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BioMed Research International
Volume 2018, Article ID 3039106, 11 pages
https://doi.org/10.1155/2018/3039106
Review Article

Burkholderia pseudomallei Adaptation for Survival in Stressful Conditions

1Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand
2Department of Companion Animal Clinical Sciences, Faculty of Veterinary Medicine, Kasetsart University, Bangkok 10900, Thailand

Correspondence should be addressed to Pornpan Pumirat; ht.ca.lodiham@mup.napnrop

Received 18 January 2018; Revised 9 March 2018; Accepted 5 April 2018; Published 27 May 2018

Academic Editor: Isabel Sá-Correia

Copyright © 2018 Taksaon Duangurai et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. J. Brett and D. E. Woods, “Pathogenesis of and immunity to melioidosis,” Acta Tropica, vol. 74, no. 2-3, pp. 201–210, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Whitmore, “An account of a glanders-like disease occurring in rangoon,” Journal of Hygiene, vol. 13, no. 1, pp. 1–34, 1913. View at Google Scholar
  3. R. P. Samy, B. G. Stiles, G. Sethi, and L. H. K. Lim, “Melioidosis: clinical impact and public health threat in the tropics,” PLOS Neglected Tropical Diseases, vol. 11, no. 5, Article ID e0004738, 2017. View at Publisher · View at Google Scholar · View at Scopus
  4. T. J. Inglis and A. Q. Sousa, “The public health implications of melioidosis,” The Brazilian Journal of Infectious Diseases, vol. 13, no. 1, pp. 59–66, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. N. J. White, “Melioidosis,” The Lancet, vol. 361, no. 9370, pp. 1715–1722, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Yabuuchi, Y. Kosako, and H. Oyaizu, “Proposal of Burkholderia gen. Anov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb: Nov,” Microbiology and Immunology, vol. 36, no. 12, pp. 1251–1275, 1992. View at Google Scholar
  7. A. C. Cheng and B. J. Currie, “Melioidosis: epidemiology, pathophysiology, and management,” Clinical Microbiology Reviews, vol. 18, no. 2, pp. 383–416, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. T. J. J. Inglis and J.-L. Sagripanti, “Environmental factors that affect the survival and persistence of Burkholderia pseudomallei,” Applied and Environmental Microbiology, vol. 72, no. 11, pp. 6865–6875, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. X. Liu, L. Pang, S. H. Sim et al., “Association of melioidosis incidence with rainfall and humidity, Singapore, 2003–2012,” Emerging Infectious Diseases, vol. 21, no. 1, pp. 159–162, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. B. J. Currie and S. P. Jacups, “Intensity of rainfall and severity of melioidosis, Australia,” Emerging Infectious Diseases, vol. 9, no. 12, pp. 1538–1542, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Kaestli, E. P. M. Grist, L. Ward, A. Hill, M. Mayo, and B. J. Currie, “The association of melioidosis with climatic factors in Darwin, Australia: a 23-year time-series analysis,” Infection, vol. 72, no. 6, pp. 687–697, 2016. View at Publisher · View at Google Scholar · View at Scopus
  12. A. J. Merritt and T. J. Inglis, “The role of climate in the epidemiology of melioidosis,” Current Tropical Medicine Reports, vol. 4, no. 4, pp. 185–191, 2017. View at Publisher · View at Google Scholar
  13. L. Manivanh, A. Pierret, S. Rattanavong et al., “Burkholderia pseudomallei in a lowland rice paddy: seasonal changes and influence of soil depth and physico-chemical properties,” Scientific Reports, vol. 7, no. 1, article no. 3031, 2017. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Tong, S. Yang, Z. Lu, and W. He, “Laboratory investigation of ecological factors influencing the environmental presence of Burkholderia pseudomallei,” Microbiology and Immunology, vol. 40, no. 6, pp. 451–453, 1996. View at Publisher · View at Google Scholar · View at Scopus
