ProCite
RefWorks
Reference Manager
BibTeX
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Alteration of the Phenotypic and Pathogenic Patterns of Burkholderia pseudomallei that Persist in a Soil Environment
Yao-Shen Chen
Yao-Shen Chen
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Wun-Ju Shieh
Wun-Ju Shieh
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Cynthia S. Goldsmith
Cynthia S. Goldsmith
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Maureen G. Metcalfe
Maureen G. Metcalfe
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Patricia W. Greer
Patricia W. Greer
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Sherif R. Zaki
Sherif R. Zaki
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Hsin-Hou Chang
Hsin-Hou Chang
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Hao Chan
Hao Chan
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Ya-Lei Chen
Ya-Lei Chen
Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung; Taiwan/Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan; Infectious Diseases Pathology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia; Department of Molecular Biology and Human Genetics, Tzu-Chi University, Hualien, Taiwan; Institute of Medical Sciences, Tzu-Chi University, Hualien, Taiwan; Department of Biotechnology, National Kaohsiung Normal University, Kaoshiung, Taiwan
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Melioidosis is caused by the soil-borne pathogen Burkholderia pseudomallei. To investigate whether the distinct phenotypic and virulent characteristics result from environmental adaptations in the soil or from the host body, two pairs of isogenic strains were generated by passages in soil or mice. After cultivation in soil, the levels of 3-hydroxytetradecanoic acid, biofilm formation, flagellar expression, and ultrastructure were altered in the bacteria. Uniformly fatal melioidosis developed as a result of infection with mouse-derived strains; however, the survival rates of mice infected with soil-derived strains prolonged. After primary infection or reinfection with soil-derived strains, the mice developed a low degree of bacterial hepatitis and bacterial colonization in the liver and bone marrow compared with mice that were infected with isogenic or heterogenic mouse-derived strains. We suggest that specific phenotypic and pathogenic patterns can be induced through infection with B. pseudomallei that has been cultured in different (soil versus mouse) environments.
Author Notes
Financial support: This work was supported by grants NSC 99-2320-B-017-002-MY3, NSC99-2320-B-075B-001-MY3, VGHKS102-016, and VGHKS99-038.
Authors' addresses: Yao-Shen Chen, Division of Infectious Diseases, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan, Graduate Institute of Science Education and Environmental Education, National Kaohsiung Normal University, Kaohsiung, Taiwan, and Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan, E-mail: dan1001@ms31.hinet.net. Wun-Ju Shieh, Centers for Disease Control and Prevention, Infectious Diseases Pathology Branch, Atlanta, GA, E-mail: WShieh@cdc.gov. Cynthia S. Goldsmith, Maureen G. Metcalfe, Patricia W. Greer, and Sherif R. Zaki, Centers for Disease Control and Prevention, Infectious Disease and Pathology Activity, Atlanta, GA, E-mails: csg1@cdc.gov, gnf3@cdc.gov, pwg1@cdc.gov, and sxz1@cdc.gov. Hsin-Hou Chang and Hao Chan, Tzu-Chi University, Department of Molecular Biology and Human Genetics, Hualien, Taiwan, E-mail: hhchang@mail.tcu.edu.tw and b_pseudo@yahoo.com.tw. Ya-Lei Chen, National Kaohsiung Normal University, Biotechnology, Yenchao, Kaohsiung, Taiwan, E-mail: dan1001@ms31.hinet.net.
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-
1.
Cheng AC, Currie BJ, 2005. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383–416.
-
2.
Limmathurotsakul D, Kanoksil M, Wuthiekanun V, Kitphati R, deStavola B, Day NP, Peacock SJ, 2013. Activities of daily living associated with acquisition of melioidosis in northeast Thailand: a matched case-control study. PLoS Negl Trop Dis 7: e2072.
-
3.
Wuthiekanun V, Chierakul W, Langa S, Chaowagul W, Panpitpat C, Saipan P, Thoujaikong T, Day NP, Peacock SJ, 2006. Development of antibodies to Burkholderia pseudomallei during childhood in melioidosis-endemic northeast Thailand. Am J Trop Med Hyg 74: 1074–1075.
-
4.
Maharjan B, Chantratita N, Vesaratchavest M, Cheng A, Wuthiekanun V, Chierakul W, Chaowagul W, Day NP, Peacock SJ, 2005. Recurrent melioidosis in patients in northeast Thailand is frequently due to re-infection rather than relapse. J Clin Microbiol 43: 6032–6034.
