1887

Abstract

Burkholderia cenocepacia K56-2 belongs to the Burkholderia cepacia complex, a group of Gram-negative opportunistic pathogens that have large and dynamic genomes. In this work, we identified the essential genome of B. cenocepacia K56-2 using high-density transposon mutagenesis and insertion site sequencing (Tn-seq circle). We constructed a library of one million transposon mutants and identified the transposon insertions at an average of one insertion per 27 bp. The probability of gene essentiality was determined by comparing of the insertion density per gene with the variance of neutral datasets generated by Monte Carlo simulations. Five hundred and eight genes were not significantly disrupted, suggesting that these genes are essential for survival in rich, undefined medium. Comparison of the B. cenocepacia K56-2 essential genome with that of the closely related B. cenocepacia J2315 revealed partial overlapping, suggesting that some essential genes are strain-specific. Furthermore, 158 essential genes were conserved in B. cenocepacia and two species belonging to the Burkholderia pseudomallei complex, B. pseudomallei K96243 and Burkholderia thailandensis E264. Porins, including OpcC, a lysophospholipid transporter, LplT, and a protein involved in the modification of lipid A with aminoarabinose were found to be essential in Burkholderia genomes but not in other bacterial essential genomes identified so far. Our results highlight the existence of cell envelope processes that are uniquely essential in species of the genus Burkholderia for which the essential genomes have been identified by Tn-seq.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000140
2017-11-21
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/mgen/3/11/mgen000140.html?itemId=/content/journal/mgen/10.1099/mgen.0.000140&mimeType=html&fmt=ahah

References

  1. Jordan IK, Rogozin IB, Wolf YI, Koonin EV. Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 2002;12:962–968 [CrossRef][PubMed]
    [Google Scholar]
  2. Rocha EP, Danchin A. Essentiality, not expressiveness, drives gene-strand bias in bacteria. Nat Genet 2003;34:377–378 [CrossRef][PubMed]
    [Google Scholar]
  3. Rocha EP, Danchin A. Gene essentiality determines chromosome organisation in bacteria. Nucleic Acids Res 2003;31:6570–6577 [CrossRef][PubMed]
    [Google Scholar]
  4. Rocha EP, Danchin A. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol Biol Evol 2004;21:108–116 [CrossRef][PubMed]
    [Google Scholar]
  5. Zhang R, Ou HY, Zhang CT. DEG: a database of essential genes. Nucleic Acids Res 2004;32:271D–272D [CrossRef][PubMed]
    [Google Scholar]
  6. Gao F, Zhang RR. Enzymes are enriched in bacterial essential genes. PLoS One 2011;6:e21683 [CrossRef][PubMed]
    [Google Scholar]
  7. Fields FR, Lee SW, McConnell MJ. Using bacterial genomes and essential genes for the development of new antibiotics. Biochem Pharmacol 2017;134:74–86 [CrossRef][PubMed]
    [Google Scholar]
  8. Mobegi FM, van Hijum SA, Burghout P, Bootsma HJ, de Vries SP et al. From microbial gene essentiality to novel antimicrobial drug targets. BMC Genomics 2014;15:958 [CrossRef][PubMed]
    [Google Scholar]
  9. Murima P, McKinney JD, Pethe K. Targeting bacterial central metabolism for drug development. Chem Biol 2014;21:1423–1432 [CrossRef][PubMed]
    [Google Scholar]
  10. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006;2:2006.0008 [CrossRef]