  15. V. Hantrakun, P. Rongkard, M. Oyuchua et al., “Soil nutrient depletion is associated with the presence of Burkholderia pseudomallei,” Applied and Environmental Microbiology, vol. 82, no. 24, pp. 7086–7092, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. H. I. Musa, L. Hassan, Z. H. Shamsuddin, C. Panchadcharam, Z. Zakaria, and S. A. Aziz, “Physicochemical properties influencing presence of Burkholderia pseudomallei in soil from small ruminant farms in peninsular Malaysia,” PLoS ONE, vol. 11, no. 9, Article ID e0162348, 2016. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Tuanyok, H. S. Kim, W. C. Nierman et al., “Genome-wide expression analysis of iron regulation in Burkholderia pseudomallei and Burkholderia mallei using DNA microarrays,” FEMS Microbiology Letters, vol. 252, no. 2, pp. 327–335, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. T. J. J. Inglis, P. Rigby, T. A. Robertson, N. S. Dutton, M. Henderson, and B. J. Chang, “Interaction between Burkholderia pseudomallei and Acanthamoeba species results in coiling phagocytosis, endamebic bacterial survival, and escape,” Infection and Immunity, vol. 68, no. 3, pp. 1681–1686, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. T. J. Inglis, F. Rodrigues, P. Rigby, R. Norton, and B. J. Currie, “Comparison of the susceptibilities of Burkholderia pseudomallei to meropenem and ceftazidime by conventional and intracellular methods,” Antimicrobial Agents and Chemotherapy, vol. 48, no. 8, pp. 2999–3005, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Noinarin, P. Chareonsudjai, P. Wangsomnuk, S. Wongratanacheewin, and S. Chareonsudjai, “Environmental free-living amoebae isolated from soil in Khon Kaen, Thailand, antagonize Burkholderia pseudomallei,” PLoS ONE, vol. 11, no. 11, Article ID e0167355, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. M. T. G. Holden, R. W. Titball, S. J. Peacock et al., “Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 101, no. 39, pp. 14240–14245, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. S. J. Willcocks, C. C. Denman, H. S. Atkins, and B. W. Wren, “Intracellular replication of the well-armed pathogen Burkholderia pseudomallei,” Current Opinion in Microbiology, vol. 29, pp. 94–103, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. G. W. Sun, Y. Chen, Y. Liu et al., “Identification of a regulatory cascade controlling Type III Secretion System 3 gene expression in Burkholderia pseudomallei,” Molecular Microbiology, vol. 76, no. 3, pp. 677–689, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Pumpuang, N. Chantratita, C. Wikraiphat et al., “Survival of Burkholderia pseudomallei in distilled water for 16 years,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 105, no. 10, pp. 598–600, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. M. A. Hamad, C. R. Austin, A. L. Stewart, M. Higgins, A. Vázquez-Torres, and M. I. Voskuil, “Adaptation and antibiotic tolerance of anaerobic Burkholderia pseudomallei,” Antimicrobial Agents and Chemotherapy, vol. 55, no. 7, pp. 3313–3323, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. A. O’Rourke, N. Yee, W. C. Nierman, and S. Beyhan, “Environmental and genetic factors controlling Burkholderia pseudomallei persister phenotypes,” Current Tropical Medicine Reports, vol. 4, no. 3, pp. 111–116, 2017. View at Publisher · View at Google Scholar
  27. P. Pumirat, J. Cuccui, R. A. Stabler et al., “Global transcriptional profiling of Burkholderia pseudomallei under salt stress reveals differential effects on the Bsa type III secretion system,” BMC Microbiology, vol. 10, article no. 171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Pumirat, P. Saetun, S. Sinchaikul, S.-T. Chen, S. Korbsrisate, and V. Thongboonkerd, “Altered secretome of Burkholderia pseudomallei induced by salt stress,” Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, vol. 1794, no. 6, pp. 898–904, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Jitprasutwit, C. Ong, N. Juntawieng et al., “Transcriptional profiles of Burkholderia pseudomallei reveal the direct and indirect roles of Sigma E under oxidative stress conditions,” BMC Genomics, vol. 15, no. 1, article no. 787, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Korbsrisate, M. Vanaporn, P. Kerdsuk et al., “The Burkholderia pseudomallei RpoE (AlgU) operon is involved in environmental stress tolerance and biofilm formation,” FEMS Microbiology Letters, vol. 252, no. 2, pp. 243–249, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. P. Pumirat, U. Boonyuen, M. Vanaporn et al., “The role of short-chain dehydrogenase/oxidoreductase, induced by salt stress, on host interaction of B. pseudomallei,” BMC Microbiology, vol. 14, no. 1, article no. 1, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Pumirat, M. Vanaporn, U. Boonyuen, N. Indrawattana, A. Rungruengkitkun, and N. Chantratita, “Effects of sodium chloride on heat resistance, oxidative susceptibility, motility, biofilm and plaque formation of Burkholderia pseudomallei,” MicrobiologyOpen, vol. 6, no. 4, Article ID e00493, 2017. View at Publisher · View at Google Scholar · View at Scopus
