1887

Abstract

Melioidosis, caused by the highly recombinogenic bacterium Burkholderia pseudomallei, is a disease with high mortality. Tracing the origin of melioidosis outbreaks and understanding how the bacterium spreads and persists in the environment are essential to protecting public and veterinary health and reducing mortality associated with outbreaks. We used whole-genome sequencing to compare isolates from a historical quarter-century outbreak that occurred between 1966 and 1991 in the Avon Valley, Western Australia, a region far outside the known range of B. pseudomallei endemicity. All Avon Valley outbreak isolates shared the same multilocus sequence type (ST-284), which has not been identified outside this region. We found substantial genetic diversity among isolates based on a comparison of genome-wide variants, with no clear correlation between genotypes and temporal, geographical or source data. We observed little evidence of recombination in the outbreak strains, indicating that genetic diversity among these isolates has primarily accrued by mutation. Phylogenomic analysis demonstrated that the isolates confidently grouped within the Australian B. pseudomallei clade, thereby ruling out introduction from a melioidosis-endemic region outside Australia. Collectively, our results point to B. pseudomallei ST-284 being present in the Avon Valley for longer than previously recognized, with its persistence and genomic diversity suggesting long-term, low-prevalence endemicity in this temperate region. Our findings provide a concerning demonstration of the potential for environmental persistence of B. pseudomallei far outside the conventional endemic regions. An expected increase in extreme weather events may reactivate latent B. pseudomallei populations in this region.

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2016-07-11
2021-10-26
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References

  1. Assefa S., Keane T. M., Otto T. D., Newbold C., Berriman M. 2009; ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 25:1968–1969 [View Article][PubMed]
    [Google Scholar]
  2. Boetzer M., Pirovano W. 2012; Toward almost closed genomes with GapFiller. Genome Biol 13:R56 [View Article][PubMed]
    [Google Scholar]
  3. Boetzer M., Henkel C. V., Jansen H. J., Butler D., Pirovano W. 2011; Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27:578–579 [View Article][PubMed]
    [Google Scholar]
  4. Cheng A. C., Currie B. J. 2005; Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18:383–416 [View Article][PubMed]
    [Google Scholar]
  5. Choy J. L., Mayo M., Janmaat A., Currie B. J. 2000; Animal melioidosis in Australia. Acta Trop 74:153–158 [View Article][PubMed]
    [Google Scholar]
  6. Cottew G. S., Sutherland A. K., Meehan J. F. 1952; Melioidosis in sheep in Queensland: description of an outbreak. Aust Vet J 28:113–123 [View Article]
    [Google Scholar]
  7. Croucher N. J., Page A. J., Connor T. R., Delaney A. J., Keane J. A., Bentley S. D., Parkhill J., Harris S. R. 2015; Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 43:e15 [View Article][PubMed]
    [Google Scholar]
  8. Currie B. J. 2015; Melioidosis: evolving concepts in epidemiology, pathogenesis, and treatment. Semin Respir Crit Care Med 36:111–125 [View Article][PubMed]
    [Google Scholar]
  9. Currie B. J., Gal D., Mayo M., Ward L., Godoy D., Spratt B. G., LiPuma J. J. 2007; Using BOX-PCR to exclude a clonal outbreak of melioidosis. BMC Infect Dis 7: [View Article][PubMed]
    [Google Scholar]
  10. Currie B., Smith-Vaughan H., Golledge C., Buller N., Sriprakash K. S., Kemp D. J. 1994; Pseudomonas pseudomallei isolates collected over 25 years from a non-tropical endemic focus show clonality on the basis of ribotyping. Epidemiol Infect 113:307–312 [View Article][PubMed]
