Burkholderia mallei and Burkholderia pseudomallei Cluster 1 Type VI Secretion System Gene Expression Is Negatively Regulated by Iron and Zinc

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Burtnick, Mary N ^a   Brett, Paul J ^a  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERROUS SULFATE; ZINC SULFATE;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BIMA GENE; BURKHOLDERIA MALLEI; BURKHOLDERIA PSEUDOMALLEI; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HCP1 GENE; NONHUMAN; TSSA GENE; TSSM GENE; TYPE VI SECRETION SYSTEM;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BURKHOLDERIA MALLEI; BURKHOLDERIA PSEUDOMALLEI; CATIONS, DIVALENT; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; IRON; MULTIGENE FAMILY; PHYSICAL CHROMOSOME MAPPING; RNA, MESSENGER; ZINC;

EID: 84885416823     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076767     Document Type: Article

References (75)

1. Miller WR, Pannell L, Cravitz L, Tanner WA, Rosebury T, (1948) Studies on certain biological characteristics of Malleomyces mallei and Malleomyces pseudomallei: II. virulence and infectivity for animals. J Bacteriol 55: 127-135.
2. Neubauer H, Sprague LD, Zacharia R, Tomaso H, Al Dahouk S, et al. (2005) Serodiagnosis of Burkholderia mallei infections in horses: state-of-the-art and perspectives. J Vet Med B Infect Dis Vet Public Health 52: 201-205.
3. Redfearn MS, Palleroni NJ, Stanier RY, (1966) A comparative study of Pseudomonas pseudomallei and Bacillus mallei. J Gen Microbiol 43: 293-313.
4. Waag DM, DeShazer D (2004) Glanders: new insights into an old disease. In: Lindler LE, Lebeda FJ, Korch GW, editors. Biological weapons defense: infectious diseases and counterbioterrorism. 1st ed: Humana Press, Inc, Totowa, NJ. 209-237.
5. Khan I, Wieler LH, Melzer F, Elschner MC, Muhammad G, et al. (2012) Glanders in animals: a review on epidemiology, clinical presentation, diagnosis and countermeasures. Transbound Emerg Dis 60: 204-221.
6. Malik P, Singha H, Khurana SK, Kumar R, Kumar S, et al. (2012) Emergence and re-emergence of glanders in India: a description of outbreaks from 2006 to 2011. Vet Ital 48: 167-178.
7. Arun S, Neubauer H, Gurel A, Ayyildiz G, Kuscu B, et al. (1999) Equine glanders in Turkey. Vet Rec 144: 255-258.
8. Elschner MC, Klaus CU, Liebler-Tenorio E, Schmoock G, Wohlsein P, et al. (2009) Burkholderia mallei infection in a horse imported from Brazil. Equine Veterinary Education 21: 147-150.
9. Wernery U, Wernery R, Joseph M, Al-Salloom F, Johnson B, et al. (2011) Natural Burkholderia mallei infection in dromedary, Bahrain. Emerg Infect Dis 17: 1277-1279.
10. Khaki P, Mosavari N, Khajeh NS, Emam M, Ahouran M, et al. (2012) Glanders outbreak at Tehran Zoo, Iran. Iran J Microbiol 4: 3-7.
11. Lopez J, Copps J, Wilhelmsen C, Moore R, Kubay J, et al. (2003) Characterization of experimental equine glanders. Microbes Infect 5: 1125-1131.
12. Howe C, Miller WR, (1947) Human glanders: report of six cases. Ann Intern Med 26: 93-115.
13. Srinivasan A, Kraus CN, DeShazer D, Becker PM, Dick JD, et al. (2001) Glanders in a military research microbiologist. N Engl J Med 345: 256-258.
14. Rotz LD, Khan AS, Lillibridge SR, Ostroff SM, Hughes JM, (2002) Public health assessment of potential biological terrorism agents. Emerg Infect Dis 8: 225-230.
15. Voskuhl GW, Cornea P, Bronze MS, Greenfield RA, (2003) Other bacterial diseases as a potential consequence of bioterrorism: Q fever, brucellosis, glanders, and melioidosis. J Okla State Med Assoc 96: 214-217.
16. Galyov EE, Brett PJ, DeShazer D, (2010) Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis. Annu Rev Microbiol 64: 495-517.
17. Burtnick MN, DeShazer D, Nair V, Gherardini FC, Brett PJ, (2010) Burkholderia mallei cluster 1 type VI secretion mutants exhibit growth and actin polymerization defects in RAW 264.7 murine macrophages. Infect Immun 78: 88-99.
