1887

Abstract

Melioidosis is a tropical disease caused by the bacterium Burkholderia pseudomallei. Outbreaks are uncommon and can generally be attributed to a single point source and strain. We used whole-genome sequencing to analyse B. pseudomallei isolates collected from an historical 2-year long case cluster that occurred in a remote northern Australian indigenous island community, where infections were previously linked to a contaminated communal water supply. We analysed the genome-wide relatedness of the two most common multilocus sequence types (STs) involved in the outbreak, STs 125 and 126. This analysis showed that although these STs were closely related on a whole-genome level, they demonstrated evidence of multiple recombination events that were unlikely to have occurred over the timeframe of the outbreak. Based on epidemiological and genetic data, we also identified two additional patients not previously associated with this outbreak. Our results confirm the previous hypothesis that a single unchlorinated water source harbouring multiple B. pseudomallei strains was linked to the outbreak, and that increased melioidosis risk in this community was associated with Piper methysticum root (kava) consumption.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000117
2017-06-13
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/mgen/3/8/mgen000117.html?itemId=/content/journal/mgen/10.1099/mgen.0.000117&mimeType=html&fmt=ahah

References

  1. Limmathurotsakul D, Golding N, Dance DA, Messina JP, Pigott DM et al. Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nat Microbiol 2016;1::15008
    [Google Scholar]
  2. Sarovich DS, Garin B, de Smet B, Kaestli M, Mayo M et al. Phylogenomic analysis reveals an Asian origin for African Burkholderia pseudomallei and further supports melioidosis endemicity in Africa. mSphere 2016;1:e00089-15 [CrossRef][PubMed]
    [Google Scholar]
  3. Wiersinga WJ, Currie BJ, Peacock SJ. Melioidosis. N Engl J Med 2012;367:1035–1044 [CrossRef][PubMed]
    [Google Scholar]
  4. Price EP, Hornstra HM, Limmathurotsakul D, Max TL, Sarovich DS et al. Within-host evolution of Burkholderia pseudomallei in four cases of acute melioidosis. PLoS Pathog 2010;6:e1000725 [CrossRef][PubMed]
    [Google Scholar]
  5. Currie BJ, Haslem A, Pearson T, Hornstra H, Leadem B et al. Identification of melioidosis outbreak by multilocus variable number tandem repeat analysis. Emerg Infect Dis 2009;15:169–174 [CrossRef][PubMed]
    [Google Scholar]
  6. Currie BJ, Mayo M, Anstey NM, Donohoe P, Haase A et al. A cluster of melioidosis cases from an endemic region is clonal and is linked to the water supply using molecular typing of Burkholderia pseudomallei isolates. Am J Trop Med Hyg 2001;65:177–179[PubMed]
    [Google Scholar]
  7. Inglis TJ, Garrow SC, Henderson M, Clair A, Sampson J et al. Burkholderia pseudomallei traced to water treatment plant in Australia. Emerg Infect Dis 2000;6:56–59 [CrossRef][PubMed]
    [Google Scholar]
  8. Gal D, Mayo M, Smith-Vaughan H, Dasari P, McKinnon M et al. Contamination of hand wash detergent linked to occupationally acquired melioidosis. Am J Trop Med Hyg 2004;71:360–362[PubMed]
    [Google Scholar]
  9. De Smet B, Sarovich DS, Price EP, Mayo M, Theobald V et al. Whole-genome sequencing confirms that Burkholderia pseudomallei multilocus sequence types common to both Cambodia and Australia are due to homoplasy. J Clin Microbiol 2015;53:323–326 [CrossRef][PubMed]
    [Google Scholar]
  10. McRobb E, Sarovich DS, Price EP, Kaestli M, Mayo M et al. Tracing melioidosis back to the source: using whole-genome sequencing to investigate an outbreak originating from a contaminated domestic water supply. J Clin Microbiol 2015;53:1144–1148 [CrossRef][PubMed]
    [Google Scholar]
  11. Currie BJ, Gal D, Mayo M, Ward L, Godoy D et al. Using BOX-PCR to exclude a clonal outbreak of melioidosis. BMC Infect Dis 2007;7:68 [CrossRef][PubMed]
    [Google Scholar]
  12. Currie BJ, Ward L, Cheng AC. The epidemiology and clinical spectrum of melioidosis: 540 cases from the 20 year Darwin prospective study. PLoS Negl Trop Dis 2010;4:e900 [CrossRef][PubMed]
    [Google Scholar]
  13. Johnson SL, Bishop-Lilly KA, Ladner JT, Daligault HE, Davenport KW et al. Complete genome sequences for 59 Burkholderia isolates, both pathogenic and near neighbor. Genome Announc 2015;3:e00159-15 [CrossRef][PubMed]
    [Google Scholar]
  14. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009;25:1754–1760 [CrossRef][PubMed]
    [Google Scholar]
