1887

Abstract

The serotype Paratyphi B complex causes a wide range of diseases, from gastroenteritis to paratyphoid fever, depending on the biotypes Java and . The burden of Paratyphi B biotypes in Bangladesh is still unknown, as these are indistinguishable by serotyping. Here, we conducted the first whole-genome sequencing (WGS) study on 79 isolates serotyped as Paratyphi B that were collected from 10 nationwide enteric disease surveillance sites in Bangladesh. Placing these in a global genetic context revealed that these are biotype Java, and the addition of these genomes expanded the previously described PG4 clade containing Bangladeshi and UK isolates. Importantly, antimicrobial resistance (AMR) genes were scarce amongst Bangladeshi . Java isolates, somewhat surprisingly given the widespread availability of antibiotics without prescription. This genomic information provides important insights into the significance of . Paratyphi B biotypes in enteric disease and their implications for public health.

Funding
This study was supported by the:
  • National Institute for Health Research
    • Principle Award Recipient: GordonDougan
  • Bill and Melinda Gates Foundation (Award OPP1135223)
    • Principle Award Recipient: FirdausiQadri
  • Wellcome Trust (Award 206194)
    • Principle Award Recipient: FirdausiQadri
  • 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.0.000617
2021-09-22
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/9/mgen000617.html?itemId=/content/journal/mgen/10.1099/mgen.0.000617&mimeType=html&fmt=ahah