  33. W. Jangiama, S. Lopraserf, and S. Tungpradabkula, “Role of Burkholderia pseudomallei RpoS in regulation of catalase activities under hydrogen peroxide induction,” ScienceAsia, vol. 34, no. 1, pp. 23–29, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Chutoam, V. Charoensawan, P. Wongtrakoongate, A. Kum-arth, P. Buphamalai, and S. Tungpradabkul, “RpoS and oxidative stress conditions regulate succinyl-CoA: 3-ketoacid-coenzyme A transferase (SCOT) expression in Burkholderia pseudomallei,” Microbiology and Immunology, vol. 57, no. 9, pp. 605–615, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Lumijiaktase, S. P. Diggle, S. Loprasert et al., “Quorum sensing regulates dpsA and the oxidative stress response in Burkholderia pseudomallei,” Microbiology, vol. 152, no. 12, pp. 3651–3659, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Loprasert, R. Sallabhan, W. Whangsuk, and S. Mongkolsuk, “Characterization and mutagenesis of fur gene from Burkholderia pseudomallei,” Gene, vol. 254, no. 1-2, pp. 129–137, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Ratledge and L. G. Dover, “Iron metabolism in pathogenic bacteria,” Annual Review of Microbiology, vol. 54, pp. 881–941, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Tabunhan, S. Wongratanacheewin, S. Wongwajana, T. U. M. Welbat, K. Faksri, and W. Namwat, “Characterization of a novel two-component system response regulator involved in biofilm formation and a low-iron response of Burkholderia pseudomallei,” The Southeast Asian Journal of Tropical Medicine and Public Health, vol. 45, no. 5, pp. 1065–1079, 2014. View at Google Scholar · View at Scopus
  39. P. L. Felgner, M. A. Kayala, A. Vigil et al., “A Burkholderia pseudomallei protein microarray reveals serodiagnostic and cross-reactive antigens,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 106, no. 32, pp. 13499–13504, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. C. W. Vander Broek, K. J. Chalmers, M. P. Stevens, and J. M. Stevens, “Quantitative proteomic analysis of Burkholderia pseudomallei Bsa type III secretion system effectors using hypersecreting mutants,” Molecular and Cellular Proteomics, vol. 14, no. 4, pp. 905–916, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. L. C. Wang, L. K. Morgan, P. Godakumbura, L. J. Kenney, and G. S. Anand, “The inner membrane histidine kinase EnvZ senses osmolality via helix-coil transitions in the cytoplasm,” EMBO Journal, vol. 34, no. 19, p. 2481, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Kimura, M. Ohtani, and K. Takegawa, “An adenylyl cyclase, CyaB, acts as an osmosensor in Myxococcus xanthus,” Journal of Bacteriology, vol. 187, no. 10, pp. 3593–3598, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. W. Kamjumphol, P. Chareonsudjai, S. Taweechaisupapong, and S. Chareonsudjai, “Morphological alteration and survival of Burkholderia pseudomallei in soil microcosms,” The American Journal of Tropical Medicine and Hygiene, vol. 93, no. 5, pp. 1058–1065, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. Y.-X. Zhang, C. D. Denoya, D. D. Skinner et al., “Genes encoding acyl-CoA dehydrogenase (AcdH) homologues from Streptomyces coelicolor and Streptomyces avermitilis provide insights into the metabolism of small branched-chain fatty acids and macrolide antibiotic production,” Microbiology, vol. 145, no. 9, pp. 2323–2334, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. W. Wu, H. Badrane, S. Arora, H. V. Baker, and S. Jin, “MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa,” Journal of Bacteriology, vol. 186, no. 22, pp. 7575–7585, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Berry, J. D. DeVault, and A. M. Chakrabarty, “High osmolarity is a signal for enhanced algD transcription in mucoid and nonmucoid Pseudomonas aeruginosa strains,” Journal of Bacteriology, vol. 171, no. 5, pp. 2312–2317, 1989. View at Publisher · View at Google Scholar · View at Scopus
