• 1.

    White NJ, 2003. Melioidosis. Lancet 361: 17151722.

  • 2.

    Cheng AC, Currie BJ, 2005. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383416.

  • 3.

    Wiersinga WJ, Currie BJ, Peacock SJ, 2012. Melioidosis. N Engl J Med 367: 10351044.

  • 4.

    Dance DA, Smith MD, Aucken HM, Pitt TL, 1999. Imported melioidosis in England and Wales. Lancet 353: 208.

  • 5.

    Visca P, Cazzola G, Petrucca A, Braggion C, 2001. Travel-associated Burkholderia pseudomallei infection (melioidosis) in a patient with cystic fibrosis: a case report. Clin Infect Dis 32: E15E16.

    • Search Google Scholar
    • Export Citation
  • 6.

    Rossi B, Epelboin L, Jaureguiberry S, Lecso M, Roos-Weil D, Gabarre J, Grenier PA, Bricaire F, Caumes E, 2013. Melioidosis and hairy cell leukemia in 2 travelers returning from Thailand. Emerg Infect Dis 19: 503505.

    • Search Google Scholar
    • Export Citation
  • 7.

    Limmathurotsakul D, Wongratanacheewin S, Teerawattanasook N, Wongsuvan G, Chaisuksant S, Chetchotisakd P, Chaowagul W, Day NP, Peacock SJ, 2010. Increasing incidence of human melioidosis in northeast Thailand. Am J Trop Med Hyg 82: 11131117.

    • Search Google Scholar
    • Export Citation
  • 8.

    Chen YL, Yen YC, Yang CY, Lee MS, Ho CK, Mena KD, Wang PY, Chen PS, 2014. The concentrations of ambient Burkholderia pseudomallei during typhoon season in endemic area of melioidosis in Taiwan. PLoS Negl Trop Dis 8: e2877.

    • Search Google Scholar
    • Export Citation
  • 9.

    Currie BJ, Jacups SP, 2003. Intensity of rainfall and severity of melioidosis, Australia. Emerg Infect Dis 9: 15381542.

  • 10.

    Meumann EM, Cheng AC, Ward L, Currie BJ, 2012. Clinical features and epidemiology of melioidosis pneumonia: results from a 21-year study and review of the literature. Clin Infect Dis 54: 362369.

    • Search Google Scholar
    • Export Citation
  • 11.

    Chen YS, Chen SC, Kao CM, Chen YL, 2003. Effects of soil pH, temperature and water content on the growth of Burkholderia pseudomallei. Folia Microbiol (Praha) 48: 253256.

    • Search Google Scholar
    • Export Citation
  • 12.

    Inglis TJ, Sagripanti JL, 2006. Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl Environ Microbiol 72: 68656875.

    • Search Google Scholar
    • Export Citation
  • 13.

    Thomas AD, Forbes-Faulkner JC, 1981. Persistence of Pseudomonas pseudomallei in soil. Aust Vet J 57: 535536.

  • 14.

    Pumpuang A, Chantratita N, Wikraiphat C, Saiprom N, Day NP, Peacock SJ, Wuthiekanun V, 2011. Survival of Burkholderia pseudomallei in distilled water for 16 years. Trans R Soc Trop Med Hyg 105: 598600.

    • Search Google Scholar
    • Export Citation
  • 15.

    Tong S, Yang S, Lu Z, He W, 1996. Laboratory investigation of ecological factors influencing the environmental presence of Burkholderia pseudomallei. Microbiol Immunol 40: 451453.

    • Search Google Scholar
    • Export Citation
  • 16.

    Wang-Ngarm S, Chareonsudjai S, Chareonsudjai P, 2014. Physicochemical factors affecting the growth of Burkholderia pseudomallei in soil microcosm. Am J Trop Med Hyg 90: 480485.

    • Search Google Scholar
    • Export Citation
  • 17.

    Larsen E, Smith JJ, Norton R, Corkeron M, 2013. Survival, sublethal injury, and recovery of environmental Burkholderia pseudomallei in soil subjected to desiccation. Appl Environ Microbiol 79: 24242427.

    • Search Google Scholar
    • Export Citation
  • 18.

    Draper AD, Mayo M, Harrington G, Karp D, Yinfoo D, Ward L, Haslem A, Currie BJ, Kaestli M, 2010. Association of the melioidosis agent Burkholderia pseudomallei with water parameters in rural water supplies in northern Australia. Appl Environ Microbiol 76: 53055307.

    • Search Google Scholar
    • Export Citation
  • 19.

    Kaestli M, Mayo M, Harrington G, Watt F, Hill J, Gal D, Currie BJ, 2007. Sensitive and specific molecular detection of Burkholderia pseudomallei, the causative agent of melioidosis, in the soil of tropical northern Australia. Appl Environ Microbiol 73: 68916897.