    [Google Scholar]
  11. Gerdes SY, Scholle MD, Campbell JW, Balázsi G, Ravasz E et al. Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J Bacteriol 2003;185:5673–5684 [CrossRef][PubMed]
    [Google Scholar]
  12. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK et al. Essential Bacillus subtilis genes. Proc Natl Acad Sci USA 2003;100:4678–4683 [CrossRef]
    [Google Scholar]
  13. Mori H, Isono K, Horiuchi T, Miki T. Functional genomics of Escherichia coli in Japan. Res Microbiol 2000;151:121–128 [CrossRef]
    [Google Scholar]
  14. Christen B, Abeliuk E, Collier JM, Kalogeraki VS, Passarelli B et al. The essential genome of a bacterium. Mol Syst Biol 2011;7:528–535 [CrossRef]
    [Google Scholar]
  15. Langridge GC, Phan M-D, Turner DJ, Perkins TT, Parts L et al. Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 2009;19:2308–2316 [CrossRef]
    [Google Scholar]
  16. Turner KH, Wessel AK, Palmer GC, Murray JL, Whiteley M. Essential genome of Pseudomonas aeruginosa in cystic fibrosis sputum. Proc Natl Acad Sci USA 2015;112:4110–4115 [CrossRef]
    [Google Scholar]
  17. Weerdenburg EM, Abdallah AM, Rangkuti F, Abd El Ghany M, Otto TD et al. Genome-wide transposon mutagenesis indicates that Mycobacterium marinum customizes its virulence mechanisms for survival and replication in different hosts. Infect Immun 2015;83:1778–1788 [CrossRef][PubMed]
    [Google Scholar]
  18. Yang H, Krumholz EW, Brutinel ED, Palani NP, Sadowsky MJ et al. Genome-scale metabolic network validation of Shewanella oneidensis using transposon insertion frequency analysis. PLoS Comput Biol 2014;10:e1003848 [CrossRef][PubMed]
    [Google Scholar]
  19. Gawronski JD, Wong SMS, Giannoukos G, Ward DV, Akerley BJ. Tracking insertion mutants within libraries by deep sequencing and a genome-wide screen for Haemophilus genes required in the lung. Proc Natl Acad Sci USA 2009;106:16422–16427 [CrossRef]
    [Google Scholar]
  20. Goodman AL, McNulty NP, Zhao Y, Leip D, Mitra RD et al. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 2009;6:279–289 [CrossRef][PubMed]
    [Google Scholar]
  21. Gallagher LA, Shendure J, Manoil C. Genome-scale identification of resistance functions in Pseudomonas aeruginosa using Tn-seq. MBio 2011;2:e00315-10 [CrossRef][PubMed]
    [Google Scholar]
  22. Moule MG, Hemsley CM, Seet Q, Guerra-Assunção JA, Lim J et al. Genome-wide saturation mutagenesis of Burkholderia pseudomallei K96243 predicts essential genes and novel targets for antimicrobial development. MBio 2014;5:e00926-13 [CrossRef][PubMed]
    [Google Scholar]
  23. Wong Y-C, Abd El Ghany M, Naeem R, Lee KW, Tan YC et al. Candidate essential genes in Burkholderia cenocepacia J2315 identified by genome-wide TraDIS. Front Microbiol 2016;7:1288 [CrossRef][PubMed]
    [Google Scholar]
  24. Eberl L, Vandamme P. Members of the genus Burkholderia: good and bad guys. F1000Res 2016;5:1007 [CrossRef][PubMed]
    [Google Scholar]
  25. Sahl JW, Vazquez AJ, Hall CM, Busch JD, Tuanyok A et al. The effects of signal erosion and core genome reduction on the identification of diagnostic markers. MBio 2016;7:e00846-16 [CrossRef][PubMed]
    [Google Scholar]
  26. Glass MB, Steigerwalt AG, Jordan JG, Wilkins PP, Gee JE. Burkholderia oklahomensis sp. nov., a Burkholderia pseudomallei-like species formerly known as the Oklahoma strain of Pseudomonas pseudomallei. Int J Syst Evol Microbiol 2006;56:2171–2176 [CrossRef]