  47. K. L. Kavanagh, H. Jörnvall, B. Persson, and U. Oppermann, “Medium- and short-chain dehydrogenase/reductase gene and protein families: the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes,” Cellular and Molecular Life Sciences, vol. 65, no. 24, pp. 3895–3906, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. U. Oppermann, C. Filling, M. Hult et al., “Short-chain dehydrogenases/reductases (SDR): the 2002 update,” Chemico-Biological Interactions, vol. 143-144, pp. 247–253, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Vanaporn, P. Vattanaviboon, V. Thongboonkerd, and S. Korbsrisate, “The rpoE operon regulates heat stress response in Burkholderia pseudomallei,” FEMS Microbiology Letters, vol. 284, no. 2, pp. 191–196, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Fu, J. Yuan, and H. Gao, “Microbial oxidative stress response: novel insights from environmental facultative anaerobic bacteria,” Archives of Biochemistry and Biophysics, vol. 584, article no. 7047, pp. 28–35, 2015. View at Publisher · View at Google Scholar · View at Scopus
  51. N.-S. Jwa, G. K. Agrawal, S. Tamogami et al., “Role of defense/stress-related marker genes, proteins and secondary metabolites in defining rice self-defense mechanisms,” Plant Physiology and Biochemistry, vol. 44, no. 5-6, pp. 261–273, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Huang, V. Canadien, G. Y. Lam et al., “Activation of antibacterial autophagy by NADPH oxidases,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 106, no. 15, pp. 6226–6231, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. F. Vatansever, W. C. M. A. de Melo, P. Avci et al., “Antimicrobial strategies centered around reactive oxygen species—bactericidal antibiotics, photodynamic therapy, and beyond,” FEMS Microbiology Reviews, vol. 37, no. 6, pp. 955–989, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. B. Subsin, M. S. Thomas, G. Katzenmeier, J. G. Shaw, S. Tungpradabkul, and M. Kunakorn, “role of the stationary growth phase sigma factor RpoS of Burkholderia pseudomallei in response to physiological stress conditions,” Journal of Bacteriology, vol. 185, no. 23, pp. 7008–7014, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. M. C. Davis, C. A. Kesthely, E. A. Franklin, and S. R. MacLellan, “The essential activities of the bacterial sigma factor,” Canadian Journal of Microbiology, vol. 63, no. 2, pp. 89–99, 2017. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Feklístov, B. D. Sharon, S. A. Darst, and C. A. Gross, “Bacterial sigma factors: A historical, structural, and genomic perspective,” Annual Review of Microbiology, vol. 68, pp. 357–376, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Yam, A. A. Rahim, S. Mohamad et al., “The multiple roles of hypothetical gene BPSS1356 in Burkholderia pseudomallei,” PLoS ONE, vol. 9, no. 6, Article ID e99218, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. D. T. Diep, N. T. Phuong, M. M. Hlaing, P. Srimanote, and S. Tungpradabkul, “Role of Burkholderia pseudomallei Sigma N2 in Amino Acids Utilization and in Regulation of Catalase E Expression at the Transcriptional Level,” International Journal of Bacteriology, vol. 2015, Article ID 623967, pp. 1–10, 2015. View at Publisher · View at Google Scholar
  59. A. E. Pegg, “Mammalian polyamine metabolism and function,” IUBMB Life, vol. 61, no. 9, pp. 880–894, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Loprasert, W. Whangsuk, R. Sallabhan, and S. Mongkolsuk, “Regulation of the katG-dpsA operon and the importance of KatG in survival of Burkholderia pseudomallei exposed to oxidative stress,” FEBS Letters, vol. 542, no. 1-3, pp. 17–21, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. W. Kamjumphol, S. Chareonsudjai, P. Chareonsudjai, S. Wongratanacheewin, and S. Taweechaisupapong, “Environmental factors affecting Burkholderia pseudomallei biofilm formation,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 44, no. 1, pp. 72–81, 2013. View at Google Scholar · View at Scopus