18. Ulrich RL, DeShazer D, (2004) Type III secretion: a virulence factor delivery system essential for the pathogenicity of Burkholderia mallei. Infect Immun 72: 1150-1154.
19. Brett PJ, Burtnick MN, Su H, Nair V, Gherardini FC, (2008) iNOS activity is critical for the clearance of Burkholderia mallei from infected RAW 264.7 murine macrophages. Cell Microbiol 10: 487-498.
20. Fritz DL, Vogel P, Brown DR, Deshazer D, Waag DM, (2000) Mouse model of sublethal and lethal intraperitoneal glanders (Burkholderia mallei). Vet Pathol 37: 626-636.
21. Ribot WJ, Ulrich RL, (2006) The animal pathogen-like type III secretion system is required for the intracellular survival of Burkholderia mallei within J774.2 macrophages. Infect Immun 74: 4349-4353.
22. Nierman WC, DeShazer D, Kim HS, Tettelin H, Nelson KE, et al. (2004) Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci U S A 101: 14246-14251.
23. Schell MA, Ulrich RL, Ribot WJ, Brueggemann EE, Hines HB, et al. (2007) Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol Microbiol 64: 1466-1485.
24. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, et al. (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103: 1528-1533.
25. Bingle LE, Bailey CM, Pallen MJ, (2008) Type VI secretion: a beginner's guide. Curr Opin Microbiol 11: 3-8.
26. Filloux A, Hachani A, Bleves S, (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154: 1570-1583.
27. Pukatzki S, McAuley SB, Miyata ST, (2009) The type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol 12: 11-17.
28. Silverman JM, Brunet YR, Cascales E, Mougous JD, (2012) Structure and regulation of the type VI secretion system. Annu Rev Microbiol 66: 453-472.
29. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ, (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A 104: 15508-15513.
30. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, et al. (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci U S A 106: 4154-4159.
31. MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki S, (2010) The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci U S A 107: 19520-19524.
32. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ, (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483: 182-186.
33. Basler M, Ho BT, Mekalanos JJ, (2013) Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152: 884-894.
34. Cotter P, (2011) Microbiology: Molecular syringes scratch the surface. Nature 475: 301-303.
35. Bonemann G, Pietrosiuk A, Mogk A, (2010) Tubules and donuts: a type VI secretion story. Mol Microbiol 76: 815-821.
36. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR, (2009) The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci U S A 106: 4160-4165.
37. Murdoch SL, Trunk K, English G, Fritsch MJ, Pourkarimi E, et al. (2011) The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J Bacteriol 193: 6057-6069.
38. Bernard CS, Brunet YR, Gueguen E, Cascales E, (2010) Nooks and crannies in type VI secretion regulation. J Bacteriol 192: 3850-3860.
39. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ, (2009) Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5: 234-243.
40. Schwarz S, Hood RD, Mougous JD, (2010) What is type VI secretion doing in all those bugs? Trends Microbiol 18: 531-537.
41. Suarez G, Sierra JC, Sha J, Wang S, Erova TE, et al. (2008) Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb Pathog 44: 344-361.
42. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7: 25-37.
43. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, et al. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475: 343-347.
44. Russell AB, LeRoux M, Hathazi K, Agnello DM, Ishikawa T, et al. (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496: 508-512.
45. English G, Trunk K, Rao VA, Srikannathasan V, Hunter WN, et al. (2012) New secreted toxins and immunity proteins encoded within the Type VI secretion system gene cluster of Serratia marcescens. Mol Microbiol 86: 921-936.
46. Miyata ST, Kitaoka M, Brooks TM, McAuley SB, Pukatzki S, (2011) Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum. Infect Immun 79: 2941-2949.
47. Leung KY, Siame BA, Snowball H, Mok YK, (2010) Type VI secretion regulation: crosstalk and intracellular communication. Current Opinion in Microbiology 14: 1-7.
48. Miyata ST, Bachmann V, Pukatzki S, (2013) Type VI secretion system regulation as a consequence of evolutionary pressure. J Med Microbiol 62: 663-676.
49. 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: 1979-1991.
50. Burtnick MN, Brett PJ, Harding SV, Ngugi SA, Ribot WJ, et al. (2011) The Cluster 1 Type VI Secretion System is a Major Virulence Determinant in Burkholderia pseudomallei. Infect Immun 79: 1512-1525.
51. Chen Y, Wong J, Sun GW, Liu Y, Tan GY, et al. (2011) Regulation of type VI secretion system during Burkholderia pseudomallei infection. Infect Immun 79: 3064-3073.
