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Volume 7, Issue 11

Genetic diversity and transmission patterns of on Hainan island, China, revealed by a population genomics analysis Open Access

Abstract

is a Gram-negative soil-dwelling bacillus that causes melioidosis, a frequently fatal infectious disease, in tropical and subtropical regions. Previous studies have identified the overall genetic and evolutionary characteristics of on a global scale, including its origin and transmission routes. However, beyond its known hyperendemicity foci in northern Australia and Southeast Asia, the distribution and genetic characteristics of in most tropical regions remain poorly understood, including in southern China. Here, we sequenced the genomes of 122 strains collected from Hainan, an island in southern China, in 2002–2018, to investigate the population structure, relationships with global strains, local epidemiology, and virulence and antimicrobial-resistance factors. A phylogenetic analysis and hierarchical clustering divided the Hainan strains into nine phylogenic groups (PGs), 80 % of which were concentrated within five major groups (group 1: corresponding to minor sequence types [STs], 12.3 %; group 3: ST46 and ST50, 31.1 %; group 9: ST58, 13.1 %; group 11: ST55, 8.2 %; group 15: mainly ST658, 15.6%). A phylogenetic analysis that included global strains suggested that in Hainan originated from Southeast Asian countries, transmitted in multiple historical importation events. We also identified several mutual transmission events between Hainan and Southeast Asian countries in recent years, including three importation events from Thailand and Singapore to Hainan and three exportation events from Hainan to Singapore, Malaysia, and Taiwan island. A statistical analysis of the temporal distribution showed that the Hainan strains of groups 3, 9, and 15 have dominated the disease epidemic locally in the last 5 years. The spatial distribution of the Hainan strains demonstrated that some PGs are distributed in different cities on Hainan island, and by combining phylogenic and geographic distribution information, we detected 21 between-city transmission events, indicating its frequent local transmission. The detection of virulence factor genes showed that 56 % of the Hainan strains in group 1 encode a -specific adherence factor, , confirming the specific pathogenic characteristics of the Hainan strains in group 1. An analysis of the antimicrobial-resistance potential of showed that various kinds of alterations were identified in clinically relevant antibiotic resistance factors, such as AmrR, PenA and PBP3, etc. Our results clarify the population structure, local epidemiology, and pathogenic characteristics of in Hainan, providing further insight into its regional and global transmission networks and improving our knowledge of its global phylogeography.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacteria genetic diversity , Burkholderia pseudomallei , genomic epidemiology , Hainan , transmission and whole genome sequencing
Funding
This study was supported by the:
  • Hainan Provincial Department of Science and Technology (Award 817398)
    • Principle Award Recipient: ChenHai
  • Ministry of Science and Technology of the People's Republic of China (Award 2018ZX10714-002)
    • Principle Award Recipient: CuiYujun
  • Ministry of Science and Technology of the People's Republic of China (Award 2018ZX10101003)
    • Principle Award Recipient: CuiYujun
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2021-11-11
2024-04-29
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References

  1. Wiersinga W, van der Poll T, White N, Day N, Peacock S. Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei . Nat Rev Microbiol 2006; 4:272–282 [View Article] [PubMed]
