1921
Volume 101, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

is a selective agent that causes septic melioidosis and exhibits a broad range of lethal doses in animals. Host cellular virulence and phagocytic resistance are pathologic keys of . We first proposed as the host cellular virulence model to mimic bacterial virulence against mammals and second established the resistance of to predation by as the phagocytosis model. The saprophytic sepsis–causing sp. (, , , and ) exhibited different virulence patterns in both simple models, but was the most toxic. Using both models, attenuated isolates of were selected from a transposon-mutant library and a panel of environmental isolates and reconfirmed by in vitro mouse peritoneal exudate cell association and invasion assays. The distinct pathological patterns of melioidosis were inducted by different selected isolates. Fatal melioidosis was induced by the isolates with high virulence in both simple models within 4–5 day, whereas the low-virulence isolates resulted in prolonged survival greater than 30 day. Infection with the isolates having high resistance to predation but a low killing effect led to 83% of mice with neurologic melioidosis. By contrast, infection with the isolates having low resistance to predation but high killing effect led to 20% cases with inflammation in the salivary glands. Our results indicated that individual isolates selected from simple biological models contribute differently to disease progression and/or tissue tropism.

Loading

Article metrics loading...

The graphs shown below represent data from March 2017
/content/journals/10.4269/ajtmh.19-0052
2019-08-05
2020-09-23
Loading full text...

Full text loading...

/deliver/fulltext/14761645/101/4/tpmd190052.html?itemId=/content/journals/10.4269/ajtmh.19-0052&mimeType=html&fmt=ahah