References

  1. Brenner FW, Villar RG, Angulo FJ, Tauxe R, Swaminathan B. Salmonella nomenclature. J Clin Microbiol 2000; 38:2465–2467 [View Article] [PubMed]
    [Google Scholar]
  2. Connor T, Owen SV, Langridge G, Connell S, Nair S. What’s in a name? Species wide whole genome sequencing resolves invasive and non-invasive Salmonella Paratyphi B. mBio 2016; 7: [View Article] [PubMed]
    [Google Scholar]
  3. Chart H. The pathogenicity of strains of Salmonella paratyphi B and Salmonella java. J Appl Microbiol 2003; 94:340–348 [View Article] [PubMed]
    [Google Scholar]
  4. Higginson EE, Ramachandran G, Hazen TH, Kania DA, Rasko DA et al. Improving our understanding of salmonella enterica Serovar paratyphi B through the engineering and testing of a live attenuated vaccine strain. mSphere 2018; 3:e00474-00418 [View Article] [PubMed]
    [Google Scholar]
  5. Barker RM, Kearney GM, Nicholson P, Blair AL, Porter R. Types of Salmonella paratyphi B and their phylogenetic significance. J Med Microbiol 1988; 26:285–293 [View Article] [PubMed]
    [Google Scholar]
  6. Ezquerra E, Burnens A, Jones C, Stanley J. Genotypic typing and phylogenetic analysis of Salmonella paratyphi B and S. java with IS200. Microbiology 1993; 139:2409–2414
    [Google Scholar]
  7. 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]
  8. Fabre L, Zhang J, Guigon G, Le Hello S, Guibert V. CRISPR typing and subtyping for improved laboratory surveillance of Salmonella infections. PloS one 2012; 7:e36995 [View Article] [PubMed]
    [Google Scholar]
  9. Authority EFS Report of the Task Force on Zoonoses Data Collection on the Analysis of the baseline survey on the prevalence of Salmonella in broiler flocks of Gallus gallus, in the EU, 2005–2006‐Part B: factors related to Salmonella flock prevalence, distribution of Salmonella serovars, and antimicrobial resistance patterns. EFSA Journal 2007; 5:101r
    [Google Scholar]
  10. Gobin M, Launders N, Lane C, Kafatos G, Adak B. National outbreak of Salmonella Java phage type 3b variant 9 infection using parallel case-control and case-case study designs, United Kingdom, July to October 2010. Euro Surveill 2011; 16:20023 [PubMed]
    [Google Scholar]
  11. Al-Nakhli H, Al-Ogaily Z, Nassar T. Representative Salmonella serovars isolated from poultry and poultry environments in Saudi Arabia. Revue Scientifique et Technique-Office International des Epizooties 1999; 18:700–709
    [Google Scholar]
  12. Barua H, Biswas PK, Talukder KA, Olsen KE, Christensen JP. Poultry as a possible source of non-typhoidal Salmonella enterica serovars in humans in Bangladesh. Vet Microbiol 2014; 168:372–380 [View Article] [PubMed]
    [Google Scholar]
  13. Rahman SIA, Dyson ZA, Klemm EJ, Khanam F, Holt KE. Population structure and antimicrobial resistance patterns of Salmonella Typhi isolates in urban Dhaka, Bangladesh from 2004 to 2016. PLoS Negl Trop Dis 2020; 14:e0008036 [View Article] [PubMed]
    [Google Scholar]
  14. Khan AI, Rashid MM, Islam MT, Afrad MH, Salimuzzaman M et al. Epidemiology of cholera in Bangladesh: findings from Nationwide Hospital-based Surveillance, 2014–2018. Clin Infect Dis 2019
    [Google Scholar]
  15. Sack RB, Siddique AK, Longini IM, Nizam A, Yunus M. A 4-year study of the epidemiology of Vibrio cholerae in four rural areas of Bangladesh. J Infect Dis 2003; 187:96–101 [View Article] [PubMed]
    [Google Scholar]
  16. Khanam F, Sheikh A, Sayeed MA, Bhuiyan MS, Choudhury FK et al. Evaluation of a typhoid/paratyphoid diagnostic assay (TPTest) detecting anti-Salmonella IgA in secretions of peripheral blood lymphocytes in patients in Dhaka, Bangladesh. PLoS Negl Trop Dis 2013; 7:e2316 [View Article]
    [Google Scholar]
  17. Ponstingl H, Ning Z. SMALT-a new mapper for DNA sequencing reads. F1000 Posters 2010; 1:313
    [Google Scholar]
  18. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
    [Google Scholar]
  19. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2:e000056
    [Google Scholar]
  20. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
    [Google Scholar]
  21. 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]
  22. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007; 23:127–128 [View Article] [PubMed]
    [Google Scholar]
  23. Yu G, Smith DK, Zhu H, Guan Y, Lam TT et al. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2016; 8:28–36 [View Article]
    [Google Scholar]
  24. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. RhierBAPS: An R implementation of the population clustering algorithm hierBAPS. Wellcome Open Res 2018; 3:93 [View Article] [PubMed]
    [Google Scholar]
  25. StataCorp L. Stata Statistical Software: Release 12.0 College Station, TX: StataCorp LP; 2011
    [Google Scholar]
  26. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  27. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  28. 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]
  29. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  30. Snipen L, Liland KH. micropan: an R-package for microbial pan-genomics. BMC Bioinformatics 2015; 16:79 [View Article] [PubMed]