     [Google Scholar]
  2. White NJ, Chaowagul W, Wuthiekanun V, Dance DAB, Wattanagoon Y. Halving of mortality of severe melioidosis by ceftazidime. The Lancet 1989; 2:697–701 [View Article]
     [Google Scholar]
  3. Lipsitz R, Garges S, Aurigemma R, Baccam P, Blaney DD et al. Workshop on treatment of and postexposure prophylaxis for Burkholderia pseudomallei and B. mallei infection, 2010. Emerging Infectious Diseases, Article 2012; 18:
     [Google Scholar]
  4. Limmathurotsakul D, Golding N, Dance DAB, Messina JP, Pigott DM. Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nat Microbiol 2016; 1:15008 [View Article] [PubMed]
     [Google Scholar]
  5. Talon D, Cailleaux V, Thouverez M, Michel-Briand Y. Discriminatory power and usefulness of pulsed-field gel electrophoresis in epidemiological studies of Pseudomonas aeruginosa . J Hosp Infect 1996; 32:135–145 [View Article] [PubMed]
     [Google Scholar]
  6. Inglis TJ, Garrow SC, Adams C, Henderson M, Mayo M. Acute melioidosis outbreak in Western Australia. Epidemiol Infect 1999; 123:437–443 [View Article] [PubMed]
     [Google Scholar]
  7. Chua KH, See KH, Thong KL, Puthucheary SD. DNA fingerprinting of human isolates of Burkholderia pseudomallei from different geographical regions of Malaysia. Trop Biomed 2010; 27:517–524 [PubMed]
     [Google Scholar]
  8. Azura MN, Norazah A, Kamel AG, Zorin SA. DNA fingerprinting of septicemic and localized Burkholderia pseudomallei isolates from Malaysian patients. Southeast Asian J Trop Med Public Health 2011; 42:114–121 [PubMed]
     [Google Scholar]
  9. Currie BJ, Haslem A, Pearson T, Hornstra H, Leadem B. Identification of Melioidosis outbreak by multilocus variable number tandem repeat analysis. Emerging Infect Dis 2009; 15:169–174 [View Article]
     [Google Scholar]
  10. Rao C, Hu Z, Chen J, Tang M, Li Q. Molecular epidemiology and antibiotic resistance of Burkholderia pseudomallei isolates from Hainan, China: A STROBE compliant observational study. Medicine (Baltimore) 2019; 98:e14461 [View Article] [PubMed]
     [Google Scholar]
  11. Zhu X, Chen H, Li S, Wang LC, Liu ZG. Molecular characteristics of Burkholderia pseudomallei collected from humans in Hainan, China. Front Microbiol 2020; 11:
     [Google Scholar]
  12. Sarovich DS, Garin B, De Smet B, Kaestli M, Mayo M. Phylogenomic analysis reveals an asian origin for African Burkholderia pseudomallei and further supports melioidosis endemicity in Africa. mSphere 2016; 1:e00089-15 [View Article] [PubMed]
     [Google Scholar]
  13. Maiden MCJ, Bygraves JA, Feil E, Morelli G, Russell JE. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 1998; 95:3140–3145 [View Article] [PubMed]
     [Google Scholar]
  14. Pearson T, Giffard P, Beckstrom-Sternberg S, Auerbach R, Hornstra H. Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer. BMC Biol 2009; 7:78 [View Article] [PubMed]
     [Google Scholar]
  15. Engelthaler DM, Bowers J, Schupp JA, Pearson T, Ginther J et al. Molecular investigations of a locally acquired case of melioidosis in Southern AZ, USA. PLoS Negl Trop Dis 2011; 5:e1347 [View Article]
     [Google Scholar]
  16. 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 [View Article] [PubMed]
     [Google Scholar]
  17. Chewapreecha C, Holden MT, Vehkala M, Valimaki N, Yang Z. Global and regional dissemination and evolution of Burkholderia pseudomallei . Nat Microbiol 2017; 2:16263 [View Article] [PubMed]
     [Google Scholar]
  18. Yanagida T, Carod J-F, Sako Y, Nakao M, Hoberg EP et al. Genetics of the pig tapeworm in Madagascar reveal a history of human dispersal and colonization. PLoS One 2014; 9:e109002 [View Article]
     [Google Scholar]
  19. Choy JL, Mayo M, Janmaat A, Currie BJ. Animal melioidosis in Australia; 2000; 74153–158