    [Google Scholar]
  11. Dance D. A. 2015; Editorial commentary: melioidosis in Puerto Rico: the iceberg slowly emerges. Clin Infect Dis 60:251–253 [View Article][PubMed]
    [Google Scholar]
  12. Darling A. C., Mau B., Blattner F. R., Perna N. T. 2004; Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403 [View Article][PubMed]
    [Google Scholar]
  13. De Smet B., Sarovich D. S., Price E. P., Mayo M., Theobald V., Kham C., Heng S., Thong P., Holden M. T. et al. 2015; Whole-genome sequencing confirms that Burkholderia pseudomallei multilocus sequence types common to both Cambodia and Australia are due to homoplasy. J Clin Microbiol 53:323–326 [View Article][PubMed]
    [Google Scholar]
  14. Doker T. J., Sharp T. M., Rivera-Garcia B., Perez-Padilla J., Benoit T. J., Ellis E. M., Elrod M. G., Gee J. E., Shieh W. J. et al. 2015; Contact investigation of melioidosis cases reveals regional endemicity in Puerto Rico. Clin Infect Dis 60:243–250 [View Article][PubMed]
    [Google Scholar]
  15. Gardy J. L., Johnston J. C., Ho Sui S. J., Cook V. J., Shah L., Brodkin E., Rempel S., Moore R., Zhao Y. et al. 2011; Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 364:730–739 [View Article][PubMed]
    [Google Scholar]
  16. Godoy D., Randle G., Simpson A. J., Aanensen D. M., Pitt T. L., Kinoshita R., Spratt B. G. 2003; Multilocus sequence typing and evolutionary relationships among the causative agents of melioidosis and glanders, Burkholderia pseudomallei and Burkholderia mallei. J Clin Microbiol 41:2068–2079 [View Article][PubMed]
    [Google Scholar]
  17. Golledge C. L., Chin W. S., Tribe A. E., Condon R. J., Ashdown L. R. 1992; A case of human melioidosis originating in south-west Western Australia. Med J Aust 157:332–334[PubMed]
    [Google Scholar]
  18. Haase A., Melder A., Smith-Vaughan H., Kemp D., Currie B. 1995; Rapd analysis of isolates of Burkholderia pseudomallei from patients with recurrent melioidosis. Epidemiol Infect 115:115–121 [View Article][PubMed]
    [Google Scholar]
  19. Hendriksen R. S., Price L. B., Schupp J. M., Gillece J. D., Kaas R. S., Engelthaler D. M., Bortolaia V., Pearson T., Waters A. E. et al. 2011; Population genetics of Vibrio cholerae from Nepal in 2010: evidence on the origin of the Haitian outbreak. MBio 2:e0015700111 [View Article][PubMed]
    [Google Scholar]
  20. Holden M. T., Titball R. W., Peacock S. J., Cerdeño-Tárraga A. M., Atkins T., Crossman L. C., Pitt T., Churcher C., Mungall K. et al. 2004; Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 101:14240–14245 [View Article][PubMed]
    [Google Scholar]
  21. Huang W., Li L., Myers J. R., Marth G. T. 2012; Art: a next-generation sequencing read simulator. Bioinformatics 28:593–594 [View Article][PubMed]
    [Google Scholar]
  22. Inglis T. J., Sagripanti J. L. 2006; Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl Environ Microbiol 72:6865–6875 [View Article][PubMed]
    [Google Scholar]
  23. Johansson A., Lärkeryd A., Widerström M., Mörtberg S., Myrtännäs K., Ohrman C., Birdsell D., Keim P., Wagner D. M. et al. 2014; An outbreak of respiratory tularemia caused by diverse clones of Francisella tularensis. Clin Infect Dis 59:1546–1553 [View Article][PubMed]
    [Google Scholar]
  24. Ketterer P. J., Bamford V. W. 1967; A case of melioidosis in lambs in south Western Australia. Aust Vet J 43:79–80 [View Article]
    [Google Scholar]
  25. Köser C. U., Ellington M. J., Cartwright E. J. P., Gillespie S. H., Brown N. M., Farrington M., Holden M. T. G., Dougan G., Bentley S. D., other authors. 2012a; Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog 8:e1002824 [View Article]
    [Google Scholar]
  26. 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. et al. 2012b; Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366:2267–2275 [View Article][PubMed]