References

  1. Cheng AC, Currie BJ, 2005. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383416.
    [Google Scholar]
  2. Dance DA, 2000. Ecology of Burkholderia pseudomallei and the interactions between environmental Burkholderia spp. and human-animal hosts. Acta Trop 74: 159168.
    [Google Scholar]
  3. Chen PS, Chen YS, Lin HH, Liu PJ, Ni WF, Hsueh PT, Liang SH, Chen C, Chen YL, 2015. Airborne transmission of melioidosis to humans from environmental aerosols contaminated with B. pseudomallei. PLoS Negl Trop Dis 9: e0003834.
    [Google Scholar]
  4. Currie BJ, Ward L, Cheng AC, 2010. The epidemiology and clinical spectrum of melioidosis: 540 cases from the 20 year Darwin prospective study. PLoS Negl Trop Dis 4: e900.
    [Google Scholar]
  5. Ulett GC et al., 2001. Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect 3: 621631.
    [Google Scholar]
  6. Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ, 2006. Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4: 272282.
    [Google Scholar]
  7. Chen YS, Shieh WJ, Goldsmith CS, Metcalfe MG, Greer PW, Zaki SR, Chang HH, Chan H, Chen YL, 2014. Alteration of the phenotypic and pathogenic patterns of Burkholderia pseudomallei that persist in a soil environment. Am J Trop Med Hyg 90: 469479.
    [Google Scholar]
  8. Vora SK, 2002. Sherlock Holmes and a biological weapon. J R Soc Med 95: 101103.
    [Google Scholar]
  9. Lee SH, Ooi SK, Mahadi NM, Tan MW, Nathan S, 2011. Complete killing of Caenorhabditis elegans by Burkholderia pseudomallei is dependent on prolonged direct association with the viable pathogen. PLoS One 6: e16707.
    [Google Scholar]
  10. Hasselbring BM, Patel MK, Schell MA, 2011. Dictyostelium discoideum as a model system for identification of Burkholderia pseudomallei virulence factors. Infect Immun 79: 20792088.
    [Google Scholar]
  11. Stone JK, DeShazer D, Brett PJ, Burtnick MN, 2014. Melioidosis: molecular aspects of pathogenesis. Expert Rev Anti Infect Ther 12: 14871499.
    [Google Scholar]
  12. O'Quinn AL, Wiegand EM, Jeddeloh JA, 2001. Burkholderia pseudomallei kills the nematode Caenorhabditis elegans using an endotoxin-mediated paralysis. Cell Microbiol 3: 381393.
    [Google Scholar]
  13. Ooi SK, Lim TY, Lee SH, Nathan S, 2012. Burkholderia pseudomallei kills Caenorhabditis elegans through virulence mechanisms distinct from intestinal lumen colonization. Virulence 3: 485496.
    [Google Scholar]
  14. Chen YS, Lin HH, Hsueh PT, Ni WF, Liu PJ, Chen PS, Chang HH, Sun DS, Chen YL, 2016. Involvement of L-selectin expression in Burkholderia pseudomallei-infected monocytes invading the brain during murine melioidosis. Virulence 8: 751766.
    [Google Scholar]
  15. Hsueh PT, Lin HH, Liu CL, Ni WF, Chen YL, Chen YS, 2018. Burkholderia pseudomallei-loaded cells act as a Trojan horse to invade the brain during endotoxemia. Sci Rep 8: 13632.
    [Google Scholar]
  16. Jones AL, Beveridge TJ, Woods DE, 1996. Intracellular survival of Burkholderia pseudomallei. Infect Immun 64: 782790.
    [Google Scholar]
  17. Chen YS, Lin HH, Hsueh PT, Liu PJ, Ni WF, Chung WC, Lin CP, Chen YL, 2015. Whole-genome sequence of an epidemic strain of Burkholderia pseudomallei vgh07 in Taiwan. Genome Announc 3: e00345-15.
    [Google Scholar]
  18. Hsueh PT, Liu JK, Chen YL, Liu PJ, Ni WF, Chen YS, Wu KM, Lin HH, 2015. Genomic sequence of Burkholderia multivorans NKI379, a soil bacterium that inhibits the growth of Burkholderia pseudomallei. Genome Announc 3: e01294-15.
    [Google Scholar]
  19. Hsueh PT, Liu CL, Wang HH, Ni WF, Chen YL, Liu JK, 2016. A comparison of the immunological potency of Burkholderia lipopolysaccharides in endotoxemic BALB/c mice. Microbiol Immunol 60: 725739.
    [Google Scholar]
  20. Yu Y et al., 2006. Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis. BMC Microbiol 6: 46.
    [Google Scholar]
  21. Chen YS, Lin HH, Liu PJ, Tsai HY, Hsueh PT, Liu HY, Chen YL, 2011. Use of 3-hydroxy fatty acid concentrations in a murine air pouch infection model as a surrogate marker for LPS activity: a feasibility study using environmental Burkholderia cenocepacia isolates. J Microbiol Methods 87: 368374.
    [Google Scholar]
  22. Pande A, Veale TC, Grove A, 2018. Gene regulation by redox-sensitive Burkholderia thailandensis OhrR and its role in bacterial killing of Caenorhabditis elegans. Infect Immun 86: e00322-18.
    [Google Scholar]
  23. Wong YC, Abd El Ghany M, Ghazzali RNM, Yap SJ, Hoh CC, Pain A, Nathan S, 2018. Genetic determinants associated with in vivo survival of Burkholderia cenocepacia in the Caenorhabditis elegans model. Front Microbiol 9: 1118.
    [Google Scholar]
  24. Cooper VS, Carlson WA, Lipuma JJ, 2009. Susceptibility of Caenorhabditis elegans to Burkholderia infection depends on prior diet and secreted bacterial attractants. PLoS One 4: e7961.
    [Google Scholar]
  25. Eng SA, Nathan S, 2015. Curcumin rescues Caenorhabditis elegans from a Burkholderia pseudomallei infection. Front Microbiol 6: 290.
    [Google Scholar]
  26. Aubert DF, Flannagan RS, Valvano MA, 2008. A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76: 19791991.
    [Google Scholar]
  27. Chen PL, Chen YW, Ou CC, Lee TM, Wu CJ, Ko WC, Chen CS, 2016. A disease model of muscle necrosis caused by Aeromonas dhakensis infection in Caenorhabditis elegans. Front Microbiol 7: 2058.