  20. Hampton V. Melioidosis in birds and Burkholderia pseudomallei dispersal, Australia. Emerging Infect Dis 2011; 17:1310–1312 [View Article]
     [Google Scholar]
  21. Price EP, Currie BJ, Sarovich DS. Genomic insights into the melioidosis pathogen, Burkholderia pseudomallei . Curr Trop Med Rep 2017; 4:95–102 [View Article]
     [Google Scholar]
  22. Zheng X, Xia Q, Xia L, Li W. Endemic melioidosis in Southern China: Past and Present. Trop Med Infect Dis 2019; 4:E39 [View Article] [PubMed]
     [Google Scholar]
  23. Li L, Lu Z, Han O. Epidemiology of melioidosis in China. Zhonghua Liu Xing Bing Xue Za Zhi 1994; 15:292–295 [PubMed]
     [Google Scholar]
  24. Fang Y, Zhu P, Li Q, Chen H, Li Y. Multilocus sequence typing of 102 Burkholderia pseudomallei strains isolated from China. Epidemiol Infect 2016; 144:1917–1923 [View Article] [PubMed]
     [Google Scholar]
  25. Fang Y, Hu Z, Chen H, Gu J, Hu H et al. Multilocus sequencing-based evolutionary analysis of 52 strains of Burkholderia pseudomallei in Hainan, China. Epidemiol Infect 20181–6
     [Google Scholar]
  26. Luo R, Liu B, Xie Y, Li Z, Huang W. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 2012; 1:18 [View Article] [PubMed]
     [Google Scholar]
  27. Cui Y, Yang X, Didelot X, Guo C, Li D. Epidemic Clones, Oceanic Gene Pools, and Eco-LD in the Free Living Marine Pathogen Vibrio parahaemolyticus . Mol Biol Evol 2015; 32:1396–1410 [View Article] [PubMed]
     [Google Scholar]
  28. Yang C, Zhang X, Fan H, Li Y, Hu Q. Genetic diversity, virulence factors and farm-to-table spread pattern of Vibrio parahaemolyticus food-associated isolates. Food Microbiol 2019; 84:103270 [View Article] [PubMed]
     [Google Scholar]
  29. Delcher AL, Salzberg SL, Phillippy AM. Using MUMmer to identify similar regions in large sequence sets. Current Protocs in Bioinformatics 2003; 10:10
     [Google Scholar]
  30. Li R, Yu C, Li Y, Lam TW, Yiu SM. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009; 25:1966–1967 [View Article] [PubMed]
     [Google Scholar]
  31. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999; 27:573–580 [View Article] [PubMed]
     [Google Scholar]
  32. 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]
  33. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–245 [View Article] [PubMed]
     [Google Scholar]
  34. Corander J, Marttinen P, Sirén J, Tang J. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 2008; 9:539 [View Article]
     [Google Scholar]
  35. Cheng L, Connor TR, Siren J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol 2013; 30:1224–1228 [View Article] [PubMed]
     [Google Scholar]
  36. 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. Nuclc Acids Research 2015e15
     [Google Scholar]
  37. Croucher NJ, Finkelstein JA, Pelton SI, Mitchell PK, Lee GM. Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet 2013; 45:656 [View Article] [PubMed]
     [Google Scholar]
  38. Assefa S, Keane TM, Otto TD, Newbold C, Berriman M. ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 2009; 25:1968–1969 [View Article] [PubMed]
     [Google Scholar]
  39. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG. ACT: the Artemis Comparison Tool. Bioinformatics 2005; 21:3422–3423 [View Article] [PubMed]
     [Google Scholar]
  40. Kozlov AM, Diego D, Tomáš F, Benoit M, Alexandros S. RAxML-NG: A fast, scalable, and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 201921
     [Google Scholar]
  41. Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol 2016; 2:16185 [View Article] [PubMed]
     [Google Scholar]
  42. Holt KE, McAdam P, Thai PVK, Thuong NTT, DTM H. Frequent transmission of the Mycobacterium tuberculosis Beijing lineage and positive selection for the EsxW Beijing variant in Vietnam. Nat Genet 2018; 50:849–856 [View Article] [PubMed]
     [Google Scholar]