    [Google Scholar]
  27. Tuanyok A, Mayo M, Scholz H, Hall CM, Allender CJ et al. Burkholderia humptydooensis sp. nov., a new species related to Burkholderia thailandensis and the fifth member of the Burkholderia pseudomallei complex. Appl Environ Microbiol 2017;83:e02802-16 [CrossRef][PubMed]
    [Google Scholar]
  28. Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ. Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 2006;4:272–282 [CrossRef]
    [Google Scholar]
  29. Mahenthiralingam E, Vandamme P. Taxonomy and pathogenesis of the Burkholderia cepacia complex. Chron Respir Dis 2005;2:209–217 [CrossRef]
    [Google Scholar]
  30. Vanlaere E, Lipuma JJ, Baldwin A, Henry D, de Brandt E et al. Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol 2008;58:1580–1590 [CrossRef]
    [Google Scholar]
  31. Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E et al. Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 2009;59:102–111 [CrossRef]
    [Google Scholar]
  32. Peeters C, Zlosnik JEA, Spilker T, Hird TJ, LiPuma JJ et al. Burkholderia pseudomultivorans sp. nov., a novel Burkholderia cepacia complex species from human respiratory samples and the rhizosphere. Syst Appl Microbiol 2013;36:483–489 [CrossRef]
    [Google Scholar]
  33. de Smet B, Spilker T, Ginther JL, Currie BJ, Zlosnik JEA et al. Burkholderia stagnalis sp. nov. and Burkholderia territorii sp. nov., two novel Burkholderia cepacia complex species from environmental and human sources. Int J Syst Evol Microbiol 2015;65:2265–2271 [CrossRef]
    [Google Scholar]
  34. Mahenthiralingam E, Baldwin A, Dowson CG. Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 2008;104:1539–1551 [CrossRef]
    [Google Scholar]
  35. Darling P, Chan M, Cox AD, Sokol PA. Siderophore production by cystic fibrosis isolates of Burkholderia cepacia. Infect Immun 1998;66:874–877
    [Google Scholar]
  36. Lipuma JJ, Spilker T, Gill LH, Campbell PW, Liu L et al. Disproportionate distribution of Burkholderia cepacia complex species and transmissibility markers in cystic fibrosis. Am J Respir Crit Care Med 2001;164:92–96 [CrossRef][PubMed]
    [Google Scholar]
  37. Cardona ST, Wopperer J, Eberl L, Valvano MA. Diverse pathogenicity of Burkholderia cepacia complex strains in the Caenorhabditis elegans host model. FEMS Microbiol Lett 2005;250:97–104 [CrossRef]
    [Google Scholar]
  38. Vergunst AC, Meijer AH, Renshaw SA, O'Callaghan D. Burkholderia cenocepacia creates an intramacrophage replication niche in zebrafish embryos, followed by bacterial dissemination and establishment of systemic infection. Infect Immun 2010;78:1495–1508 [CrossRef][PubMed]
    [Google Scholar]
  39. Mahenthiralingam E, Coenye T, Chung JW, Speert DP, Govan JR et al. Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 2000;38:910–913
    [Google Scholar]
  40. Holden MT, Seth-Smith HM, Crossman LC, Sebaihia M, Bentley SD et al. The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 2009;191:261–277 [CrossRef][PubMed]
    [Google Scholar]
  41. Bloodworth R. Essential genes and genomes of the Burkholderia cepacia complex. 2013;http://mspace.lib.umanitoba.ca/xmlui/handle/1993/30912 Accessed 31 March 2017
  42. Baldwin A, Sokol PA, Parkhill J, Mahenthiralingam E. The Burkholderia cepacia epidemic strain marker is part of a novel genomic island encoding both virulence and metabolism-associated genes in Burkholderia cenocepacia. Infect Immun 2004;72:1537–1547 [CrossRef][PubMed]
