1887

Abstract

Purpose. The presence of alginate-overproducing (Alg) strains of Pseudomonas aeruginosa in cystic fibrosis patients is indicative of chronic infection. The Alg phenotype is generally due to a mutation in the mucA gene, encoding an innermembrane protein that sequesters AlgT/U, the alginate-specific sigma factor. AlgT/U release from the anti-sigma factor MucA is orchestrated via a complex cascade called regulated intramembrane proteolysis. The goal of this study is to identify new players involved in the regulation of alginate production.

Methodology. Previously, a mutant with a second-site suppressor of alginate production (sap), sap27, was isolated from the constitutively Alg PDO300 that harbours the mucA22 allele. A cosmid from a P. aeruginosa minimum tiling path library was identified via en masse complementation of sap27. The cosmid was transposon mutagenized to map the contributing gene involved in the alginate production. The identified gene was sequenced in sap27 along with algT/U, mucA, algO and mucP. The role of the novel gene was explored using precise in-frame algO and algW deletion mutants of PAO1 and PDO300.

Results/Key findings. The gene responsible for restoring the mucoid phenotype was mapped to lptD encoding an outer-membrane protein. However, the sequencing of sap27 revealed a mutation in algO, but not in lptD. In addition, we demonstrate that lipopolysaccharide transport protein D (LptD)-dependent alginate production requires AlgW in PAO1 and AlgO in PDO300.

Conclusion. LptD plays a specific role in alginate production. Our findings suggest that there are two pathways for the production of alginate in P. aeruginosa, one involving AlgW in the wild-type, and one involving AlgO in the mucA22 mutant.

Keyword(s): Imp , LptE , OptP , OstA , PdxA and SurA
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2018-06-20
2024-04-20
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References