  43. Bollback JP. SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 2006; 7:88 [View Article] [PubMed]
     [Google Scholar]
  44. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 2012; 3:217–223 [View Article]
     [Google Scholar]
  45. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2019; 47:D687–D692 [View Article] [PubMed]
     [Google Scholar]
  46. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
     [Google Scholar]
  47. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
     [Google Scholar]
  48. Wang H, Yang C, Sun Z, Zheng W, Zhang W et al. Genomic epidemiology of Vibrio cholerae reveals the regional and global spread of two epidemic non-toxigenic lineages. PLoS Negl Trop Dis 2020; 14:e0008046
     [Google Scholar]
  49. Wang XM, Zheng X, Wu H, Zhou XJ, Kuang HH. Multilocus sequence typing of clinical isolates of Burkholderia pseudomallei collected in Hainan, a tropical Island of Southern China. Am J Trop Med Hyg 2016; 95:760–764 [View Article] [PubMed]
     [Google Scholar]
  50. Balder R, Lipski S, Lazarus JJ, Grose W, Wooten RM et al. Identification of Burkholderia mallei and Burkholderia pseudomallei adhesins for human respiratory epithelial cells; 2010; 10250
  51. Andrea J, Dowling A. genome-wide analysis reveals loci encoding anti-macrophage factors in the human pathogen Burkholderia pseudomallei K96243. PLoS One 2010
     [Google Scholar]
  52. Schweizer HP. Mechanisms of antibiotic resistance in Burkholderia pseudomallei: implications for treatment of melioidosis. Future Microbiol 2012; 7:1389–1399 [View Article] [PubMed]
     [Google Scholar]
  53. Sarovich DS, Webb JR, Pitman MC, Viberg LT, Mayo M. Raising the stakes: loss of efflux pump regulation decreases meropenem susceptibility in Burkholderia pseudomallei . Clin Infect Dis 2018; 67:243–250 [View Article] [PubMed]
     [Google Scholar]
  54. Trunck LA, Propst KL, Wuthiekanun V, Tuanyok A, Beckstrom-Sternberg SM. Molecular basis of rare aminoglycoside susceptibility and pathogenesis of Burkholderia pseudomallei clinical isolates from Thailand. PLoS Negl Trop Dis 2009; 3:e519 [View Article] [PubMed]
     [Google Scholar]
  55. Madden DE, Webb JR, Steinig EJ, Currie BJ, Price EP. Taking the next-gen step: Comprehensive antimicrobial resistance detection from Burkholderia pseudomallei. EBioMedicine 2021; 63:103152 [View Article] [PubMed]
     [Google Scholar]
  56. Keith KE, Oyston PC, Crossett B, Fairweather NF, Brown KA. Functional Characterization of OXA-57, a Class D β-Lactamase from Burkholderia pseudomallei . Antimicrob Agents Chemother 2005; 49:1639–1641 [View Article] [PubMed]
     [Google Scholar]
  57. Sarovich DS, Price EP, Von Schulze AT, Cook JM, Mayo M et al. Characterization of ceftazidime resistance mechanisms in clinical isolates of Burkholderia pseudomallei from Australia. PLoS One 2012; 7:e30789 [View Article]
     [Google Scholar]
  58. Sarovich DS, Price EP, Limmathurotsakul D, Cook JM, Von Schulze AT. Development of ceftazidime resistance in an acute Burkholderia pseudomallei infection. Infect Drug Resist 2012; 5:129–132 [View Article] [PubMed]
     [Google Scholar]
  59. Rholl DA, Papp-Wallace KM, Tomaras AP, Vasil ML, Bonomo RA. Molecular investigations of PenA-mediated β-lactam resistance in Burkholderia pseudomallei . Front Microbiol 2011; 2:139 [View Article] [PubMed]
     [Google Scholar]
  60. Chantratita N, Rholl DA, Sim B, Wuthiekanun V, Limmathurotsakul D. Antimicrobial resistance to ceftazidime involving loss of penicillin-binding protein 3 in Burkholderia pseudomallei . Proc Natl Acad Sci U S A 2011; 108:17165–17170 [View Article] [PubMed]
     [Google Scholar]
  61. Bugrysheva JV, Sue D, Gee JE, Elrod MG, Hoffmaster AR. Antibiotic resistance markers in Burkholderia pseudomallei strain Bp1651 identified by genome sequence analysis. Antimicrob Agents Chemother 2017; 61:e00010-17 [View Article] [PubMed]