    [Google Scholar]
  31. Tettelin H, Riley D, Cattuto C, Medini D. Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 2008; 11:472–477 [View Article] [PubMed]
    [Google Scholar]
  32. Baddam R, Kumar N, Shaik S, Lankapalli AK, Ahmed N. Genome dynamics and evolution of Salmonella Typhi strains from the typhoid-endemic zones. Sci Rep 2014; 4:7457 [View Article] [PubMed]
    [Google Scholar]
  33. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 2020; 21:180 [View Article] [PubMed]
    [Google Scholar]
  34. Hadfield J, Croucher NJ, Goater RJ, Abudahab K, Aanensen DM et al. Phandango: an interactive viewer for bacterial population genomics. Bioinformatics 2017; 34:292–293
    [Google Scholar]
  35. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498–2504 [View Article] [PubMed]
    [Google Scholar]
  36. Donkor ES, Dayie NT, Adiku TK. Bioinformatics with basic local alignment search tool (blast) and fast alignment (fasta). J Bioinform Seq Anal 2014; 6:1–6
    [Google Scholar]
  37. Jones P, Binns D, Chang H-Y, Fraser M, Li W. InterProScan 5: genome-scale protein function classification. Bioinformatics 2014; 30:1236–1240 [View Article] [PubMed]
    [Google Scholar]
  38. Eichinger V, Nussbaumer T, Platzer A, Jehl M-A, Arnold R et al. EffectiveDB--updates and novel features for a better annotation of bacterial secreted proteins and Type III, IV, VI secretion systems. Nucleic Acids Res 2016; 44:D669–74D669 [View Article]
    [Google Scholar]
  39. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: Rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:e000131 [View Article]
    [Google Scholar]
  40. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 2013; 57:3348–3357 [View Article] [PubMed]
    [Google Scholar]
  41. Carattoli A, Zankari E, García-Fernández A, Larsen MV, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother (Bethesda) 2014; 58:3895–3903 [View Article]
    [Google Scholar]
  42. Chen L, Yang J, Yu J, Yao Z, Sun L et al. VFDB: A reference database for bacterial virulence factors. Nucleic Acids Research 2005; 33:D325–D328
    [Google Scholar]
  43. 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]
  44. Argimón S, Yeats CA, Goater RJ, Abudahab K, Taylor B et al. A global resource for genomic predictions of antimicrobial resistance and surveillance of Salmonella Typhi at Pathogenwatch. bioRxiv 2020.2007.2003.186692:
    [Google Scholar]
  45. Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:90 [View Article] [PubMed]
    [Google Scholar]
  46. Azriel S, Goren A, Shomer I, Aviv G, Rahav G. 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]
  47. Robinson N. Typhi colonization factor (Tcf) genetically conserved yet functionally diverse. Virulence 2017; 8:1511–1512 [View Article] [PubMed]
    [Google Scholar]
  48. Dhanani AS, Block G, Dewar K, Forgetta V, Topp E et al. Genomic Comparison of Non-Typhoidal Salmonella enterica Serovars Typhimurium, Enteritidis, Heidelberg, Hadar and Kentucky Isolates from Broiler Chickens. PLoS One 2015; 10:e0128773
    [Google Scholar]
  49. Lou L, Zhang P, Piao R, Wang Y. Salmonella pathogenicity Island 1 (SPI-1) and its complex regulatory network. Front Cell Infect Microbiol 2019; 9:270 [View Article]
    [Google Scholar]
  50. Mirold S, Rabsch W, Tschäpe H, Hardt WD. Transfer of the Salmonella type III effector sopE between unrelated phage families. J Mol Biol 2001; 312:7–16 [View Article] [PubMed]
    [Google Scholar]
  51. Kidgell C, Pickard D, Wain J, James K, Diem Nga LT. Characterisation and distribution of a cryptic Salmonella typhi plasmid pHCM2. Plasmid 2002; 47:159–171 [View Article] [PubMed]
    [Google Scholar]
  52. Zhang D, Zhao Y, Feng J, Hu L, Jiang X et al. Replicon-based typing of inci-complex plasmids, and comparative genomics analysis of inciγ/k1 plasmids. Front Microbiol 2019; 10:48 [View Article]
    [Google Scholar]
  53. Khanam F, Rajib NH, Tonks S, Khalequzzaman M, Pollard AJ et al. Case report: Salmonella enterica serovar paratyphi B infection in a febrile ILL child during enhanced passive surveillance in an urban slum in Mirpur, Dhaka. Am J Trop Med Hyg 2020; 103:231–233 [View Article] [PubMed]
    [Google Scholar]
  54. Threlfall J, Levent B, Hopkins KL, de Pinna E, Ward LR et al. Multidrug-resistant Salmonella Java. Emerging Infect Dis 2005; 11:170–171
    [Google Scholar]
  55. Kloska F, Beyerbach M, Klein G. Infection dynamics and antimicrobial resistance profile of Salmonella paratyphi B d-tartrate positive (JAVA) in a persistently infected broiler barn. Int J Environ Res Public Health 2017; 14: [View Article] [PubMed]
    [Google Scholar]
  56. LH S, Chiu CH. Salmonella: clinical importance and evolution of nomenclature. Chang Gung Med J 2007; 30:210–219 [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000617
Loading
/content/journal/mgen/10.1099/mgen.0.000617
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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