    [Google Scholar]
  43. Graindorge A, Menard A, Monnez C, Cournoyer B. Insertion sequence evolutionary patterns highlight convergent genetic inactivations and recent genomic island acquisitions among epidemic Burkholderia cenocepacia. J Med Microbiol 2012;61:394–409 [CrossRef]
    [Google Scholar]
  44. Lessie TG, Hendrickson W, Manning BD, Devereux R. Genomic complexity and plasticity of Burkholderia cepacia. FEMS Microbiol Lett 1996;144:117–128 [CrossRef]
    [Google Scholar]
  45. Seo YS, Lim JY, Park J, Kim S, Lee HH et al. Comparative genome analysis of rice-pathogenic Burkholderia provides insight into capacity to adapt to different environments and hosts. BMC Genomics 2015;16:349 [CrossRef][PubMed]
    [Google Scholar]
  46. Horvath P, Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science 2010;327:167–170 [CrossRef][PubMed]
    [Google Scholar]
  47. Dennis JJ. Burkholderia cenocepacia virulence microevolution in the CF lung: variations on a theme. Virulence 2016;1–3
    [Google Scholar]
  48. Baugh L, Gallagher LA, Patrapuvich R, Clifton MC, Gardberg AS et al. Combining functional and structural genomics to sample the essential Burkholderia structome. PLoS One 2013;8:e53851 [CrossRef][PubMed]
    [Google Scholar]
  49. Baldwin A, Mahenthiralingam E, Thickett KM, Honeybourne D, Maiden MC et al. Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 2005;43:4665–4673 [CrossRef][PubMed]
    [Google Scholar]
  50. Miller VL, Mekalanos JJ. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 1988;170:2575–2583 [CrossRef]
    [Google Scholar]
  51. Figurski DH, Helinski DR. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 1979;76:1648–1652 [CrossRef]
    [Google Scholar]
  52. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9:357–359 [CrossRef]
    [Google Scholar]
  53. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139–140 [CrossRef]
    [Google Scholar]
  54. Noble WS. How does multiple testing correction work?. Nat Biotechnol 2009;27:1135–1137 [CrossRef]
    [Google Scholar]
  55. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 1995;57:289–300
    [Google Scholar]
  56. Fraley C, Raftery AE. MCLUST: software for model-based cluster analysis. J Classif 1999;16:297–306 [CrossRef]
    [Google Scholar]
  57. Luo H, Lin Y, Gao F, Zhang CT, Zhang R. DEG 10, an update of the database of essential genes that includes both protein-coding genes and noncoding genomic elements. Nucleic Acids Res 2014;42:D574–D580 [CrossRef][PubMed]
    [Google Scholar]
  58. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 2000;28:33–36 [CrossRef]
    [Google Scholar]
  59. Mao X, Ma Q, Zhou C, Chen X, Zhang H et al. DOOR 2.0: presenting operons and their functions through dynamic and integrated views. Nucleic Acids Res 2014;42:D654–D659 [CrossRef]
    [Google Scholar]
  60. Bloodworth RAM, Gislason AS, Cardona ST. Burkholderia cenocepacia conditional growth mutant library created by random promoter replacement of essential genes. Microbiologyopen 2013;2:243–258 [CrossRef]
    [Google Scholar]
  61. Gallagher LA, Ramage E, Patrapuvich R, Weiss E, Brittnacher M et al. Sequence-defined transposon mutant library of Burkholderia thailandensis. MBio 2013;4:e00604-13 [CrossRef][PubMed]
    [Google Scholar]
  62. Quail MA, Otto TD, Gu Y, Harris SR, Skelly TF et al. Optimal enzymes for amplifying sequencing libraries. Nat Methods 2011;9:10–11 [CrossRef]