    • Search Google Scholar
    • Export Citation
  • 20.

    Kamjumphol W, Chareonsudjai S, Chareonsudjai P, Wongratanacheewin S, Taweechaisupapong S, 2013. Environmental factors affecting Burkholderia pseudomallei biofilm formation. Southeast Asian J Trop Med Public Health 44: 7281.

    • Search Google Scholar
    • Export Citation
  • 21.

    Pumirat P, Cuccui J, Stabler RA, Stevens JM, Muangsombut V, Singsuksawat E, Stevens MP, Wren BW, Korbsrisate S, 2010. Global transcriptional profiling of Burkholderia pseudomallei under salt stress reveals differential effects on the Bsa type III secretion system. BMC Microbiol 10: 171.

    • Search Google Scholar
    • Export Citation
  • 22.

    Suebrasri T, Wang-ngarm S, Chareonsudjai P, Sermswan RW, Chareonsudjai S, 2013. Seasonal variation of soil environmental characteristics affect the presence of Burkholderia pseudomallei in Khon Kaen, Thailand. Afr J Microbiol Res 7: 19401945.

    • Search Google Scholar
    • Export Citation
  • 23.

    Chen S-Y, Jane W-N, Chen Y-S, Wong H-C, 2009. Morphological changes of Vibrio parahaemolyticus under cold and starvation stresses. Int J Food Microbiol 129: 157165.

    • Search Google Scholar
    • Export Citation
  • 24.

    Adams BL, Bates TC, Oliver JD, 2003. Survival of Helicobacter pylori in a natural freshwater environment. Appl Environ Microbiol 69: 74627466.

    • Search Google Scholar
    • Export Citation
  • 25.

    Robertson J, Levy A, Sagripanti JL, Inglis TJ, 2010. The survival of Burkholderia pseudomallei in liquid media. Am J Trop Med Hyg 82: 8894.

  • 26.

    Sermswan RW, Wongratanacheewin S, Trakulsomboon S, Thamlikitkul V, 2001. Ribotyping of Burkholderia pseudomallei from clinical and soil isolates in Thailand. Acta Trop 80: 237244.

    • Search Google Scholar
    • Export Citation
  • 27.

    Taweechaisupapong S, Kaewpa C, Arunyanart C, Kanla P, Homchampa P, Sirisinha S, Proungvitaya T, Wongratanacheewin S, 2005. Virulence of Burkholderia pseudomallei does not correlate with biofilm formation. Microb Pathog 39: 7785.

    • Search Google Scholar
    • Export Citation
  • 28.

    Trung TT, Hetzer A, Topfstedt E, Gohler A, Limmathurotsakul D, Wuthiekanun V, Peacock SJ, Steinmetz I, 2011. Improved culture-based detection and quantification of Burkholderia pseudomallei from soil. Trans R Soc Trop Med Hyg 105: 346351.

    • Search Google Scholar
    • Export Citation
  • 29.

    Sachidanandham R, Gin KY-H, 2009. A dormancy state in nonspore-forming bacteria. Appl Microbiol Biotechnol 81: 927941.

  • 30.

    Boulos L, Prevost M, Barbeau B, Coallier J, Desjardins R, 1999. LIVE/DEAD® BacLight: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J Microbiol Methods 37: 7786.

    • Search Google Scholar
    • Export Citation
  • 31.

    Berney M, Hammes F, Bosshard F, Weilenmann HU, Egli T, 2007. Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with flow cytometry. Appl Environ Microbiol 73: 32833290.

    • Search Google Scholar
    • Export Citation
  • 32.

    Palasatien S, Lertsirivorakul R, Royros P, Wongratanacheewin S, Sermswan RW, 2008. Soil physicochemical properties related to the presence of Burkholderia pseudomallei. Trans R Soc Trop Med Hyg 102 (Suppl 1): S5S9.

    • Search Google Scholar
    • Export Citation
  • 33.

    Kaestli M, Mayo M, Harrington G, Ward L, Watt F, Hill JV, Cheng AC, Currie BJ, 2009. Landscape changes influence the occurrence of the melioidosis bacterium Burkholderia pseudomallei in soil in northern Australia. PLoS Negl Trop Dis 3: e364.

    • Search Google Scholar
    • Export Citation
  • 34.

    Thanachit S, Suddhiprakarn A, Kheoruenromne I, Sindhusen P, Gilkes R, 2010. Micromorphological characteristic of soils on the Nam Phong and Khon Buri catenae, northeast Thailand. Thai Journal of Agricultural Science 43: 7190.

    • Search Google Scholar
    • Export Citation
  • 35.

    Weber KA, Achenbach LA, Coates JD, 2006. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4: 752764.

    • Search Google Scholar
    • Export Citation
  • 36.

    Meneghini R, 1997. Iron homeostasis, oxidative stress, and DNA damage. Free Radic Biol Med 23: 783792.

