu J, Yao Z, Sun L et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 2005; 33:D325–D328 [View Article] [PubMed]
    [Google Scholar]
  53. Wu J, Pugh R, Laughlin RC, Andrews-Polymenis H, McClelland M et al. High-throughput assay to phenotype Salmonella enterica Typhimurium association, invasion, and replication in macrophages. J Vis Exp 2014e51759 [View Article] [PubMed]
    [Google Scholar]
  54. Shariat NW, Timme RE, Walters AT. Phylogeny of Salmonella enterica subspecies arizonae by whole-genome sequencing reveals high incidence of polyphyly and low phase 1 H antigen variability. Microb Genom 2021; 7:000522 [View Article] [PubMed]
    [Google Scholar]
  55. Cherchame E, Ilango G, Noël V, Cadel-Six S. Polyphyly in widespread Salmonella enterica serovars and using genomic proximity to choose the best reference genome for bioinformatics analyses. Front Public Health 2022; 10:963188 [View Article] [PubMed]
    [Google Scholar]
  56. Shariat N, Timme RE, Pettengill JB, Barrangou R, Dudley EG. Characterization and evolution of Salmonella CRISPR-Cas systems. Microbiology 2015; 161:374–386 [View Article] [PubMed]
    [Google Scholar]
  57. Kushwaha SK, Bhavesh NLS, Abdella B, Lahiri C, Marathe SA. The phylogenomics of CRISPR-Cas system and revelation of its features in Salmonella. Sci Rep 2020; 10:21156 [View Article] [PubMed]
    [Google Scholar]
  58. Harbottle H, White DG, McDermott PF, Walker RD, Zhao S. Comparison of multilocus sequence typing, pulsed-field gel electrophoresis, and antimicrobial susceptibility typing for characterization of Salmonella enterica serotype Newport isolates. J Clin Microbiol 2006; 44:2449–2457 [View Article] [PubMed]
    [Google Scholar]
  59. Tate H, Hsu C-H, Chen JC, Han J, Foley SL et al. Genomic diversity, antimicrobial resistance, and virulence gene profiles of Salmonella serovar Kentucky isolated from humans, food, and animal ceca content sources in the United States. Foodborne Pathog Dis 2022; 19:509–521 [View Article] [PubMed]
    [Google Scholar]
  60. EFSA BIOHAZ Panel Salmonella control in poultry flocks and its public health impact. EFSA J 2019; 17:e05596 [View Article]
    [Google Scholar]
  61. Samper-Cativiela C, Diéguez-Roda B, Trigo da Roza F, Ugarte-Ruiz M, Elnekave E et al. Genomic characterization of multidrug-resistant Salmonella serovar Kentucky ST198 isolated in poultry flocks in Spain (2011–2017). Microb Genom 2022; 8:000773 [View Article] [PubMed]
    [Google Scholar]
  62. Le Hello S, Hendriksen RS, Doublet B, Fisher I, Nielsen EM et al. International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. J Infect Dis 2011; 204:675–684 [View Article] [PubMed]
    [Google Scholar]
  63. de Mesquita Sousa Saraiva M, Benevides VP, da Silva NMV, de Mello Varani A, de Freitas Neto OC et al. Genomic and evolutionary analysis of Salmonella enterica serovar Kentucky sequence type 198 isolated from livestock In East Africa. Front Cell Infect Microbiol 2022; 12:772829 [View Article] [PubMed]
    [Google Scholar]
  64. NCBI Pathogen Detection NCBI Methods. n.d https://ftp.ncbi.nlm.nih.gov/pathogen/Methods.txt
  65. Tay MYF, Pathirage S, Chandrasekaran L, Wickramasuriya U, Sadeepanie N et al. Whole-genome sequencing analysis of nontyphoidal Salmonella enterica of chicken meat and human origin under surveillance in Sri Lanka. Foodborne Pathog Dis 2019; 16:531–537 [View Article] [PubMed]
    [Google Scholar]
  66. Wang S, Liao X, Xiong Z, Lin Q, Wen J et al. Characterization of the emerging multidrug-resistant Salmonella enterica serotype Kentucky ST314 in China. Zoonoses Public Health 2021; 68:622–629 [View Article] [PubMed]
    [Google Scholar]
  67. Slowey R, Kim SW, Prendergast D, Madigan G, Van Kessel JAS et al. Genomic diversity and resistome profiles of Salmonella enterica subsp. enterica serovar Kentucky isolated from food and animal sources in Ireland. Zoonoses Public Health 2022; 69:1–12 [View Article] [PubMed]
    [Google Scholar]
  68. De Masi L, Yue M, Hu C, Rakov AV, Rankin SC et al. Cooperation of adhesin alleles in Salmonella-host tropism. mSphere 2017; 2:e00066-17 [View Article] [PubMed]
    [Google Scholar]