     [Google Scholar]
  62. Aziz A, Currie BJ, Mayo M, Sarovich DS, Price EP. Comparative genomics confirms a rare melioidosis human-to-human transmission event and reveals incorrect phylogenomic reconstruction due to polyclonality. Microb Genom 2020; 6: [View Article] [PubMed]
     [Google Scholar]
  63. Limmathurotsakul D, Kanoksil M, Wuthiekanun V, Kitphati R, deStavola B et al. Activities of daily living associated with acquisition of melioidosis in northeast Thailand: a matched case-control study. PLoS Negl Trop Dis 2013; 7:e2072
     [Google Scholar]
  64. Limmathurotsakul D, Wongsuvan G, Aanensen D, Ngamwilai S, Saiprom N. Melioidosis caused by Burkholderia pseudomallei in drinking water, Thailand, 2012. Emerg Infect Dis 2014; 20:265–268 [View Article] [PubMed]
     [Google Scholar]
  65. Chen PS, Chen YS, Lin HH, Liu PJ, Ni WF. Airborne transmission of melioidosis to humans from environmental aerosols contaminated with B. PLoS Negl Trop Dis 2015; 9:e0003834 [View Article] [PubMed]
     [Google Scholar]
  66. Cheng AC, Jacups SP, Gal D, Mayo M, Currie BJ. Extreme weather events and environmental contamination are associated with case-clusters of melioidosis in the Northern Territory of Australia. Int J Epidemiol 2006; 35:323–329 [View Article] [PubMed]
     [Google Scholar]
  67. Dong S, Wu L, Long F, Wu Q, Liu X. The prevalence and distribution of Burkholderia pseudomallei in rice paddy within Hainan, China. Acta Trop 2018; 187:165–168 [View Article] [PubMed]
     [Google Scholar]
  68. Pumirat P, Cuccui J, Stabler RA, Stevens JM, Muangsombut V. Global transcriptional profiling of Burkholderia pseudomallei under salt stress reveals differential effects on the Bsa type III secretion system. BMC Microbiol 2010; 10:171 [View Article] [PubMed]
     [Google Scholar]
  69. Stopnisek N, Bodenhausen N, Frey B, Fierer N, Eberl L. Genus-wide acid tolerance accounts for the biogeographical distribution of soil Burkholderia populations. Environ Microbiol 2014; 16:1503–1512 [View Article] [PubMed]
     [Google Scholar]
  70. Chen YL, Yen YC, Yang CY, Lee MS, CK H. The concentrations of ambient Burkholderia pseudomallei during typhoon season in endemic area of melioidosis in Taiwan. PLoS Negl Trop Dis 2014; 8:e2877 [View Article] [PubMed]
     [Google Scholar]
  71. Liu X, Pang L, Sim SH, Goh KT, Ravikumar S. Association of melioidosis incidence with rainfall and humidity, Singapore, 2003-2012. Emerg Infect Dis 2015; 21:159–162 [View Article] [PubMed]
     [Google Scholar]
  72. Baker A, Mayo M, Owens L, Burgess G, Norton R et al. Biogeography of Burkholderia pseudomallei in the torres strait Islands of Northern Australia. J Clin Microbiol 2013; 51:2520–2525 [View Article]
     [Google Scholar]
  73. Baker AL, Pearson T, Sahl JW, Hepp C, Price EP et al. Burkholderia pseudomallei distribution in Australasia is linked to paleogeographic and anthropogenic history. PLoS ONE 2018; 13:11
     [Google Scholar]
  74. Rao C, Hu Z, Chen J, Tang M, Chen H. Molecular epidemiology and antibiotic resistance of Burkholderia pseudomallei isolates from Hainan, China: A STROBE compliant observational study. Medicine (Baltimore) 2019; 98:e14461 [View Article] [PubMed]
     [Google Scholar]
  75. Ambler RP, Coulson AF, Frère JM, Ghuysen JM, Joris B. A standard numbering scheme for the class A beta-lactamases. Biochem J 1991; 276:269–270 [View Article] [PubMed]
     [Google Scholar]
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Genetic diversity and transmission patterns of Burkholderia pseudomallei on Hainan island, China, revealed by a population genomics analysis
M Gen 7, 000659 (2021); https://doi.org/10.1099/mgen.0.000659
/content/journal/mgen/10.1099/mgen.0.000659
/content/journal/mgen/10.1099/mgen.0.000659
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