Whole-genome sequencing investigation of animal-skin-drum-associated UK anthrax cases reveals evidence of mixed populations and relatedness to a US case Open Access

Abstract

There have been two anthrax cases affecting people that played and/or made animal-skin drums in the UK during the last 10 years, with single fatal occurrences in Scotland in 2006 and London in 2008. Investigations by the Health Protection Agency (now Public Health England) employing multi-locus-variable number tandem repeat analysis had previously linked the clinical cases to spores associated with animal skins and drums the patients had been in contact with. In this study, whole-genome sequencing of 23 isolates harvested during the investigations was performed. High-quality draft assemblies of these genomes provided greater characterization of the strains present and placed them all upon a new branch of the global phylogeny. Although closely related, the clinical isolates from the two events, and another isolated from a drum-skin-associated case in New York in 2006, were distinct from each other. Multiple distinct genotypes were found during both investigations, implying either multiple contamination events or a single heterogeneous contamination. One environmental isolate from the Scottish incident was more closely related to London isolates than to the other Scottish isolates. As of this subgroup was present at both geographically and temporally distinct events, it may be more widespread at the source of contamination. All isolates were distinct from currently characterized West African strains, despite this being the likely origin of the drums and hides, therefore adding to our knowledge of diversity in the region.

Keyword(s): animal-hide , anthrax , phylogeography and UK
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000039
2015-11-06
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/mgen/1/5/mgen000039.html?itemId=/content/journal/mgen/10.1099/mgen.0.000039&mimeType=html&fmt=ahah