    [Google Scholar]
  63. Dhillon BK, Laird MR, Shay JA, Winsor GL, Lo R et al. IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis. Nucleic Acids Res 2015;43:W104–W108 [CrossRef][PubMed]
    [Google Scholar]
  64. Cardona ST, Mueller C, Valvano MA. Identification of essential operons in Burkholderia cenocepacia with a rhamnose inducible promoter. Appl Environ Microbiol 2006;72:2547–2555
    [Google Scholar]
  65. Juhas M, Stark M, von Mering C, Lumjiaktase P, Crook DW et al. High confidence prediction of essential genes in Burkholderia cenocepacia. PLoS One 2012;7:e40064 [CrossRef][PubMed]
    [Google Scholar]
  66. Mohamed YF, Valvano MA. A Burkholderia cenocepacia MurJ (MviN) homolog is essential for cell wall peptidoglycan synthesis and bacterial viability. Glycobiology 2014;24:564–576 [CrossRef]
    [Google Scholar]
  67. Ortega XP, Cardona ST, Brown AR, Loutet SA, Flannagan RS et al. A putative gene cluster for aminoarabinose biosynthesis is essential for Burkholderia cenocepacia viability. J Bacteriol 2007;189:3639–3644 [CrossRef][PubMed]
    [Google Scholar]
  68. Bloodworth RAM, Zlitni S, Brown ED, Cardona ST. An electron transfer flavoprotein is essential for viability and its depletion causes a rod-to-sphere change in Burkholderia cenocepacia. Microbiology 2015;161:1909–1920 [CrossRef]
    [Google Scholar]
  69. Gislason AS, Choy M, Bloodworth RA, Qu W, Stietz MS et al. Competitive growth enhances conditional growth mutant sensitivity to antibiotics and exposes a two-component system as an emerging antibacterial target in Burkholderia cenocepacia. Antimicrob Agents Chemother 2017;2016: [CrossRef]
    [Google Scholar]
  70. Winsor GL, Khaira B, Van Rossum T, Lo R, Whiteside MD et al. The Burkholderia genome database: facilitating flexible queries and comparative analyses. Bioinformatics 2008;24:2803–2804 [CrossRef]
    [Google Scholar]
  71. Caspi R, Billington R, Ferrer L, Foerster H, Fulcher CA et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 2016;44:D471–D480 [CrossRef][PubMed]
    [Google Scholar]
  72. Higgins S, Sanchez-Contreras M, Gualdi S, Pinto-Carbó M, Carlier A et al. The essential genome of Burkholderia cenocepacia H111. J Bacteriol 2017;199:e00260-17 [CrossRef][PubMed]
    [Google Scholar]
  73. Onishi HR, Pelak BA, Gerckens LS, Silver LL, Kahan FM et al. Antibacterial agents that inhibit lipid A biosynthesis. Science 1996;274:980–982 [CrossRef][PubMed]
    [Google Scholar]
  74. Tomasz A. The mechanism of the irreversible antimicrobial effects of penicillins: how the beta-lactam antibiotics kill and lyse bacteria. Annu Rev Microbiol 1979;33:113–137 [CrossRef][PubMed]
    [Google Scholar]
  75. Moskowitz SM, Ernst RK, Miller SI. PmrAB, a two-component regulatory system of Pseudomonas aeruginosa that modulates resistance to cationic antimicrobial peptides and addition of aminoarabinose to lipid A. J Bacteriol 2004;186:575–579 [CrossRef][PubMed]
    [Google Scholar]
  76. Raetz CR, Reynolds CM, Trent MS, Bishop RE. Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 2007;76:295–329 [CrossRef][PubMed]
    [Google Scholar]
  77. Wang X, Quinn PJ. Endotoxins: lipopolysaccharides of gram-negative bacteria. Subcell Biochem 2010;53:3–25
    [Google Scholar]
  78. Zhou Z, Ribeiro AA, Lin S, Cotter RJ, Miller SI et al. Lipid A modifications in polymyxin-resistant Salmonella typhimurium: PMRA-dependent 4-amino-4-deoxy-L-arabinose, and phosphoethanolamine incorporation. J Biol Chem 2001;276:43111–43121
