1887

Microbial Genomics logo

Volume 7, Issue 2

Phylogeny of subspecies by whole-genome sequencing reveals high incidence of polyphyly and low phase 1 H antigen variability Open Access

Abstract

subspecies is frequently associated with animal reservoirs, particularly reptiles, and can cause illness in some mammals, including humans. Using whole-genome sequencing data, core genome phylogenetic analyses were performed using 112 . subsp. isolates, representing 46 of 102 described serovars. Nearly one-third of these are polyphyletic, including two serovars that appear in four and five distinct evolutionary lineages. Subspecies has a monophasic H antigen. Among the 46 serovars investigated, only 8 phase 1 H antigens were identified, demonstrating high conservation for this antigen. Prophages and plasmids were found throughout this subspecies including five novel prophages. Polyphyly was also reflected in prophage content, although some clade-specific enrichment for some phages was observed. IncFII(S) was the most frequent plasmid replicon identified and was found in a quarter of subsp. genomes. pathogenicity islands (SPIs) 1 and 2 are present across all , including this subspecies, although effectors , and in SPI-1 and and in SPI-2 appear to be lost in this lineage. SPI-20, encoding a type VI secretion system, is exclusive to this subspecies and is well maintained in all genomes sampled. A number of fimbral operons were identified, including the operon that appears to be a synapomorphy for this subspecies, while others exhibited more clade-specific patterns. This work reveals evolutionary patterns in subsp. that make this subspecies a unique lineage within this very diverse species.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): H antigen , polyphyly , Salmonella , subspecies arizonae and whole-genome sequencing
© Microbiology Society
  • 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.0.000522
2021-02-04
2024-05-06
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/2/mgen000522.html?itemId=/content/journal/mgen/10.1099/mgen.0.000522&mimeType=html&fmt=ahah