  1. Bayes HK, Ritchie N, Irvine S, Evans TJ. A murine model of early Pseudomonas aeruginosa lung disease with transition to chronic infection. Sci Rep 2016; 6:35838 [View Article]
    [Google Scholar]
  2. McAvoy MJ, Newton V, Paull A, Morgan J, Gacesa P et al. Isolation of mucoid strains of Pseudomonas aeruginosa from non-cystic-fibrosis patients and characterisation of the structure of their secreted alginate. J Med Microbiol 1989; 28:183–189 [View Article]
    [Google Scholar]
  3. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG et al. Common virulence factors for bacterial pathogenicity in plants and animals. Science 1995; 268:1899–1902 [View Article][PubMed]
    [Google Scholar]
  4. Young VM. Pseudomonas Aeruginosa: Ecological Aspects and Patient Colonization New York: Raven Press; 1977
    [Google Scholar]
  5. Bodey GP, Bolivar R, Fainstein V, Jadeja L. Infections caused by Pseudomonas aeruginosa. Rev Infect Dis 1983; 5:279–313 [View Article][PubMed]
    [Google Scholar]
  6. National action plan for combating antibiotic resistant bacteria: National Institute of Health; 2015 Available from www.cdc.gov/drugresistance/federal-engagement-in-ar/national-strategy/index.html
  7. 2016 Cystic Fibrosis Foundation Patient Registry: Cystic Fibrosis Foundation; 2016 Available from www.cff.org/our-research/CF-patient-registry/2015-patient-registry-annual-data-report.pdf
  8. Hoiby N, Flensborg EW, Beck B, Friis B, Jacobsen SV et al. Pseudomonas aeruginosa infection in cystic fibrosis. Diagnostic and prognostic significance of Pseudomonas aeruginosa precipitins determined by means of crossed immunoelectrophoresis. Scand J Respir Dis 1977; 58:65–79
    [Google Scholar]
  9. Tummler B, Bosshammer J, Breitenstein S, Brockhausen I, Gudowius P et al. Infections in Pseudomonas aeruginosa in patients with cystic fibrosis. Behring Inst Mitt 1997; 98:249–255
    [Google Scholar]
  10. Doggett RG, Harrison GM, Carter RE. Mucoid Pseudomonas aeruginosa in patients with chronic illnesses. Lancet 1971; 1:236–237
    [Google Scholar]
  11. Doggett RG, Harrison GM. Pseudomonas aeruginosa: immune status in patients with cystic fibrosis. Infect Immun 1972; 6:628–635
    [Google Scholar]
  12. Govan JR, Sarasola P, Taylor DJ, Tatnell PJ, Russell NJ et al. Isolation of a mucoid alginate producing Pseudomonas aeruginosa strain from the equine guttural pouch. J Clin Microbiol 1992; 30:595–599
    [Google Scholar]
  13. Grobe S, Wingender J, Trüper HG. Characterization of mucoid Pseudomonas aeruginosa strains isolated from technical water systems. J Appl Bacteriol 1995; 79:94–102 [View Article][PubMed]
    [Google Scholar]
  14. Hoiby N. Prevalence of mucoid strains of Pseudomonas aeruginosa in bacteriological specimens from patients with cystic fibrosis and patients with other diseases. Acta Pathol Microbiol Scand Suppl 1975; 83:549–552 [View Article][PubMed]
    [Google Scholar]
  15. Pedersen SS, Hoiby N, Espersen F, Koch C. Role of alginate in infection with mucoid Pseudomonas aeruginosa in cystic fibrosis. Thorax 1992; 47:6–13 [View Article]
    [Google Scholar]
  16. Kulczycki LL, Murphy TM, Bellanti JA. Pseudomonas colonization in cystic fibrosis. A study of 160 patients. JAMA 1978; 240:30–34
    [Google Scholar]
  17. Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR et al. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-γ-mediated macrophage killing. J Immunol 2005; 175:7512–7518 [View Article][PubMed]
    [Google Scholar]
  18. Govan JR, Fyfe JA. Mucoid Pseudomonas aeruginosa and cystic fibrosis: resistance of the mucoid from to carbenicillin, flucloxacillin and tobramycin and the isolation of mucoid variants in vitro. J Antimicrob Chemother 1978; 4:233–240 [View Article][PubMed]
    [Google Scholar]
  19. Hodges NA, Gordon CA. Protection of Pseudomonas aeruginosa against ciprofloxacin and beta-lactams by homologous alginate. Antimicrob Agents Chemother 1991; 35:2450–2452 [View Article]
    [Google Scholar]
  20. Oliver AM, Weir DM. Inhibition of bacterial binding to mouse macrophages by Pseudomonas alginate. J Clin Lab Immunol 1983; 10:221–224
    [Google Scholar]
  21. Mathee K, Ciofu O, Sternberg C, Lindum PW, Campbell JI et al. Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 1999; 145:1349–1357 [View Article][PubMed]
    [Google Scholar]
  22. Schwarzmann S, Boring JR. Antiphagocytic effect of slime from a mucoid strain of Pseudomonas aeruginosa. Infect Immun 1971; 3:762–767
    [Google Scholar]
  23. Boucher JC, Yu H, Mudd MH, Deretic V. Mucoid Pseudomonas aeruginosa in cystic fibrosis: characterization of muc mutations in clinical isolates and analysis of clearance in a mouse model of respiratory infection. Infect Immun 1997; 65:3838–3846
    [Google Scholar]