    [Google Scholar]
  27. Limmathurotsakul D., Golding N., Dance D. A., Messina J. P., Pigott D. M., Moyes C. L., Rolim D. B., Bertherat E., Day N. P. et al. 2016; Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nat Microbio 1: [View Article][PubMed]
    [Google Scholar]
  28. Limmathurotsakul D., Holden M. T., Coupland P., Price E. P., Chantratita N., Wuthiekanun V., Amornchai P., Parkhill J., Peacock S. J. 2014; Microevolution of Burkholderia pseudomallei during an acute infection. J Clin Microbiol 52:3418–3421 [View Article][PubMed]
    [Google Scholar]
  29. Lloyd J. M., Suijdendorp P., Soutar W. R. 1988; Melioidosis in a dog. Aust Vet J 65:191–192 [View Article][PubMed]
    [Google Scholar]
  30. McRobb E., Sarovich D. S., Price E. P., Kaestli M., Mayo M., Keim P., Currie B. J. 2015; Tracing melioidosis back to the source: using whole-genome sequencing to investigate an outbreak originating from a contaminated domestic water supply. J Clin Microbiol 53:1144–1148 [View Article][PubMed]
    [Google Scholar]
  31. Milne I., Stephen G., Bayer M., Cock P. J., Pritchard L., Cardle L., Shaw P. D., Marshall D. 2013; Using Tablet for visual exploration of second-generation sequencing data. Brief Bioinform 14:193–202 [View Article][PubMed]
    [Google Scholar]
  32. Mollaret H. H. 1988; L'affaire Du Jardin des plantesou comment la mélioïdose fit son apparition en France. Med Mal Infect 18:643–654 [View Article]
    [Google Scholar]
  33. Moore R. A., Tuanyok A., Woods D. E. 2008; Survival of Burkholderia pseudomallei in water. BMC Res Notes 1: [View Article][PubMed]
    [Google Scholar]
  34. Munckhof W. J., Mayo M. J., Scott I., Currie B. J. 2001; Fatal human melioidosis acquired in a subtropical Australian city. Am J Trop Med Hyg 65:325–328[PubMed]
    [Google Scholar]
  35. O'Brien H. 1834; Disordar [sic] among sheep. In The Perth Gazette and Western Australian Journal pp. 323–324 Perth, Western Australia: Charles Macfaull;
    [Google Scholar]
  36. Otto T. D., Sanders M., Berriman M., Newbold C. 2010; Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 26:1704–1707 [View Article][PubMed]
    [Google Scholar]
  37. Pearson T., Giffard P., Beckstrom-Sternberg S., Auerbach R., Hornstra H., Tuanyok A., Price E. P., Glass M. B., Leadem B. et al. 2009; Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer. BMC Biol 7: [View Article][PubMed]
    [Google Scholar]
  38. Pearson T., U'Ren J. M., Schupp J. M., Allan G. J., Foster P. G., Mayo M. J., Gal D., Choy J. L., Daugherty R. L. et al. 2007; VNTR analysis of selected outbreaks of Burkholderia pseudomallei in Australia. Infect Genet Evol 7:416–423 [View Article][PubMed]
    [Google Scholar]
  39. Price E. P., Hornstra H. M., Limmathurotsakul D., Max T. L., Sarovich D. S., Vogler A. J., Dale J. L., Ginther J. L., Leadem B. et al. 2010; Within-host evolution of Burkholderia pseudomallei in four cases of acute melioidosis. PLoS Pathog 6:e1000725 [View Article][PubMed]
    [Google Scholar]
  40. Price E. P., Sarovich D. S., Mayo M., Tuanyok A., Drees K. P., Kaestli M., Beckstrom-Sternberg S. M., Babic-Sternberg J. S., Kidd T. J. et al. 2013; Within-host evolution of Burkholderia pseudomallei over a twelve-year chronic carriage infection. MBio 4:e0038800313 [View Article][PubMed]
    [Google Scholar]
  41. Price E. P., Sarovich D. S., Smith E. J., MacHunter B., Harrington G., Theobald V., Hall C. M., Hornstra H. M., McRobb E. et al. 2016; Unprecedented melioidosis cases in Northern Australia caused by an Asian Burkholderia pseudomallei strain identified by using large-scale comparative genomics. Appl Environ Microbiol 82:954–963 [View Article]
    [Google Scholar]
  42. Price E. P., Sarovich D. S., Viberg L., Mayo M., Kaestli M., Tuanyok A., Foster J. T., Keim P., Pearson T. et al. 2015; 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 53:282–286 [View Article][PubMed]
