1887

Abstract

The evolution of serovar Typhimurium (. Typhimurium) within passerines has resulted in pathoadaptation of this serovar to the avian host in Europe. Recently, we identified an . Typhimurium lineage from passerines in North America. The emergence of passerine-adapted . Typhimurium in Europe and North America raises questions regarding its evolutionary origin. Here, we demonstrated that the UK and US passerine-adapted . Typhimurium shared a common ancestor from . 1838, and larids played a key role in the clonal expansion by disseminating the common ancestor between North America and Europe. Further, we identified virulence gene signatures common in the passerine- and larid-adapted . Typhimurium, including conserved pseudogenes in fimbrial gene and Type 3 Secretion System (T3SS) effector gene . However, the UK and US passerine-adapted . Typhimurium also possessed unique virulence gene signatures (i.e. pseudogenes in fimbrial gene and T3SS effector genes , , and ), and the majority of them (38/47) lost a virulence plasmid pSLT that was present in the larid-adapted . Typhimurium. These results provide evidence that passerine-adapted . Typhimurium share a common ancestor with those from larids, and the divergence of passerine- and larid-adapted . Typhimurium might be due to pseudogenization or loss of specific virulence genes.

Funding
This study was supported by the:
  • U.S. Department of Agriculture (Award PEN4522)
    • Principle Award Recipient: EdwardG. Dudley
  • U.S. Food and Drug Administration (Award 1 U19 FD007114-01)
    • Principle Award Recipient: EdwardG. Dudley
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000775
2022-02-23
2022-07-06
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/2/mgen000775.html?itemId=/content/journal/mgen/10.1099/mgen.0.000775&mimeType=html&fmt=ahah