References

  1. Grimont P, Weill F. Antigenic formulae of the Salmonella serovars. WHO Collab Cent Ref Res Salmonella, 9th ed. 2007
     [Google Scholar]
  2. Ewing W, Edwards P. Edwards and Ewing’s Identification of Enterobacteriaceae , 4th ed. New York: Elsevier; 1986
     [Google Scholar]
  3. Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, de Pinna E et al. Supplement 2008-2010 (NO. 48) to the White-Kauffmann-Le minor scheme. Res Microbiol 2014; 165:526–530 [View Article][PubMed]
     [Google Scholar]
  4. Lamas A, Miranda JM, Regal P, Vázquez B, Franco CM et al. A comprehensive review of non-enterica subspecies of Salmonella enterica . Microbiol Res 2018; 206:60–73 [View Article][PubMed]
     [Google Scholar]
  5. 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]
  6. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J et al. Supplement 2003-2007 (NO. 47) to the White-Kauffmann-Le minor scheme. Res Microbiol 2010; 161:26–29 [View Article][PubMed]
     [Google Scholar]
  7. Le Minor L, Véron M, Popoff M. [A proposal for Salmonella nomenclature]. Ann Microbiol 1982; 133:245–254[PubMed]
     [Google Scholar]
  8. Tracy LM, Hicks JA, Grogan KB, Nicholds JA, Morningstar-Shaw BR et al. Molecular detection of Salmonella enterica subsp. arizonae by quantitative PCR. Avian Dis 64: [View Article]
     [Google Scholar]
  9. Mitchell MA, Shane SM. Salmonella in reptiles. Semin Avian Exot Pet Med 2001; 10:25–35 [View Article]
     [Google Scholar]
  10. Orós J, Rodríguez JL, Herráez P, Santana P, Fernández A. Respiratory and digestive lesions caused by Salmonella arizonae in two snakes. J Comp Pathol 1996; 115:185–189 [View Article][PubMed]
     [Google Scholar]
  11. Orós J, Rodríguez JL, Espinosa de los Monteros A, Rodríguez F, Herráez P et al. Tracheal malformation in a bicephalic Honduran milk snake (Lampropeltis hondurensis) and subsequent fatal Salmonella arizonae infection. J Zoo Wildl Med 1997; 28:331–335[PubMed]
     [Google Scholar]
  12. Boever WJ, Williams J. Arizona septicemia in three boa constrictors. Vet Med Small Anim Clin 1975; 70:1357–1359[PubMed]
     [Google Scholar]
  13. Krum SH, Stevens DR, Hirsh DC. Salmonella arizonae bacteremia in a cat. J Am Vet Med Assoc 1977; 170:42–44[PubMed]
     [Google Scholar]
  14. Macri NP, Stevenson GW, Wu CC. Salmonella arizonae sepsis in a Lynx. J Wildl Dis 1997; 33:908–911 [View Article][PubMed]
     [Google Scholar]
  15. Meehan JT, Brogden KA, Courtney C, Cutlip RC, Lehmkuhl HD. Chronic proliferative rhinitis associated with Salmonella arizonae in sheep. Vet Pathol 1992; 29:556–559 [View Article][PubMed]
     [Google Scholar]
  16. Shivaprasad HL. Arizonosis. In Swayne DE, Glisson JR, McDougald LR, Nolan LK, Suarez DL. (editors) Diseases of Poultry Ames, IA: Wiley-Blackwell; 2013 pp 706–713
     [Google Scholar]
  17. Hall ML, Rowe B. Salmonella arizonae in the United Kingdom from 1966 to 1990. Epidemiol Infect 1992; 108:59–65 [View Article][PubMed]
     [Google Scholar]
  18. Abbott SL, Ni FCY, Janda JM. Increase in extraintestinal infections caused by Salmonella enterica subspecies II-IV. Emerg Infect Dis 2012; 18:637–639 [View Article][PubMed]
     [Google Scholar]
  19. CDC National enteric disease surveillance: Salmonella annual report; 2016
  20. Lan R, Reeves PR, Octavia S. Population structure, origins and evolution of major Salmonella enterica clones. Infect Genet Evol 2009; 9:996–1005 [View Article][PubMed]
     [Google Scholar]
  21. 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; 4:19–21 [View Article][PubMed]
     [Google Scholar]
  22. den Bakker HC, Moreno Switt AI, Govoni G, Cummings CA, Ranieri ML et al. Genome sequencing reveals diversification of virulence factor content and possible host adaptation in distinct subpopulations of Salmonella enterica . BMC Genomics 2011; 12:425 [View Article][PubMed]
     [Google Scholar]
  23. 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]
  24. 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:e02303–02318 [View Article][PubMed]
     [Google Scholar]
  25. Boyd EF, Wang FS, Whittam TS, Selander RK. Molecular genetic relationships of the salmonellae . Appl Environ Microbiol 1996; 62:804–808 [View Article][PubMed]
     [Google Scholar]
  26. Desai PT, Porwollik S, Long F, Cheng P, Wollam A et al. Evolutionary genomics of Salmonella enterica subspecies. mBio 2013; 4:e00198–13 [View Article][PubMed]
     [Google Scholar]
  27. Criscuolo A, Issenhuth-Jeanjean S, Didelot X, Thorell K, Hale J et al. The speciation and hybridization history of the genus Salmonella . Microb Genom 2019; 5: [View Article][PubMed]
     [Google Scholar]
  28. Reeves MW, Evins GM, Heiba AA, Plikaytis BD, Farmer JJ. Clonal nature of Salmonella Typhi and its genetic relatedness to other salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov. J Clin Microbiol 1989; 27:313–320 [View Article][PubMed]
     [Google Scholar]
  29. Chan K, Baker S, Kim CC, Detweiler CS, Dougan G et al. Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar Typhimurium DNA microarray. J Bacteriol 2003; 185:553–563 [View Article][PubMed]
     [Google Scholar]
  30. Blondel CJ, Jiménez JC, Contreras I, Santiviago CA. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 2009; 10:354 [View Article][PubMed]
     [Google Scholar]
  31. 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]
  32. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
     [Google Scholar]
  33. 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]
  34. 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]
  35. 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]
  36. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article][PubMed]
     [Google Scholar]
  37. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article][PubMed]
     [Google Scholar]
  38. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2:e000056 [View Article][PubMed]
     [Google Scholar]
  39. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
     [Google Scholar]
  40. Torpdahl M, Skov MN, Sandvang D, Baggesen DL. Genotypic characterization of Salmonella by multilocus sequence typing, pulsed-field gel electrophoresis and amplified fragment length polymorphism. J Microbiol Methods 2005; 63:173–184 [View Article][PubMed]
     [Google Scholar]