  • 37.

    Touati DL, 2000. Iron and oxidative stress in bacteria. Arch Biochem Biophys 373: 16.

  • 38.

    Sagripanti JL, Carrera M, Robertson J, Levy A, Inglis TJ, 2011. Size distribution and buoyant density of Burkholderia pseudomallei. Arch Microbiol 193: 6975.

    • Search Google Scholar
    • Export Citation
  • 39.

    Baker RM, Singleton FL, Hood MA, 1983. Effects of nutrient deprivation on Vibrio cholerae. Appl Environ Microbiol 46: 930940.

  • 40.

    Erlebach CE, Illmer P, Schinner F, 2000. Changes of cell size distribution during the batch culture of Arthrobacter strain PI/1-95. Antonie van Leeuwenhoek 77: 329335.

    • Search Google Scholar
    • Export Citation
  • 41.

    Thomas RJ, Davies C, Nunez A, Hibbs S, Eastaugh L, Harding S, Jordan J, Barnes K, Oyston P, Eley S, 2012. Particle-size dependent effects in the Balb/c murine model of inhalational melioidosis. Front Cell Infect Microbiol 2: 101.

    • Search Google Scholar
    • Export Citation
  • 42.

    Li L, Mendis N, Trigui H, Oliver JD, Faucher SP, 2014. The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol 5: 258.

    • Search Google Scholar
    • Export Citation
  • 43.

    Oliver JD, 2010. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34: 415425.

  • 44.

    Anuchin AM, Mulyukin AL, Suzina NE, Duda VI, El-Registan GI, Kaprelyants AS, 2009. Dormant forms of Mycobacterium smegmatis with distinct morphology. Microbiology 155: 10711079.

    • Search Google Scholar
    • Export Citation
  • 45.

    Weichart D, Kjelleberg S, 1996. Stress resistance and recovery potential of culturable and viable but nonculturable cells of Vibrio vulnificus. Microbiology 142: 845853.

    • Search Google Scholar
    • Export Citation
  • 46.

    Wong HC, Wang P, 2004. Induction of viable but nonculturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J Appl Microbiol 96: 359366.

    • Search Google Scholar
    • Export Citation
  • 47.

    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.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Morphological Alteration and Survival of Burkholderia pseudomallei in Soil Microcosms

View More View Less
  • Department of Microbiology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Department of Environmental Science, Faculty of Science, Khon Kaen University, Khon Kaen, Thailand; Biofilm Research Group, Department of Oral Diagnosis, Faculty of Dentistry, Khon Kaen University, Khon Kaen, Thailand; Melioidosis Research Center, Khon Kaen University, Khon Kaen, Thailand

The resilience of Burkholderia pseudomallei, the causative agent of melioidosis, was evaluated in control soil microcosms and in soil microcosms containing NaCl or FeSO4 at 30°C. Iron (Fe(II)) promoted the growth of B. pseudomallei during the 30-day observation, contrary to the presence of 1.5% and 3% NaCl. Scanning electron micrographs of B. pseudomallei in soil revealed their morphological alteration from rod to coccoid and the formation of microcolonies. The smallest B. pseudomallei cells were found in soil with 100 μM FeSO4 compared with in the control soil or soil with 0.6% NaCl (P < 0.05). The colony count on Ashdown's agar and bacterial viability assay using the LIVE/DEAD® BacLight stain combined with flow cytometry showed that B. pseudomallei remained culturable and viable in the control soil microcosms for at least 120 days. In contrast, soil with 1.5% NaCl affected their culturability at day 90 and their viability at day 120. Our results suggested that a low salinity and iron may influence the survival of B. pseudomallei and its ability to change from a rod-like to coccoid form. The morphological changes of B. pseudomallei cells may be advantageous for their persistence in the environment and may increase the risk of their transmission to humans.

Author Notes

* Address correspondence to Sorujsiri Chareonsudjai, Department of Microbiology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand 40002. E-mail: sorujsr@kku.ac.th

Financial support: This study was supported by the Higher Education Research Promotion and National Research University Project of Thailand and the Office of the Higher Education Commission through the Center of Excellence in Specific Health Problems in the Greater Mekong Sub-Region Cluster (SHeP-GMS), Khon Kaen University.

Authors' addresses: Watcharaporn Kamjumphol and Sorujsiri Chareonsudjai, Department of Microbiology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, E-mails: watchark48@gmail.com and sorujsr@kku.ac.th. Pisit Chareonsudjai, Department of Environmental Science, Khon Kaen University, Khon Kaen, Thailand, E-mail: pisit@kku.ac.th. Suwimol Taweechaisupapong, Department of Oral Diagnosis, Faculty of Dentistry, Khon Kaen University, Khon Kaen, Thailand, E-mail: suvi_taw@kku.ac.th.

Save