  62. B. Gerhardy and G. Simpson, “Melioidosis and idiopathic pulmonary hemosiderosis: a cast-iron case,” Respirology Case Reports, vol. 1, no. 2, pp. 46-47, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. W. Amornrit, V. Muangsombut, T. Wangteeraprasert, and S. Korbsrisate, “Elevated intracellular levels of iron in host cells promotes Burkholderia pseudomallei infection,” Asian Biomedicine, vol. 6, no. 3, pp. 465–471, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Suputtamongkol, W. Chaowagul, P. Chetchotisakd et al., “Risk factors for melioidosis and bacteremic melioidosis,” Clinical Infectious Diseases, vol. 29, no. 2, pp. 408–413, 1999. View at Publisher · View at Google Scholar · View at Scopus
  65. S. M. Fong, K. J. Wong, M. Fukushima, and T. W. Yeo, “Thalassemia major is a major risk factor for pediatric melioidosis in Kota Kinabalu, Sabah, Malaysia,” Clinical Infectious Diseases, vol. 60, no. 12, pp. 1802–1807, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. I. H. Schmidt, C. Gildhorn, M. A. Böning et al., “Burkholderia pseudomallei modulates host iron homeostasis to facilitate iron availability and intracellular survival,” PLOS Neglected Tropical Diseases, vol. 12, no. 1, p. e0006096, 2018. View at Publisher · View at Google Scholar
  67. C. M. Litwin and S. B. Calderwood, “Role of iron in regulation of virulence genes,” Clinical Microbiology Reviews, vol. 6, no. 2, pp. 137–149, 1993. View at Publisher · View at Google Scholar · View at Scopus
  68. L. Runyen-Janecky, A. Daugherty, B. Lloyd, C. Wellington, H. Eskandarian, and M. Sagransky, “Role and regulation of iron-sulfur cluster biosynthesis genes in Shigella flexneri virulence,” Infection and Immunity, vol. 76, no. 3, pp. 1083–1092, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Dacanay, S. C. Johnson, R. Bjornsdottir et al., “Molecular characterization and quantitative analysis of superoxide dismutases in virulent and avirulent strains of Aeromonas salmonicida subsp. salmonicida,” Journal of Bacteriology, vol. 185, no. 15, pp. 4336–4344, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. B. H. Kvitko, A. Goodyear, K. L. Propst, S. W. Dow, and H. P. Schweizer, “Burkholderia pseudomallei known siderophores and hemin uptake are dispensable for lethal murine melioidosis,” PLOS Neglected Tropical Diseases, vol. 6, no. 6, Article ID e1715, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. A. T. Butt and M. S. Thomas, “Iron acquisition mechanisms and their role in the virulence of Burkholderia species,” Frontiers in Cellular and Infection Microbiology, vol. 7, article no. 460, 2017. View at Publisher · View at Google Scholar · View at Scopus
  72. P. A. Sokol, P. Darling, D. E. Woods, E. Mahenthiralingam, and C. Kooi, “Role of ornibactin biosynthesis in the virulence of Burkholderia cepacia: characterization of pvdA, the gene encoding L-ornithine N5- oxygenase,” Infection and Immunity, vol. 67, no. 9, pp. 4443–4455, 1999. View at Google Scholar · View at Scopus
  73. M. B. Visser, S. Majumdar, E. Hani, and P. A. Sokol, “Importance of the ornibactin and pyochelin siderophore transport systems in Burkholderia cenocepacia lung infections,” Infection and Immunity, vol. 72, no. 5, pp. 2850–2857, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. D. N. Harland, E. Dassa, R. W. Titball, K. A. Brown, and H. S. Atkins, “ATP-binding cassette systems in Burkholderia pseudomallei and Burkholderia mallei,” BMC Genomics, vol. 8, article no. 83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. C. Kunyanee, W. Kamjumphol, S. Taweechaisupapong et al., “Burkholderia pseudomallei biofilm promotes adhesion, internalization and stimulates proinflammatory cytokines in human epithelial A549 cells,” PLoS ONE, vol. 11, no. 8, Article ID e0160741, 2016. View at Publisher · View at Google Scholar · View at Scopus