    [Google Scholar]
  79. Loutet S, Valvano MA. Extreme antimicrobial peptide and polymyxin B resistance in the genus Burkholderia. Front Cell Infect Microbiol 2011;1:6 [CrossRef]
    [Google Scholar]
  80. Elsbach P, Weiss J. The bactericidal/permeability-increasing protein (BPI), a potent element in host-defense against Gram-negative bacteria and lipopolysaccharide. Immunobiology 1993;187:417–429 [CrossRef]
    [Google Scholar]
  81. Russell AB, Leroux M, Hathazi K, Agnello DM, Ishikawa T et al. Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 2013;496:508–512 [CrossRef]
    [Google Scholar]
  82. Wright GC, Weiss J, Kim KS, Verheij H, Elsbach P. Bacterial phospholipid hydrolysis enhances the destruction of Escherichia coli ingested by rabbit neutrophils. Role of cellular and extracellular phospholipases. J Clin Invest 1990;85:1925–1935 [CrossRef]
    [Google Scholar]
  83. Harvat EM, Zhang YM, Tran CV, Zhang Z, Frank MW et al. Lysophospholipid flipping across the Escherichia coli inner membrane catalyzed by a transporter (LplT) belonging to the major facilitator superfamily. J Biol Chem 2005;280:12028–12034 [CrossRef][PubMed]
    [Google Scholar]
  84. Siritapetawee J, Prinz H, Krittanai C, Suginta W. Expression and refolding of Omp38 from Burkholderia pseudomallei and Burkholderia thailandensis, and its function as a diffusion porin. Biochem J 2004;384:609–617 [CrossRef]
    [Google Scholar]
  85. Siritapetawee J, Prinz H, Samosornsuk W, Ashley RH, Suginta W. Functional reconstitution, gene isolation and topology modelling of porins from Burkholderia pseudomallei and Burkholderia thailandensis. Biochem J 2004;377:579–587 [CrossRef]
    [Google Scholar]
  86. Zhang YJ, Ioerger TR, Huttenhower C, Long JE, Sassetti CM et al. Global assessment of genomic regions required for growth in Mycobacterium tuberculosis. PLoS Pathog 2012;8:e1002946 [CrossRef][PubMed]
    [Google Scholar]
  87. Lee DG, Urbach JM, Wu G, Liberati NT, Feinbaum RL et al. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 2006;7:R90 [CrossRef]
    [Google Scholar]
  88. Yu Y, Kim HS, Chua H, Lin C, Sim S et al. Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis. BMC Microbiol 2006;6:46 [CrossRef]
    [Google Scholar]
  89. Centers for Disease Control and Prevention (CDC), Department of Health and Human Services (HHS) Possession, use, and transfer of select agents and toxins; biennial review of the list of select agents and toxins and enhanced biosafety requirements. Final rule. Fed Regist 2017;82:6278–6294[PubMed]
    [Google Scholar]
  90. Chewapreecha C, Holden MTG, Vehkala M, Välimäki N, Yang Z et al. Global and regional dissemination and evolution of Burkholderia pseudomallei. Nat Microbiol 2017;2:16263 [CrossRef]
    [Google Scholar]
  91. Glass MB, Gee JE, Steigerwalt AG, Cavuoti D, Barton T et al. Pneumonia and septicemia caused by Burkholderia thailandensis in the United States. J Clin Microbiol 2006;44:4601–4604 [CrossRef]
    [Google Scholar]
  92. Harley VS, Dance DA, Drasar BS, Tovey G. Effects of Burkholderia pseudomallei and other Burkholderia species on eukaryotic cells in tissue culture. Microbios 1998;96:71–93
    [Google Scholar]
  93. Hasselbring BM, Patel MK, Schell MA. Dictyostelium discoideum as a model system for identification of Burkholderia pseudomallei virulence factors. Infect Immun 2011;79:2079–2088 [CrossRef][PubMed]