  41. Grissa I, Vergnaud G, Pourcel C. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 2007; 8:172 [View Article][PubMed]
     [Google Scholar]
  42. Couvin D, Bernheim A, Toffano-Nioche C, Touchon M, Michalik J et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res 2018; 46:W246–W251 [View Article][PubMed]
     [Google Scholar]
  43. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–W21 [View Article][PubMed]
     [Google Scholar]
  44. Besemer J, Borodovsky M. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 2005; 33:W451–W454 [View Article][PubMed]
     [Google Scholar]
  45. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
     [Google Scholar]
  46. 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]
  47. Libby SJ, Lesnick M, Hasegawa P, Kurth M, Belcher C et al. Characterization of the spv locus in Salmonella enterica serovar Arizona. Infect Immun 2002; 70:3290–3294 [View Article][PubMed]
     [Google Scholar]
  48. Cambre RC, Green DE, Smith EE, Montali RJ, Bush M. Salmonellosis and arizonosis in the reptile collection at the National zoological Park. J Am Vet Med Assoc 1980; 177:800–883[PubMed]
     [Google Scholar]
  49. Lock BA, Wellehan J. Chapter 8 - Ophidia (Snakes). In Miller RE Fowler. editor MEBT-FZ and WAM 8 St. Louis: W.B. Saunders; pp 60–74
     [Google Scholar]
  50. 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]
  51. Octavia S, Lan R. Frequent recombination and low level of clonality within Salmonella enterica subspecies I. Microbiology 2006; 152:1099–1108 [View Article][PubMed]
     [Google Scholar]
  52. 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]
  53. 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]
  54. 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]
  55. 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]
  56. Brown EW, Mammel MK, LeClerc JE, Cebula TA. Limited boundaries for extensive horizontal gene transfer among Salmonella pathogens. Proc Natl Acad Sci U S A 2003; 100:15676–15681 [View Article][PubMed]
     [Google Scholar]
  57. Didelot X, Achtman M, Parkhill J, Thomson NR, Falush D. A bimodal pattern of relatedness between the Salmonella Paratyphi A and Typhi genomes: convergence or divergence by homologous recombination?. Genome Res 2007; 17:61–68 [View Article][PubMed]
     [Google Scholar]
  58. Didelot X, Bowden R, Street T, Golubchik T, Spencer C et al. Recombination and population structure in Salmonella enterica . PLoS Genet 2011; 7:e1002191 [View Article][PubMed]
     [Google Scholar]
  59. Soyer Y, Moreno Switt A, Davis MA, Maurer J, McDonough PL et al. Salmonella enterica serotype 4,5,12:i:-, an emerging Salmonella serotype that represents multiple distinct clones. J Clin Microbiol 2009; 47:3546–3556 [View Article][PubMed]
     [Google Scholar]
  60. Centers for Disease Control and Prevention https://www.cdc.gov/salmonella/pdf/salmonella-atlas-508c.pdf ; 2013
  61. Figueroa-Bossi N, Uzzau S, Maloriol D, Bossi L. Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella . Mol Microbiol 2001; 39:260–272 [View Article][PubMed]
     [Google Scholar]
  62. Switt AIM, Sulakvelidze A, Wiedmann M, Kropinski AM, Wishart DS et al. Salmonella phages and prophages: genomics, taxonomy, and applied aspects. Methods Mol Biol 2015; 1225:237–287 [View Article][PubMed]
     [Google Scholar]
  63. Colavecchio A, D'Souza Y, Tompkins E, Jeukens J, Freschi L et al. Prophage integrase typing is a useful indicator of genomic diversity in Salmonella enterica . Front Microbiol 2017; 8:1283 [View Article][PubMed]
     [Google Scholar]
  64. Bruno VM, Hannemann S, Lara-Tejero M, Flavell RA, Kleinstein SH et al. Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog 2009; 5:e1000538 [View Article][PubMed]
     [Google Scholar]
  65. Patel JC, Galán JE. Manipulation of the host actin cytoskeleton by Salmonella-all in the name of entry. Curr Opin Microbiol 2005; 8:10–15 [View Article][PubMed]
     [Google Scholar]
  66. Hapfelmeier S, Stecher B, Barthel M, Kremer M, Müller AJ et al. 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 2005; 174:1675–1685 [View Article][PubMed]
     [Google Scholar]
  67. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E et al. Simultaneous identification of bacterial virulence genes by negative selection. Science 1995; 269:400–403 [View Article][PubMed]
     [Google Scholar]
  68. Ochman H, Groisman EA. Distribution of pathogenicity islands in Salmonella spp. Infect Immun 1996; 64:5410–5412 [View Article][PubMed]
     [Google Scholar]
  69. Jennings E, Thurston TLM, Holden DW. Salmonella SPI-2 type III secretion system effectors: molecular mechanisms and physiological consequences. Cell Host Microbe 2017; 22:217–231 [View Article][PubMed]
     [Google Scholar]
  70. Salcedo SP, Holden DW. Sseg, a virulence protein that targets Salmonella to the Golgi network. Embo J 2003; 22:5003–5014 [View Article][PubMed]
     [Google Scholar]
  71. Grabe GJ, Zhang Y, Przydacz M, Rolhion N, Yang Y. The Salmonella effector SpvD is a cysteine hydrolase with a serovar-specific polymorphism influencing catalytic activity, suppression of immune responses, and bacterial virulence. J Biol Chem 2016; 291:25853 [View Article][PubMed]
     [Google Scholar]
  72. Guiney DG, Fierer J. The role of the spv genes in Salmonella pathogenesis. Front Microbiol 2011; 2:129 [View Article][PubMed]
     [Google Scholar]
  73. Boyd EF, Hartl DL. Salmonella virulence plasmid. modular acquisition of the spv virulence region by an F-plasmid in Salmonella enterica subspecies I and insertion into the chromosome of subspecies II, IIIa, IV and VII isolates. Genetics 1998; 149:1183 LP–1190[PubMed]
     [Google Scholar]
  74. 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]
  75. Fookes M, Schroeder GN, Langridge GC, Blondel CJ, Mammina C et al. Salmonella bongori provides insights into the evolution of the salmonellae. PLoS Pathog 2011; 7:e1002191 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000522
Loading
Phylogeny of Salmonella enterica subspecies arizonae by whole-genome sequencing reveals high incidence of polyphyly and low phase 1 H antigen variability
M Gen 7, 000522 (2021); https://doi.org/10.1099/mgen.0.000522
/content/journal/mgen/10.1099/mgen.0.000522
/content/journal/mgen/10.1099/mgen.0.000522
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Most cited 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