  69. Bäumler AJ, Tsolis RM, Heffron F. Contribution of fimbrial operons to attachment to and invasion of epithelial cell lines by Salmonella typhimurium. Infect Immun 1996; 64:1862–1865 [View Article] [PubMed]
    [Google Scholar]
  70. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM et al. The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect Immun 2005; 73:3358–3366 [View Article] [PubMed]
    [Google Scholar]
  71. Yue M, Han X, De Masi L, Zhu C, Ma X et al. Allelic variation contributes to bacterial host specificity. Nat Commun 2015; 6:8754 [View Article] [PubMed]
    [Google Scholar]
  72. Azriel S, Goren A, Shomer I, Aviv G, Rahav G et al. The typhi colonization factor (Tcf) is encoded by multiple non-typhoidal Salmonella serovars but exhibits a varying expression profile and interchanging contribution to intestinal colonization. Virulence 2017; 8:1791–1807 [View Article] [PubMed]
    [Google Scholar]
  73. Foley SL, Johnson TJ, Ricke SC, Nayak R, Danzeisen J. Salmonella pathogenicity and host adaptation in chicken-associated serovars. Microbiol Mol Biol Rev 2013; 77:582–607 [View Article] [PubMed]
    [Google Scholar]
  74. Figueira R, Holden DW. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology 2012; 158:1147–1161 [View Article] [PubMed]
    [Google Scholar]
  75. Kujat Choy SL, Boyle EC, Gal-Mor O, Goode DL, Valdez Y et al. SseK1 and SseK2 are novel translocated proteins of Salmonella enterica serovar Typhimurium. Infect Immun 2004; 72:5115–5125 [View Article] [PubMed]
    [Google Scholar]
  76. Zhang X, He L, Zhang C, Yu C, Yang Y et al. The impact of sseK2 deletion on Salmonella enterica serovar Typhimurium virulence in vivo and in vitro. BMC Microbiol 2019; 19:182 [View Article] [PubMed]
    [Google Scholar]
  77. Jiang X, Rossanese OW, Brown NF, Kujat-Choy S, Galán JE et al. The related effector proteins SopD and SopD2 from Salmonella enterica serovar Typhimurium contribute to virulence during systemic infection of mice. Mol Microbiol 2004; 54:1186–1198 [View Article] [PubMed]
    [Google Scholar]
  78. Tasmin R, Hasan NA, Grim CJ, Grant A, Choi SY et al. Genotypic and phenotypic characterization of multidrug resistant Salmonella Typhimurium and Salmonella Kentucky strains recovered from chicken carcasses. PLoS One 2017; 12:e0176938 [View Article] [PubMed]
    [Google Scholar]
  79. Cheng Y, Pedroso AA, Porwollik S, McClelland M, Lee MD et al. rpoS-regulated core genes involved in the competitive fitness of Salmonella enterica serovar Kentucky in the intestines of chickens. Appl Environ Microbiol 2015; 81:502–514 [View Article] [PubMed]
    [Google Scholar]
  80. Beutlich J, Jahn S, Malorny B, Hauser E, Hühn S et al. Antimicrobial resistance and virulence determinants in European Salmonella genomic island 1-positive Salmonella enterica isolates from different origins. Appl Environ Microbiol 2011; 77:5655–5664 [View Article] [PubMed]
    [Google Scholar]
  81. Sly LM, Guiney DG, Reiner NE. Salmonella enterica serovar Typhimurium periplasmic superoxide dismutases SodCI and SodCII are required for protection against the phagocyte oxidative burst. Infect Immun 2002; 70:5312–5315 [View Article] [PubMed]
    [Google Scholar]
  82. Vonaesch P, Sellin ME, Cardini S, Singh V, Barthel M et al. The Salmonella Typhimurium effector protein SopE transiently localizes to the early SCV and contributes to intracellular replication. Cell Microbiol 2014; 16:1723–1735 [View Article] [PubMed]
    [Google Scholar]
  83. Brink T, Leiss V, Siegert P, Jehle D, Ebner JK et al. Salmonella Typhimurium effector SseI inhibits chemotaxis and increases host cell survival by deamidation of heterotrimeric Gi proteins. PLoS Pathog 2018; 14:e1007248 [View Article] [PubMed]
    [Google Scholar]
  84. Ray LC, Collins JP, Griffin PM, Shah HJ, Boyle MM et al. Decreased incidence of infections caused by pathogens transmitted commonly through food during the COVID-19 pandemic – foodborne diseases active surveillance network, 10 U.S. sites, 2017–2020. MMWR Morb Mortal Wkly Rep 2021; 70:1332–1336 [View Article] [PubMed]
    [Google Scholar]
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