    [Google Scholar]
  28. Fey P, Kowal AS, Gaudet P, Pilcher KE, Chisholm RL, 2007. Protocols for growth and development of Dictyostelium discoideum. Nat Protoc 2: 13071316.
    [Google Scholar]
  29. Novem V et al., 2009. Structural and biological diversity of lipopolysaccharides from Burkholderia pseudomallei and Burkholderia thailandensis. Clin Vaccin Immunol 16: 14201428.
    [Google Scholar]
  30. Lin HH, Chen YS, Li YC, Tseng IL, Hsieh TH, Buu LM, Chen YL, 2011. Burkholderia multivorans acts as an antagonist against the growth of Burkholderia pseudomallei in soil. Microbiol Immunol 55: 616624.
    [Google Scholar]
  31. Hsueh PT, Chen YS, Lin HH, Liu PJ, Ni WF, Liu MC, Chen YL, 2015. Comparison of whole-genome sequences from two colony morphovars of Burkholderia pseudomallei. Genome Announc 3: e01194-15.
    [Google Scholar]
  32. Chen YS, Lin HH, Hung CC, Mu JJ, Hsiao YS, Chen YL, 2009. Phenotypic characteristics and pathogenic ability across distinct morphotypes of Burkholderia pseudomallei DT. Microbiol Immunol 53: 184189.
    [Google Scholar]
  33. Wiersinga WJ, Virk HS, Torres AG, Currie BJ, Peacock SJ, Dance DAB, Limmathurotsakul D, 2018. Melioidosis. Nat Rev Dis Primers 4: 17107.
    [Google Scholar]
  34. Loutet SA, Valvano MA, 2010. A decade of Burkholderia cenocepacia virulence determinant research. Infect Immun 78: 40881400.
    [Google Scholar]
  35. Glass MB, Gee JE, Steigerwalt AG, Cavuoti D, Barton T, Hardy RD, Godoy D, Spratt BG, Clark TA, Wilkins PP, 2006. Pneumonia and septicemia caused by Burkholderia thailandensis in the United States. J Clin Microbiol 44: 46014604.
    [Google Scholar]
  36. Rozsa L, Apari P, Sulyok M, Tappe D, Bodo I, Hardi R, Müller V, 2017. The evolutionary logic of sepsis. Infect Genet Evol 55: 135141.
    [Google Scholar]
  37. Eberl L, 2006. Quorum sensing in the genus Burkholderia. Int J Med Microbiol 296: 103110.
    [Google Scholar]
  38. Buroni S, Scoffone VC, Fumagalli M, Makarov V, Cagnone M, Trespidi G, De Rossi E, Forneris F, Riccardi G, Chiarelli LR, 2018. Investigating the mechanism of action of diketopiperazines inhibitors of the Burkholderia cenocepacia quorum sensing synthase CepI: a site-directed mutagenesis study. Front Pharmacol 9: 836.
    [Google Scholar]
  39. Klaus JR et al., 2018. Malleilactone is a Burkholderia pseudomallei virulence factor regulated by antibiotics and quorum sensing. J Bacteriol 200: e00008-18.
    [Google Scholar]
  40. Chua KL, Chan YY, Gan YH, 2003. Flagella are virulence determinants of Burkholderia pseudomallei. Infect Immun 71: 16221629.
    [Google Scholar]
  41. Valvano MA, 2015. Intracellular survival of Burkholderia cepacia complex in phagocytic cells. Can J Microbiol 61: 607615.
    [Google Scholar]
  42. Whiteley L, Haug M, Klein K, Willmann M, Bohn E, Chiantia S, Schwarz S, 2017. Cholesterol and host cell surface proteins contribute to cell-cell fusion induced by the Burkholderia type VI secretion system 5. PLoS One 12: e0185715.
    [Google Scholar]
  43. Whiteley L et al., 2017. Entry, intracellular survival, and multinucleated-giant-cell-forming activity of Burkholderia pseudomallei in human primary phagocytic and nonphagocytic cells. Infect Immun 85: e00468-17.
    [Google Scholar]
  44. Liu PJ, Chen YS, Lin HH, Ni WF, Hsieh TH, Chen HT, Chen YL, 2013. Induction of mouse melioidosis with meningitis by CD11b+ phagocytic cells harboring intracellular B. pseudomallei as a Trojan horse. PLoS Negl Trop Dis 7: e2363.
    [Google Scholar]
  45. Pukatzki S, Kessin RH, Mekalanos JJ, 2002. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Natl Acad Sci USA 99: 31593164.
    [Google Scholar]
  46. Willcocks SJ, Denman CC, Atkins HS, Wren BW, 2016. Intracellular replication of the well-armed pathogen Burkholderia pseudomallei. Curr Opin Microbiol 29: 94103.
    [Google Scholar]
  47. Hsueh PT, Huang WT, Hsueh HK, Chen YL, Chen YS, 2018. Transmission modes of melioidosis in Taiwan. Trop Med Infect Dis 3: E26.
    [Google Scholar]
  48. Zueter AR, Rahman ZA, Abumarzouq M, Harun A, 2018. Multilocus sequence types of clinical Burkholderia pseudomallei isolates from peninsular Malaysia and their associations with disease outcomes. BMC Infect Dis 18: 5.
    [Google Scholar]
  49. Vesaratchavest M et al., 2006. Nonrandom distribution of Burkholderia pseudomallei clones in relation to geographical location and virulence. J Clin Microbiol 44: 25532557.
    [Google Scholar]
  50. Shea AA et al., 2017. Two stable variants of Burkholderia pseudomallei strain MSHR5848 express broadly divergent in vitro phenotypes associated with their virulence differences. PLoS One 12: e0171363.
    [Google Scholar]
  51. Owen SJ, Batzloff M, Chehrehasa F, Meedeniya A, Casart Y, Logue CA, Hirst RG, Peak IR, Mackay-Sim A, Beacham IR, 2009. Nasal-associated lymphoid tissue and olfactory epithelium as portals of entry for Burkholderia pseudomallei in murine melioidosis. J Infect Dis 199: 17611770.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.19-0052
Loading
/content/journals/10.4269/ajtmh.19-0052
Loading

Data & Media loading...

Supplemental Materials

  • Received : 16 Jan 2019
  • Accepted : 15 May 2019
  • Published online : 05 Aug 2019
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