52. Ishikawa T, Rompikuntal PK, Lindmark B, Milton DL, Wai SN, (2009) Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS One 4: e6734.
53. Ishikawa T, Sabharwal D, Broms J, Milton DL, Sjostedt A, et al. (2011) Pathoadaptive conditional regulation of the type VI secretion system in Vibrio cholerae O1 strains. Infect Immun 80: 575-584.
54. Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, et al. (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 4: e1000093.
55. Shalom G, Shaw JG, Thomas MS, (2007) In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. Microbiology 153: 2689-2699.
56. Yuan ZC, Liu P, Saenkham P, Kerr K, Nester EW, (2008) Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a complex acid-mediated signaling involved in Agrobacterium-plant interactions. J Bacteriol 190: 494-507.
57. Zheng J, Shin OS, Cameron DE, Mekalanos JJ, (2010) Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae. Proc Natl Acad Sci U S A 107: 21128-21133.
58. Hamad MA, Zajdowicz SL, Holmes RK, Voskuil MI, (2009) An allelic exchange system for compliant genetic manipulation of the select agents Burkholderia pseudomallei and Burkholderia mallei. Gene 430: 123-131.
59. Sun GW, Chen Y, Liu Y, Tan GY, Ong C, et al. (2010) Identification of a regulatory cascade controlling Type III Secretion System 3 gene expression in Burkholderia pseudomallei. Mol Microbiol 76: 677-689.
60. French CT, Toesca IJ, Wu TH, Teslaa T, Beaty SM, et al. (2011) Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade. Proc Natl Acad Sci U S A 108: 12095-12100.
61. Brunet YR, Bernard CS, Gavioli M, Lloubes R, Cascales E, (2011) An epigenetic switch involving overlapping fur and DNA methylation optimizes expression of a type VI secretion gene cluster. PLoS Genet 7: e1002205.
62. Chakraborty S, Li M, Chatterjee C, Sivaraman J, Leung KY, et al. (2010) Temperature and Mg2+ sensing by a novel PhoP-PhoQ two-component system for regulation of virulence in Edwardsiella tarda. J Biol Chem 285: 38876-38888.
63. Chakraborty S, Sivaraman J, Leung KY, Mok YK, (2011) Two-component PhoB-PhoR regulatory system and ferric uptake regulator sense phosphate and iron to control virulence genes in type III and VI secretion systems of Edwardsiella tarda. J Biol Chem 286: 39417-39430.
64. Rogge ML, Thune RL, (2011) Regulation of the Edwardsiella ictaluri type III secretion system by pH and phosphate concentration through EsrA, EsrB, and EsrC. Appl Environ Microbiol 77: 4293-4302.
65. Sana TG, Hachani A, Bucior I, Soscia C, Garvis S, et al. (2012) The second type VI secretion system of Pseudomonas aeruginosa strain PAO1 is regulated by quorum sensing and Fur and modulates internalization in epithelial cells. J Biol Chem 287: 27095-27105.
66. Cellier MF, Courville P, Campion C, (2007) Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 9: 1662-1670.
67. Loprasert S, Sallabhan R, Whangsuk W, Mongkolsuk S, (2000) Characterization and mutagenesis of fur gene from Burkholderia pseudomallei. Gene 254: 129-137.
68. 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.
69. Schwarz S, West TE, Boyer F, Chiang WC, Carl MA, et al. (2010) Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 6.
70. Simon R, Priefer U, Puhler A, (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio-Technology 1: 784-791.
71. Ulrich RL, Ulrich MP, Schell MA, Kim HS, DeShazer D, (2006) Development of a polymerase chain reaction assay for the specific identification of Burkholderia mallei and differentiation from Burkholderia pseudomallei and other closely related Burkholderiaceae. Diagn Microbiol Infect Dis 55: 37-45.
72. Holden MT, Titball RW, Peacock SJ, Cerdeno-Tarraga AM, Atkins T, et al. (2004) Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 101: 14240-14245.
73. DeShazer D, Brett PJ, Carlyon R, Woods DE, (1997) Mutagenesis of Burkholderia pseudomallei with Tn5-OT182: isolation of motility mutants and molecular characterization of the flagellin structural gene. J Bacteriol 179: 2116-2125.
74. Brett PJ, DeShazer D, Woods DE, (1998) Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol 48 Pt 1: 317-320.
75. Burtnick M, Bolton A, Brett P, Watanabe D, Woods D, (2001) Identification of the acid phosphatase (acpA) gene homologues in pathogenic and non-pathogenic Burkholderia spp. facilitates TnphoA mutagenesis. Microbiology 147: 111-120.