-
5.
Currie BJ, Jacups SP, 2003. Intensity of rainfall and severity of melioidosis, Australia. Emerg Infect Dis 9: 1538–1542.
-
6.
Su HP, Yang HW, Chen YL, Ferng TL, Chou YL, Chung TC, Chen CH, Chiang CS, Kuan MM, Lin HH, Chen YS, 2007. Prevalence of melioidosis in the Er-Ren River Basin, Taiwan: implications for transmission. J Clin Microbiol 45: 2599–2603.
-
7.
Inglis TJ, O'Reilly L, Merritt AJ, Levy A, Heath CH, 2011. The aftermath of the Western Australian melioidosis outbreak. Am J Trop Med Hyg 84: 851–857.
-
8.
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: 272–282.
-
9.
Ulett GC, Currie BJ, Clair TW, Mayo M, Ketheesan N, Labrooy J, Gal D, Norton R, Smith CA, Barnes J, Warner J, Hirst RG, 2001. Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect 3: 621–631.
-
10.
Chantratita N, Wuthiekanun V, Boonbumrung K, Tiyawisutsri R, Vesaratchavest M, Limmathurotsakul D, Chierakul W, Wongratanacheewin S, Pukritiyakamee S, White NJ, Day NP, Peacock S, 2006. Biological relevance of colony morphology and phenotypic switching by Burkholderia pseudomallei. J Bacteriol 189: 807–817.
-
11.
Sawasdidoln C, Taweechaisupapong S, Sermswan RW, Tattawasart U, Tungpradabkul S, Wongratanacheewin S, 2010. Growing Burkholderia pseudomallei in biofilm stimulating conditions significantly induces antimicrobial resistance. PLoS ONE 5: e9196.
-
12.
Vellasamy KM, Vasu C, Puthucheary SD, Vadivelu J, 2009. Comparative analysis of extracellular enzymes and virulence exhibited by Burkholderia pseudomallei from different sources. Microb Pathog 47: 111–117.
-
13.
Mann EE, Wozniak DJ, 2012. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36: 893–916.
-
14.
Choi KS, Veeraragouda Y, Cho KM, Lee SO, Jo GR, Cho K, Lee K, 2007. Effect of gacS and gacA mutations on colony architecture, surface motility, biofilm formation and chemical toxicity in Pseudomonas sp. KL28. J Microbiol 45: 492–498.
-
15.
Yan Q, Hu X, Wang N, 2012. The novel virulence-related gene nlxA in the lipopolysaccharide cluster of Xanthomonas citri ssp. citri is involved in the production of lipopolysaccharide and extracellular polysaccharide, motility, biofilm formation and stress resistance. Mol Plant Pathol 13: 923–934.
-
16.
Subramoni S, Nguyen DT, Sokol PA, 2011. Burkholderia cenocepacia ShvR-regulated genes that influence colony morphology, biofilm formation, and virulence. Infect Immun 79: 2984–2997.
-
17.
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: 184–189.
-
18.
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): S5–S9.
-
19.
Chen YS, Lin HH, Mu JJ, Chiang CS, Chen CH, Buu LM, Lin YE, Chen YL, 2010. Distribution of melioidosis cases and viable Burkholderia pseudomallei in soil: evidence for emerging melioidosis in Taiwan. J Clin Microbiol 48: 1432–1434.
-
20.
Chen YL, Lin YC, Chen YS, Chen SC, Liu YM, Tseng IL, Chiang CS, Lin HH, Mu JJ, 2013. Characterization of predominant molecular patterns of Burkholderia pseudomallei in Taiwan. Trans R Soc Trop Med Hyg 107: 165–169.
-
21.
Inglis TJ, Sagripanti JL, 2006. Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl Environ Microbiol 72: 6865–6875.
-
22.
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: 253–256.
-
23.
Mima T, Schweizer HP, 2010. The BpeAB-OprB efflux pump of Burkholderia pseudomallei 1026b does not play a role in quorum sensing, virulence factor production, or extrusion of aminoglycosides but is a broad-spectrum drug efflux system. Antimicrob Agents Chemother 54: 3113–3120.
-
24.
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: 368–374.
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