  24. Bragonzi A, Worlitzsch D, Pier GB, Timpert P, Ulrich M et al. Nonmucoid Pseudomonas aeruginosa expresses alginate in the lungs of patients with cystic fibrosis and in a mouse model. J Infect Dis 2005; 192:410–419 [View Article][PubMed]
    [Google Scholar]
  25. Pier GB, Boyer D, Preston M, Coleman FT, Llosa N et al. Human monoclonal antibodies to Pseudomonas aeruginosa alginate that protect against infection by both mucoid and nonmucoid strains. J Immunol 2004; 173:5671–5678 [View Article][PubMed]
    [Google Scholar]
  26. Song Z et al. Pseudomonas aeruginosa alginate is refractory to Th1 immune response and impedes host immune clearance in a mouse model of acute lung infection. J Med Microbiol 2003; 52:731–740 [View Article]
    [Google Scholar]
  27. Yu H, Hanes M, Chrisp CE, Boucher JC, Deretic V. Microbial pathogenesis in cystic fibrosis: pulmonary clearance of mucoid Pseudomonas aeruginosa and inflammation in a mouse model of repeated respiratory challenge. Infect Immun 1998; 66:280–288
    [Google Scholar]
  28. Terry JM, Pina SE, Mattingly SJ. Environmental conditions which influence mucoid conversion in Pseudomonas aeruginosa PA01. Infect Immun 1991; 59:471–477
    [Google Scholar]
  29. Speert DP, Farmer SW, Campbell ME, Musser JM, Selander RK et al. Conversion of Pseudomonas aeruginosa to the phenotype characteristic of strains from patients with cystic fibrosis. J Clin Microbiol 1990; 28:188–194
    [Google Scholar]
  30. Evans LR, Linker A. Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J Bacteriol 1973; 116:915–924
    [Google Scholar]
  31. Devault JD, Kimbara K, Chakrabarty AM. Pulmonary dehydration and infection in cystic fibrosis: evidence that ethanol activates alginate gene expression and induction of mucoidy in Pseudomonas aeruginosa. Mol Microbiol 1990; 4:737–745 [View Article][PubMed]
    [Google Scholar]
  32. Damron FH, Davis MR, Withers TR, Ernst RK, Goldberg JB et al. Vanadate and triclosan synergistically induce alginate production by Pseudomonas aeruginosa strain PAO1. Mol Microbiol 2011; 81:554–570 [View Article][PubMed]
    [Google Scholar]
  33. Hassett DJ. Anaerobic production of alginate by Pseudomonas aeruginosa: alginate restricts diffusion of oxygen. J Bacteriol 1996; 178:7322–7325 [View Article]
    [Google Scholar]
  34. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 2002; 109:317–325 [View Article]
    [Google Scholar]
  35. Baynham PJ, Wozniak DJ. Identification and characterization of AlgZ, an AlgT-dependent DNA-binding protein required for Pseudomonas aeruginosa algD transcription. Mol Microbiol 1996; 22:97–108 [View Article]
    [Google Scholar]
  36. Goldberg JB, Gorman WL, Flynn JL, Ohman DE. A mutation in algN permits trans activation of alginate production by algT in Pseudomonas species. J Bacteriol 1993; 175:1303–1308 [View Article][PubMed]
    [Google Scholar]
  37. Kato J, Chakrabarty AM. Purification of the regulatory protein AlgR1 and its binding in the far upstream region of the algD promoter in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 1991; 88:1760–1764 [View Article][PubMed]
    [Google Scholar]
  38. Leech AJ, Sprinkle A, Wood L, Wozniak DJ, Ohman DE. The NtrC family regulator AlgB, which controls alginate biosynthesis in mucoid Pseudomonas aeruginosa, binds directly to the algD promoter. J Bacteriol 2008; 190:581–589 [View Article][PubMed]
    [Google Scholar]
  39. Mohr CD, Leveau JH, Krieg DP, Hibler NS, Deretic V. AlgR-binding sites within the algD promoter make up a set of inverted repeats separated by a large intervening segment of DNA. J Bacteriol 1992; 174:6624–6633 [View Article][PubMed]
    [Google Scholar]
  40. Wozniak DJ, Ohman DE. Pseudomonas aeruginosa AlgB, a two-component response regulator of the NtrC family, is required for algD transcription. J Bacteriol 1991; 173:1406–1413 [View Article][PubMed]
    [Google Scholar]
  41. Goldberg JB, Ohman DE. Construction and characterization of Pseudomonas aeruginosa algB mutants: role of algB in high-level production of alginate. J Bacteriol 1987; 169:1593–1602 [View Article]
    [Google Scholar]
  42. Goldberg JB, Dahnke T. Pseudomonas aeruginosa AlgB, which modulates the expression of alginate, is a member of the NtrC subclass of prokaryotic regulators. Mol Microbiol 1992; 6:59–66 [View Article][PubMed]
    [Google Scholar]
  43. Ma S, Wozniak DJ, Ohman DE. Identification of the histidine protein kinase KinB in Pseudomonas aeruginosa and its phosphorylation of the alginate regulator AlgB. J Biol Chem 1997; 272:17952–17960 [View Article][PubMed]
    [Google Scholar]
  44. Whitchurch CB, Alm RA, Mattick JS. The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 1996; 93:9839–9843 [View Article][PubMed]
    [Google Scholar]