    [Google Scholar]
  43. Sarovich D. S., Price E. P. 2014; SPANDx: a genomics pipeline for comparative analysis of large haploid whole genome re-sequencing datasets. BMC Res Notes 7: [View Article][PubMed]
    [Google Scholar]
  44. Sarovich D. S., Garin B., De Smet B., Kaestli M., Mayo M., Vandamme P., Jacobs J., Lompo P., Tahita M. C. et al. 2016; Phylogenomic analysis reveals an Asian origin for African Burkholderia pseudomallei and further supports melioidosis endemicity in Africa. MSphere 1:e0008900015 [View Article]
    [Google Scholar]
  45. Scott I. A., Bell A. M., Staines D. R. 1997; Fatal human melioidosis in south-eastern Queensland. Med J Aust 166:197–199[PubMed]
    [Google Scholar]
  46. Snitkin E. S., Zelazny A. M., Thomas P. J., Stock F., Henderson D. K., Palmore T. N., Segre J. A., Sequencing N. C. 2012; Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 4:ra116 [View Article]
    [Google Scholar]
  47. Swofford D. L. 2002 Phylogenetic analysis using parsimony (*and other methods). Version 4 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  48. Tsai I. J., Otto T. D., Berriman M. 2010; Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol 11:R41 [View Article][PubMed]
    [Google Scholar]
  49. Walker T. M., Ip C. L., Harrell R. H., Evans J. T., Kapatai G., Dedicoat M. J., Eyre D. W., Wilson D. J., Hawkey P. M. et al. 2013; Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 13:137–146 [View Article][PubMed]
    [Google Scholar]
  50. Wiersinga W. J., Currie B. J., Peacock S. J. 2012; Melioidosis. N Engl J Med 367:1035–1044 [View Article][PubMed]
    [Google Scholar]
  51. Wuthiekanun V., Smith M. D., White N. J. 1995; Survival of Burkholderia pseudomallei 587 in the absence of nutrients. Trans R Soc Trop Med Hyg 66:
    [Google Scholar]
  52. Yip T. W., Hewagama S., Mayo M., Price E. P., Sarovich D. S., Bastian I., Baird R. W., Spratt B. G., Currie B. J. 2015; Endemic melioidosis in residents of desert region after atypically intense rainfall in Central Australia, 2011. Emerg Infect Dis 21:1038–1040 [View Article][PubMed]
    [Google Scholar]
  53. Zerbino D. R., Birney E. 2008; Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829 [View Article][PubMed]
    [Google Scholar]
  54. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://www.ebi.ac.uk/ena/data/view/ERS205900 2016
  55. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://www.ebi.ac.uk/ena/data/view/ERS205902 2016
  56. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://www.ebi.ac.uk/ena/data/view/ERS205903 2016
  57. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://trace.ncbi.nlm.nih.gov/Traces/sra/?run=SRR2134233 2016
  58. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://trace.ncbi.nlm.nih.gov/Traces/sra/?run=SRR2134234 2016
  59. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://trace.ncbi.nlm.nih.gov/Traces/sra/?run=SRR2134235 2016
  60. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://trace.ncbi.nlm.nih.gov/Traces/sra/?run=SRR2134237 2016
  61. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://trace.ncbi.nlm.nih.gov/Traces/sra/?run=SRR2134238 2016
  62. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://trace.ncbi.nlm.nih.gov/Traces/sra/?run=SRR2134239 2016
  63. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://trace.ncbi.nlm.nih.gov/Traces/sra/?run=SRR2134240 2016
  64. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://trace.ncbi.nlm.nih.gov/Traces/sra/?run=SRR2134242 2016
  65. Chapple, S. N. J., Sarovich, N. S., Holden, M. T. G., Peacock, S. J., Buller, N., Golledge, C., Mayo, M., Currie, B. J., Price, E. P. http://www.ncbi.nlm.nih.gov/nuccore/LGKL00000000 2016
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