References

  1. Rabsch W, Andrews HL, Kingsley RA, Prager R, Tschäpe H et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun 2002; 70:2249–2255 [View Article] [PubMed]
    [Google Scholar]
  2. Pasmans F, Van Immerseel F, Heyndrickx M, Martel A, Godard C et al. Host adaptation of pigeon isolates of Salmonella enterica subsp. enterica serovar Typhimurium variant Copenhagen phage type 99 is associated with enhanced macrophage cytotoxicity. Infect Immun 2003; 71:6068–6074 [View Article] [PubMed]
    [Google Scholar]
  3. Okoro CK, Barquist L, Connor TR, Harris SR, Clare S et al. Signatures of adaptation in human invasive Salmonella Typhimurium ST313 populations from sub-Saharan Africa. PLoS Negl Trop Dis 2015; 9:e0003611 [View Article] [PubMed]
    [Google Scholar]
  4. Van Puyvelde S, Pickard D, Vandelannoote K, Heinz E, Barbé B et al. An African Salmonella Typhimurium ST313 sublineage with extensive drug-resistance and signatures of host adaptation. Nat Commun 2019; 10:1–12 [View Article] [PubMed]
    [Google Scholar]
  5. Pulford CV, Perez-Sepulveda BM, Canals R, Bevington JA, Bengtsson RJ et al. Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa. Nat Microbiol 2021; 6:327–338 [View Article] [PubMed]
    [Google Scholar]
  6. Hughes LA, Shopland S, Wigley P, Bradon H, Leatherbarrow AH et al. Characterisation of Salmonella enterica serotype Typhimurium isolates from wild birds in northern England from 2005 - 2006. BMC Vet Res 2008; 4:1–10 [View Article] [PubMed]
    [Google Scholar]
  7. Lawson B, de Pinna E, Horton RA, Macgregor SK, John SK et al. Epidemiological evidence that garden birds are a source of human salmonellosis in England and Wales. PLoS One 2014; 9:e88968 [View Article] [PubMed]
    [Google Scholar]
  8. Söderlund R, Jernberg C, Trönnberg L, Pääjärvi A, Ågren E et al. Linked seasonal outbreaks of Salmonella Typhimurium among passerine birds, domestic cats and humans, Sweden, 2009 to 2016. Euro Surveill 2019; 24:1900074 [View Article] [PubMed]
    [Google Scholar]
  9. Refsum T, Vikøren T, Handeland K, Kapperud G, Holstad G. Epidemiologic and pathologic aspects of Salmonella typhimurium infection in passerine birds in Norway. J Wildl Dis 2003; 39:64–72 [View Article] [PubMed]
    [Google Scholar]
  10. Mather AE, Lawson B, de Pinna E, Wigley P, Parkhill J et al. Genomic Analysis of Salmonella enterica Serovar Typhimurium from Wild Passerines in England and Wales. Appl Environ Microbiol 2016; 82:6728–6735 [View Article] [PubMed]
    [Google Scholar]
  11. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 2001; 413:852–856 [View Article] [PubMed]
    [Google Scholar]
  12. Bawn M, Alikhan N-F, Thilliez G, Kirkwood M, Wheeler NE et al. Evolution of Salmonella enterica serotype Typhimurium driven by anthropogenic selection and niche adaptation. PLoS Genet 2020; 16:e1008850 [View Article] [PubMed]
    [Google Scholar]
  13. Hoiseth SK, Stocker BAD. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981; 291:238–239 [View Article] [PubMed]
    [Google Scholar]
  14. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE et al. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 2009; 19:2279–2287 [View Article] [PubMed]
    [Google Scholar]
  15. Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 2012; 44:1215–1221 [View Article] [PubMed]
    [Google Scholar]
  16. Mather AE, Reid SWJ, Maskell DJ, Parkhill J, Fookes MC et al. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science 2013; 341:1514–1517 [View Article] [PubMed]
    [Google Scholar]
  17. Petrovska L, Mather AE, AbuOun M, Branchu P, Harris SR et al. Microevolution of Monophasic Salmonella Typhimurium during Epidemic, United Kingdom, 2005-2010. Emerg Infect Dis 2016; 22:617–624 [View Article] [PubMed]
    [Google Scholar]
  18. Kirkwood M, Vohra P, Bawn M, Thilliez G, Pye H et al. Ecological niche adaptation of Salmonella Typhimurium U288 is associated with altered pathogenicity and reduced zoonotic potential. Commun Biol 2021; 4:498 [View Article] [PubMed]
    [Google Scholar]
  19. Tassinari E, Bawn M, Thilliez G, Charity O, Acton L et al. Whole-genome epidemiology links phage-mediated acquisition of a virulence gene to the clonal expansion of a pandemic Salmonella enterica serovar Typhimurium clone. Microb Genom 2020; 6:mgen000456 [View Article] [PubMed]
    [Google Scholar]
  20. Stevens MP, Kingsley RA. Salmonella pathogenesis and host-adaptation in farmed animals. Curr Opin Microbiol 2021; 63:52–58 [View Article] [PubMed]
    [Google Scholar]
  21. 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] [PubMed]
    [Google Scholar]
  22. Shariat N, Dudley EG. CRISPRs: molecular signatures used for pathogen subtyping. Appl Environ Microbiol 2014; 80:430–439 [View Article] [PubMed]
    [Google Scholar]
  23. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 1998; 95:3140–3145 [View Article] [PubMed]
    [Google Scholar]
  24. Barrangou R, Dudley EG. CRISPR-based typing and next-generation tracking technologies. Annu Rev Food Sci Technol 2016; 7:395–411 [View Article] [PubMed]
    [Google Scholar]
  25. Salipante SJ, Hall BG. Determining the limits of the evolutionary potential of an antibiotic resistance gene. Mol Biol Evol 2003; 20:653–659 [View Article] [PubMed]
    [Google Scholar]
  26. Fu Y, M’ikanatha NM, Whitehouse CA, Tate H, Ottesen A et al. Low occurrence of multi-antimicrobial and heavy metal resistance in Salmonella enterica from wild birds in the United States. Environ Microbiol 2021 [View Article] [PubMed]
    [Google Scholar]