References

  1. Anaraki S., Addiman S., Nixon G., Krahé D., Ghosh R., Brooks T., Lloyd G., Spencer R., Walsh A., other authors. 2008; Investigations and control measures following a case of inhalation anthrax in East London in a drum maker and drummer, October 2008. Euro Surveill 13:19076[PubMed]
    [Google Scholar]
  2. Ågren J., Finn M., Bengtsson B., Segerman B. 2014; Microevolution during an Anthrax outbreak leading to clonal heterogeneity and penicillin resistance. PLoS One 9:e89112 [View Article][PubMed]
    [Google Scholar]
  3. Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., Lesin V. M., Nikolenko S. I., Pham S., other authors. 2012; SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477 [View Article][PubMed]
    [Google Scholar]
  4. Blankenberg D., Von Kuster G., Coraor N., Ananda G., Lazarus R., Mangan M., Nekrutenko A., Taylor J. 2010; Galaxy: a web-based genome analysis tool for experimentalists. Curr Prot Mol Biol 19:101–1021
    [Google Scholar]
  5. Bolger A. M., Lohse M., Usadel B. 2014; Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  6. CDC 2006; Inhalation anthrax associated with dried animal hides- Pennsylvania and New York City, 2006. MMWR Morb Mortal Wkly Rep 55:280–282[PubMed]
    [Google Scholar]
  7. CDC 2010; Gastrointestinal anthrax after an animal-hide drumming event-New Hampshire and Massachusetts, 2009. MMWR Morb Mortal Wkly Rep 59:872–877[PubMed]
    [Google Scholar]
  8. DePristo M. A., Banks E., Poplin R., Garimella K. V., Maguire J. R., Hartl C., Philippakis A. A., del Angel G., Rivas M. A., other authors. 2011; A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498 [View Article][PubMed]
    [Google Scholar]
  9. Derzelle S., Girault G., Roest H. I. J., Koene M. 2015; Molecular diversity of Bacillus anthracis in the Netherlands: investigating the relationship to the worldwide population using whole-genome SNP discovery. Infect Genet Evol 32:370–376 [CrossRef]
    [Google Scholar]
  10. Eyre D. W., Cule M. L., Wilson D. J., Griffiths D., Vaughan A., O'Connor L., Ip C. L. C., Golubchik T., Batty E. M., other authors. 2013; Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med 369:1195–1205 [View Article][PubMed]
    [Google Scholar]
  11. Frampton M., Houlston R. 2012; Generation of artificial FASTQ files to evaluate the performance of next-generation sequencing pipelines. PLoS One 7:e49110 [View Article][PubMed]
    [Google Scholar]
  12. Gardy J. L., Johnston J. C., Ho Sui S. J., Cook V. J., Shah L., Brodkin E., Rempel S., Moore R., Zhao Y., other authors. 2011; Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 364:730–739 [View Article][PubMed]
    [Google Scholar]
  13. Giardine B., Riemer C., Hardison R. C., Burhans R., Elnitski L., Shah P., Zhang Y., Blankenberg D., Albert I., other authors. 2005; Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15:1451–1455 [View Article][PubMed]
    [Google Scholar]
  14. Goecks J., Nekrutenko A., Taylor J., Galaxy Team T., Galaxy Team. 2010; Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11:R86 [View Article][PubMed]
    [Google Scholar]
  15. Guh A., Heyman M. L., Barden D., Fontana J., Hadler J. L. 2010; Lessons learned from the investigation of a cluster of cutaneous anthrax cases in Connecticut. J Public Health Manag Pract 16:201–210 [View Article][PubMed]
    [Google Scholar]
  16. Keim P., Price L. B., Klevytska A. M., Smith K. L., Schupp J. M., Okinaka R., Jackson P. J., Hugh-Jones M. E. 2000; Multiple-locus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis . J Bacteriol 182:2928–2936 [View Article][PubMed]
    [Google Scholar]
  17. Köser C. U., Holden M. T. G., Ellington M. J., Cartwright E. J. P., Brown N. M., Ogilvy-Stuart A. L., Hsu L. Y., Chewapreecha C., Croucher N. J., other authors. 2012; Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366:2267–2275 [View Article][PubMed]
    [Google Scholar]
  18. Li H., Durbin R. 2009; Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760 [View Article][PubMed]
    [Google Scholar]
  19. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R., 1000 Genome Project Data Processing Subgroup. 2009; The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  20. Marston C. K., Allen C. A., Beaudry J., Price E. P., Wolken S. R., Pearson T., Keim P., Hoffmaster A. R. 2011; Molecular epidemiology of anthrax cases associated with recreational use of animal hides and yarn in the United States. PLoS One 6:e28274 [View Article][PubMed]
    [Google Scholar]
  21. Nguyen T. Q., Clark N., The 2006 NYC Anthrax Working Group. 2010; Public health and environmental response to the first case of naturally acquired inhalational anthrax in the United States in 30 years: infection of a New York City resident who worked with dried animal hides. J Public Health Manag Pract 16:189–200 [View Article][PubMed]
    [Google Scholar]
  22. Osborn S. H. 1920; Anthrax problem in Massachusetts. Am J Public Health (N Y) 10:657–665 [View Article][PubMed]
    [Google Scholar]
  23. Pearson T., Okinaka R. T., Foster J. T., Keim P. 2009; Phylogenetic understanding of clonal populations in an era of whole genome sequencing. Infect Genet Evol 9:1010–1019 [View Article][PubMed]
    [Google Scholar]
  24. Price E. P., Seymour M. L., Sarovich D. S., Latham J., Wolken S. R., Mason J., Vincent G., Drees K. P., Beckstrom-Sternberg S. M., other authors. 2012; Molecular epidemiologic investigation of an anthrax outbreak among heroin users, Europe. Emerg Infect Dis 18:1307–1313 [View Article][PubMed]
    [Google Scholar]
  25. Riley A. 2007; Report on the management of an anthrax incident in the Scottish Borders, July 2006 to May 2007. http://news.bbc.co.uk/1/shared/bsp/hi/pdfs/13_12_07_anthrax.pdf
  26. Rouli L., MBengue M., Robert C., Ndiaye M., La Scola B., Raoult D. 2014; Genomic analysis of three African strains of Bacillus anthracis demonstrates that they are part of the clonal expansion of an exclusively pathogenic bacterium. New Microbes New Infect 2:161–169 [View Article][PubMed]
    [Google Scholar]
  27. Stratilo C., Bader D. 2007; Molecular typing of Bacillus anthracis using multiple-locus variable number tandem repeat analysis (MLVA-8). Defence R&D Canada, Technical Memorandum.
    [Google Scholar]
  28. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  29. Treangen T. J., Ondov B. D., Koren S., Phillippy A. M. 2014; The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 15:524 [View Article][PubMed]
    [Google Scholar]
  30. Van Ert M. N., Easterday W. R., Huynh L. Y., Okinaka R. T., Hugh-Jones M. E., Ravel J., Zanecki S. R., Pearson T., Simonson T. S., other authors. 2007; Global genetic population structure of Bacillus anthracis . PLoS One 2:e461 [View Article][PubMed]
    [Google Scholar]
  31. Vogler A. J., Busch J. D., Percy-Fine S., Tipton-Hunton C., Smith K. L., Keim P. 2002; Molecular analysis of rifampin resistance in Bacillus anthracis and Bacillus cereus . Antimicrob Agents Chemother 46:511–513 [View Article][PubMed]
    [Google Scholar]
  32. Pullan, S. T. (2015). Sequence Read Archive, BioProject: PRJNA287512 (2015).
  33. Pullan, S. (2015). Figshare, Table S4. http://dx.doi.org/10.6084/m9.figshare.1569313.
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000039
Loading
/content/journal/mgen/10.1099/mgen.0.000039
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited Most Cited RSS feed