  15. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010;20:1297–1303 [CrossRef][PubMed]
    [Google Scholar]
  16. Cingolani P, Platts A, Wang L, Coon M, Nguyen T et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012;6:80–92 [CrossRef][PubMed]
    [Google Scholar]
  17. Sarovich DS, Price EP. SPANDx: a genomics pipeline for comparative analysis of large haploid whole genome re-sequencing datasets. BMC Res Notes 2014;7:618 [CrossRef][PubMed]
    [Google Scholar]
  18. 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 [CrossRef][PubMed]
    [Google Scholar]
  19. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol 2015;11:e1004041 [CrossRef][PubMed]
    [Google Scholar]
  20. Swofford DL. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4 Sunderland, MA: Sinauer Associates; 2002
    [Google Scholar]
  21. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–1313 [CrossRef][PubMed]
    [Google Scholar]
  22. Chain PS, Grafham DV, Fulton RS, Fitzgerald MG, Hostetler J et al. Genome project standards in a new era of sequencing. Science 2009;326:236–237 [CrossRef][PubMed]
    [Google Scholar]
  23. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30:2114–2120 [CrossRef][PubMed]
    [Google Scholar]
  24. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008;18:821–829 [CrossRef][PubMed]
    [Google Scholar]
  25. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011;27:578–579 [CrossRef][PubMed]
    [Google Scholar]
  26. Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol 2012;13:R56 [CrossRef][PubMed]
    [Google Scholar]
  27. Tsai IJ, Otto TD, Berriman M. Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol 2010;11:R41 [CrossRef][PubMed]
    [Google Scholar]
  28. Otto TD, Sanders M, Berriman M, Newbold C. Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 2010;26:1704–1707 [CrossRef][PubMed]
    [Google Scholar]
  29. Jolley KA, Maiden MC. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010;11:595 [CrossRef][PubMed]
    [Google Scholar]
  30. Chapple SN, Sarovich DS, Holden MT, Peacock SJ, Buller N et al. Whole-genome sequencing of a quarter-century melioidosis outbreak in temperate Australia uncovers a region of low-prevalence endemicity. Microb Genom 2016;2:e000067 [CrossRef][PubMed]
    [Google Scholar]
  31. Hayden HS, Lim R, Brittnacher MJ, Sims EH, Ramage ER et al. Evolution of Burkholderia pseudomallei in recurrent melioidosis. PLoS One 2012;7:e36507 [CrossRef][PubMed]
    [Google Scholar]
  32. Price EP, Sarovich DS, Mayo M, Tuanyok A, Drees KP et al. Within-host evolution of Burkholderia pseudomallei over a twelve-year chronic carriage infection. MBio 2013;4:e00388-13 [CrossRef][PubMed]
    [Google Scholar]
  33. Price EP, Sarovich DS, Viberg L, Mayo M, Kaestli M et al. Whole-genome sequencing of Burkholderia pseudomallei isolates from an unusual melioidosis case identifies a polyclonal infection with the same multilocus sequence type. J Clin Microbiol 2015;53:282–286 [CrossRef][PubMed]
    [Google Scholar]
  34. Spring-Pearson SM, Stone JK, Doyle A, Allender CJ, Okinaka RT et al. Pangenome analysis of Burkholderia pseudomallei: genome evolution preserves gene order despite high recombination rates. PLoS One 2015;10:e0140274 [CrossRef][PubMed]
    [Google Scholar]
  35. Price EP, Sarovich DS, Smith EJ, Machunter B, Harrington G et al. Unprecedented melioidosis cases in Northern Australia caused by an Asian Burkholderia pseudomallei strain identified by using large-scale comparative genomics. Appl Environ Microbiol 2016;82:954–963 [CrossRef][PubMed]
    [Google Scholar]
  36. Pearson T, Giffard P, Beckstrom-Sternberg S, Auerbach R, Hornstra H et al. Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer. BMC Biol 2009;7:78 [CrossRef][PubMed]
    [Google Scholar]
  37. Chewapreecha C, Holden MT, Vehkala M, Välimäki N, Yang Z et al. Global and regional dissemination and evolution of Burkholderia pseudomallei. Nat Microbiol 2017;2:16263 [CrossRef][PubMed]
    [Google Scholar]
  38. Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D et al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 2011;43:1275–1280 [CrossRef][PubMed]
    [Google Scholar]
  39. Meumann EM, Cheng AC, Ward L, Currie BJ. Clinical features and epidemiology of melioidosis pneumonia: results from a 21-year study and review of the literature. Clin Infect Dis 2012;54:362–369 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000117
Loading
/content/journal/mgen/10.1099/mgen.0.000117
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

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