  27. Hiley L, Graham RMA, Jennison AV. Genetic characterisation of variants of the virulence plasmid, pSLT, in Salmonella enterica serovar Typhimurium provides evidence of a variety of evolutionary directions consistent with vertical rather than horizontal transmission. PLoS One 2019; 14:e0215207 [View Article] [PubMed]
    [Google Scholar]
  28. Bäumler AJ, Tsolis RM, Heffron F. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer’s patches. Proc Natl Acad Sci U S A 1996; 93:279–283 [View Article] [PubMed]
    [Google Scholar]
  29. Althouse C, Patterson S, Fedorka-Cray P, Isaacson RE. Type 1 fimbriae of Salmonella enterica serovar Typhimurium bind to enterocytes and contribute to colonization of swine in vivo. Infect Immun 2003; 71:6446–6452 [View Article] [PubMed]
    [Google Scholar]
  30. Bhavsar AP, Brown NF, Stoepel J, Wiermer M, Martin DDO et al. The Salmonella type III effector SspH2 specifically exploits the NLR co-chaperone activity of SGT1 to subvert immunity. PLoS Pathog 2013; 9:e1003518 [View Article] [PubMed]
    [Google Scholar]
  31. Fàbrega A, Vila J. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 2013; 26:308–341 [View Article] [PubMed]
    [Google Scholar]
  32. Kuźmińska-Bajor M, Grzymajło K, Ugorski M. Type 1 fimbriae are important factors limiting the dissemination and colonization of mice by Salmonella Enteritidis and contribute to the induction of intestinal inflammation during Salmonella invasion. Front Microbiol 2015; 6:276 [View Article] [PubMed]
    [Google Scholar]
  33. Dos Santos AMP, Ferrari RG, Conte-Junior CA. Virulence factors in Salmonella Typhimurium: the sagacity of a bacterium. Curr Microbiol 2019; 76:762–773 [View Article] [PubMed]
    [Google Scholar]
  34. Cohen E, Azriel S, Auster O, Gal A, Zitronblat C et al. Pathoadaptation of the passerine-associated Salmonella enterica serovar Typhimurium lineage to the avian host. PLoS Pathog 2021; 17:e1009451 [View Article] [PubMed]
    [Google Scholar]
  35. Kingsley RA, Kay S, Connor T, Barquist L, Sait L et al. Genome and transcriptome adaptation accompanying emergence of the definitive type 2 host-restricted Salmonella enterica serovar Typhimurium pathovar. mBio 2013; 4:e00565–13 [View Article] [PubMed]
    [Google Scholar]
  36. Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 2019; 15:e1006650 [View Article] [PubMed]
    [Google Scholar]
  37. Gross AO. The migration of kent island herring gulls. Bird-Banding 1940; 11:129 [View Article]
    [Google Scholar]
  38. Lonergan P, Mullarney K. Identification of American Herring Gull in a western European context. Dutch Bird 2004; 26:1–35
    [Google Scholar]
  39. Langridge GC, Fookes M, Connor TR, Feltwell T, Feasey N et al. Patterns of genome evolution that have accompanied host adaptation in Salmonella. Proc Natl Acad Sci U S A 2015; 112:863–868 [View Article] [PubMed]
    [Google Scholar]
  40. Yue M, Han X, De Masi L, Zhu C, Ma X et al. Allelic variation contributes to bacterial host specificity. Nat Commun 2015; 6:1–11 [View Article] [PubMed]
    [Google Scholar]
  41. Tanner JR, Kingsley RA. Evolution of Salmonella within Hosts. Trends Microbiol 2018; 26:986–998 [View Article] [PubMed]
    [Google Scholar]
  42. Sabbagh SC, Forest CG, Lepage C, Leclerc JM, Daigle F. So similar, yet so different: uncovering distinctive features in the genomes of Salmonella enterica serovars Typhimurium and Typhi. FEMS Microbiol Lett 2010; 305:1–13 [View Article] [PubMed]
    [Google Scholar]
  43. Fu Y, M’ikanatha NM, Lorch JM, Blehert DS, Berlowski-Zier B et al. Salmonella enterica serovar typhimurium from wild birds in the United States represent distinct lineages defined by bird type. bioRxiv 2021 2021 [View Article]
    [Google Scholar]
  44. Timme RE, Wolfgang WJ, Balkey M, Venkata SLG, Randolph R et al. Optimizing open data to support one health: best practices to ensure interoperability of genomic data from bacterial pathogens. One Health Outlook 2020; 2:20 [View Article] [PubMed]
    [Google Scholar]
  45. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  46. Zhou Z, Alikhan NF, Mohamed K, Fan Y, Achtman M et al. 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]
  47. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2016; 2:vew007 [View Article] [PubMed]
    [Google Scholar]
  48. Duchêne S, Duchêne D, Holmes EC, Ho SYW. The performance of the date-randomization test in phylogenetic analyses of time-structured virus data. Mol Biol Evol 2015; 32:1895–1906 [View Article] [PubMed]
    [Google Scholar]
  49. de Bernardi Schneider A, Ford CT, Hostager R, Williams J, Cioce M et al. StrainHub: a phylogenetic tool to construct pathogen transmission networks. Bioinformatics 2020; 36:945–947 [View Article] [PubMed]
    [Google Scholar]
  50. 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]
  51. Shariat N, Sandt CH, DiMarzio MJ, Barrangou R, Dudley EG. CRISPR-MVLST subtyping of Salmonella enterica subsp. entericaserovars Typhimurium and Heidelberg and application in identifying outbreak isolates. BMC Microbiol 2013; 13:1–17 [View Article] [PubMed]
    [Google Scholar]
  52. Seemann T. Shovill: Faster SPAdes assembly of Illumina reads; 2017 https://github.com/tseemann/shovill
  53. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
    [Google Scholar]
  54. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
    [Google Scholar]
  55. Liu B, Zheng DD, Jin Q, Chen LH, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2019; 47:D687–D692 [View Article] [PubMed]
    [Google Scholar]
  56. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000775
Loading
/content/journal/mgen/10.1099/mgen.0.000775
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error