  76. M. N. Burtnick and P. J. Brett, “Burkholderia mallei and Burkholderia pseudomallei cluster 1 type VI secretion system gene expression is negatively regulated by iron and Zinc,” PLoS ONE, vol. 8, no. 10, Article ID e76767, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. M. A. Valvano, K. E. Keith, and S. T. Cardona, “Survival and persistence of opportunistic Burkholderia species in host cells,” Current Opinion in Microbiology, vol. 8, no. 1, pp. 99–105, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. M. G. Moule, N. Spink, S. Willcocks et al., “Characterization of new virulence factors involved in the intracellular growth and survival of Burkholderia pseudomallei,” Infection and Immunity, vol. 84, no. 3, pp. 701–710, 2016. View at Publisher · View at Google Scholar · View at Scopus
  79. M. P. Stevens, A. Haque, T. Atkins et al., “Attenuated virulence and protective efficacy of a Burkholderia pseudomallei bsa type III secretion mutant in murine models of melioidosis,” Microbiology, vol. 150, no. 8, pp. 2669–2676, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. P. Pumirat, C. V. Broek, N. Juntawieng et al., “Analysis of the prevalence, secretion and function of a cell cycle-inhibiting factor in the melioidosis pathogen Burkholderia pseudomallei,” PLoS ONE, vol. 9, no. 5, Article ID e96298, 2014. View at Publisher · View at Google Scholar · View at Scopus
  81. M. P. Stevens, M. W. Wood, L. A. Taylor et al., “An Inv/Mxi-Spa-like type III protein secretion system in Burkholderia pseudomallei modulates intracellular behaviour of the pathogen,” Molecular Microbiology, vol. 46, no. 3, pp. 649–659, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. M. N. Burtnick, P. J. Brett, V. Nair, J. M. Warawa, D. E. Woods, and F. C. Gherardini, “Burkholderia pseudomallei type III secretion system mutants exhibit delayed vacuolar escape phenotypes in RAW 264.7 murine macrophages,” Infection and Immunity, vol. 76, no. 7, pp. 2991–3000, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. B. E. Teh, C. T. French, Y. Chen et al., “Type three secretion system-mediated escape of Burkholderia pseudomallei into the host cytosol is critical for the activation of NFκB,” BMC Microbiology, vol. 14, no. 1, article no. 115, 2014. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Pilatz, K. Breitbach, N. Hein et al., “Identification of Burkholderia pseudomallei genes required for the intracellular life cycle and in vivo virulence,” Infection and Immunity, vol. 74, no. 6, pp. 3576–3586, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. C. T. French, I. J. Toesca, T.-H. Wu et al., “Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 108, no. 29, pp. 12095–12100, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. V. Muangsombut, S. Suparak, P. Pumirat et al., “Inactivation of Burkholderia pseudomallei bsaQ results in decreased invasion efficiency and delayed escape of bacteria from endocytic vesicles,” Archives of Microbiology, vol. 190, no. 6, pp. 623–631, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. Y. Chen, I. Schröder, C. T. French et al., “Characterization and analysis of the Burkholderia pseudomallei BsaN virulence regulon,” BMC Microbiology, vol. 14, no. 1, article no. 206, 2014. View at Publisher · View at Google Scholar · View at Scopus
  88. V. Srinon, S. Muangman, N. Imyaem et al., “Comparative assessment of the intracellular survival of the Burkholderia pseudomallei bopC mutant,” Journal of Microbiology, vol. 51, no. 4, pp. 522–526, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Cullinane, L. Gong, X. Li et al., “Stimulation of autophagy suppresses the intracellular survival of Burkholderia pseudomallei in mammalian cell lines,” Autophagy, vol. 4, no. 6, pp. 744–753, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. Y. Chen, J. Wong, G. W. Sun, Y. Liu, G.-Y. G. Tan, and Y.-H. Gan, “Regulation of type VI secretion system during Burkholderia pseudomallei infection,” Infection and Immunity, vol. 79, no. 8, pp. 3064–3073, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. C. Sitthidet, S. Korbsrisate, A. N. Layton, T. R. Field, M. P. Stevens, and J. M. Stevens, “Identification of motifs of Burkholderia pseudomallei BimA required for intracellular motility, actin binding, and actin polymerization,” Journal of Bacteriology, vol. 193, no. 8, pp. 1901–1910, 2011. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Chieng, L. Carreto, and S. Nathan, “Burkholderia pseudomallei transcriptional adaptation in macrophages,” BMC Genomics, vol. 13, article 328, 2012. View at Publisher · View at Google Scholar · View at Scopus