    [Google Scholar]
  94. Hamad MA, di Lorenzo F, Molinaro A, Valvano MA. Aminoarabinose is essential for lipopolysaccharide export and intrinsic antimicrobial peptide resistance in Burkholderia cenocepacia. Mol Microbiol 2012;85:962–974 [CrossRef][PubMed]
    [Google Scholar]
  95. Lin Y, Bogdanov M, Tong S, Guan Z, Zheng L. Substrate selectivity of lysophospholipid transporter LplT involved in membrane phospholipid remodeling in Escherichia coli. J Biol Chem 2016;291:2136–2149 [CrossRef]
    [Google Scholar]
  96. Arunmanee W, Pathania M, Solovyova AS, Le Brun AP, Ridley H et al. Gram-negative trimeric porins have specific LPS binding sites that are essential for porin biogenesis. Proc Natl Acad Sci USA 2016;113:E5034E5043 [CrossRef]
    [Google Scholar]
  97. Hancock RE. Resistance mechanisms in Pseudomonas aeruginosa and other nonfermentative gram-negative bacteria. Clin Infect Dis 1998;27 Suppl 1:S93–S99 [CrossRef][PubMed]
    [Google Scholar]
  98. Pagès J-M, James CE, Winterhalter M. The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. Nat Rev Microbiol 2008;6:893–903 [CrossRef]
    [Google Scholar]
  99. Blake KL, O'Neill AJ. Transposon library screening for identification of genetic loci participating in intrinsic susceptibility and acquired resistance to antistaphylococcal agents. J Antimicrob Chemother 2013;68:12–16 [CrossRef][PubMed]
    [Google Scholar]
  100. Santa Maria JP, Sadaka A, Moussa SH, Brown S, Zhang YJ et al. Compound-gene interaction mapping reveals distinct roles for Staphylococcus aureus teichoic acids. Proc Natl Acad Sci USA 2014;111:12510–12515 [CrossRef][PubMed]
    [Google Scholar]
  101. Shan Y, Lazinski D, Rowe S, Camilli A, Lewis K. Genetic basis of persister tolerance to aminoglycosides in Escherichia coli. MBio 2015;6:e00078-15 [CrossRef][PubMed]
    [Google Scholar]
  102. Chantratita N, Rholl DA, Sim B, Wuthiekanun V, Limmathurotsakul D et al. Antimicrobial resistance to ceftazidime involving loss of penicillin-binding protein 3 in Burkholderia pseudomallei. Proc Natl Acad Sci USA 2011;108:17165–17170 [CrossRef][PubMed]
    [Google Scholar]
  103. Pradenas GA, Myers JN, Torres AG. Characterization of the Burkholderia cenocepacia TonB mutant as a potential live attenuated vaccine. Vaccines 2017;5:33 [CrossRef][PubMed]
    [Google Scholar]
  104. Titball RW, Burtnick MN, Bancroft GJ, Brett P. Burkholderia pseudomallei and Burkholderia mallei vaccines: are we close to clinical trials?. Vaccine 2017;35:5981–5989 [CrossRef]
    [Google Scholar]
  105. Semler DD, Goudie AD, Finlay WH, Dennis JJ. Aerosol phage therapy efficacy in Burkholderia cepacia complex respiratory infections. Antimicrob Agents Chemother 2014;58:4005–4013 [CrossRef]
    [Google Scholar]
  106. Guang-Han O, Leang-Chung C, Vellasamy KM, Mariappan V, Li-Yen C et al. Experimental phage therapy for Burkholderia pseudomallei infection. PLoS One 2016;11:e0158213 [CrossRef][PubMed]
    [Google Scholar]
  107. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010;5:e11147 [CrossRef][PubMed]
    [Google Scholar]
  108. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011;12:402 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000140
Loading
/content/journal/mgen/10.1099/mgen.0.000140
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Supplementary File 2

Most Cited This Month

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