  45. Yu H, Mudd M, Boucher JC, Schurr MJ, Deretic V. Identification of the algZ gene upstream of the response regulator algR and its participation in control of alginate production in Pseudomonas aeruginosa. J Bacteriol 1997; 179:187–193 [View Article]
    [Google Scholar]
  46. Damron FH, Qiu D, Yu HD. The Pseudomonas aeruginosa sensor kinase KinB negatively controls alginate production through AlgW-dependent MucA proteolysis. J Bacteriol 2009; 191:2285–2295 [View Article][PubMed]
    [Google Scholar]
  47. Ma S, Selvaraj U, Ohman DE, Quarless R, Hassett DJ et al. Phosphorylation-independent activity of the response regulators AlgB and AlgR in promoting alginate biosynthesis in mucoid Pseudomonas aeruginosa. J Bacteriol 1998; 180:956–968
    [Google Scholar]
  48. Baynham PJ, Brown AL, Hall LL, Wozniak DJ. Pseudomonas aeruginosa AlgZ, a ribbon-helix-helix DNA-binding protein, is essential for alginate synthesis and algD transcriptional activation. Mol Microbiol 1999; 33:1069–1080 [View Article][PubMed]
    [Google Scholar]
  49. Hay ID, Remminghorst U, Rehm BH. MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl Environ Microbiol 2009; 75:1110–1120 [View Article][PubMed]
    [Google Scholar]
  50. Devries CA, Ohman DE. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J Bacteriol 1994; 176:6677–6687 [View Article][PubMed]
    [Google Scholar]
  51. Hershberger CD, Ye RW, Parsek MR, Xie ZD, Chakrabarty AM. The algT (algU) gene of Pseudomonas aeruginosa, a key regulator involved in alginate biosynthesis, encodes an alternative sigma factor (sigma E). Proc Natl Acad Sci USA 1995; 92:7941–7945 [View Article]
    [Google Scholar]
  52. Lonetto M, Gribskov M, Gross CA. The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol 1992; 174:3843–3849 [View Article]
    [Google Scholar]
  53. Martin DW, Holloway BW, Deretic V. Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor. J Bacteriol 1993; 175:1153–1164 [View Article]
    [Google Scholar]
  54. Wozniak DJ, Ohman DE. Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB, and algD reveals a hierarchy of alginate gene expression which is modulated by algT. J Bacteriol 1994; 176:6007–6014 [View Article][PubMed]
    [Google Scholar]
  55. Devries CA, Ohman DE. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J Bacteriol 1994; 176:6677–6687 [View Article][PubMed]
    [Google Scholar]
  56. Wozniak DJ, Sprinkle AB, Baynham PJ. Control of Pseudomonas aeruginosa algZ expression by the alternative sigma factor AlgT. J Bacteriol 2003; 185:7297–7300 [View Article][PubMed]
    [Google Scholar]
  57. Yin Y, Damron FH, Withers TR, Pritchett CL, Wang X et al. Expression of mucoid induction factor MucE is dependent upon the alternate sigma factor AlgU in Pseudomonas aeruginosa. BMC Microbiol 2013; 13:232 [View Article][PubMed]
    [Google Scholar]
  58. Martin DW, Schurr MJ, Mudd MH, Govan JR, Holloway BW et al. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc Natl Acad Sci USA 1993; 90:8377–8381 [View Article][PubMed]
    [Google Scholar]
  59. Mathee K, McPherson CJ, Ohman DE. Posttranslational control of the algT (algU)-encoded sigma22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN). J Bacteriol 1997; 179:3711–3720 [View Article]
    [Google Scholar]
  60. Xie ZD, Hershberger CD, Shankar S, Ye RW, Chakrabarty AM. Sigma factor-anti-sigma factor interaction in alginate synthesis: inhibition of AlgT by MucA. J Bacteriol 1996; 178:4990–4996 [View Article][PubMed]
    [Google Scholar]
  61. Bragonzi A, Wiehlmann L, Klockgether J, Cramer N, Worlitzsch D et al. Sequence diversity of the mucABD locus in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 2006; 152:3261–3269 [View Article][PubMed]
    [Google Scholar]
  62. Boucher JC, Martinez-Salazar J, Schurr MJ, Mudd MH, Yu H et al. Two distinct loci affecting conversion to mucoidy in Pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease HtrA. J Bacteriol 1996; 178:511–523 [View Article]
    [Google Scholar]
  63. Martin DW, Schurr MJ, Mudd MH, Deretic V. Differentiation of Pseudomonas aeruginosa into the alginate-producing form: inactivation of mucB causes conversion to mucoidy. Mol Microbiol 1993; 9:497–506 [View Article][PubMed]
    [Google Scholar]
  64. Schurr MJ, Yu H, Martinez-Salazar JM, Boucher JC, Deretic V. Control of AlgU, a member of the sigma E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J Bacteriol 1996; 178:4997–5004 [View Article][PubMed]
    [Google Scholar]
  65. Brown MS, Ye J, Rawson RB, Goldstein JL. Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 2000; 100:391–398
    [Google Scholar]
  66. Wood LF, Ohman DE. Use of cell wall stress to characterize σ22 (AlgT/U) activation by regulated proteolysis and its regulon in Pseudomonas aeruginosa. Mol Microbiol 2009; 72:183–201 [View Article][PubMed]
    [Google Scholar]
  67. Cezairliyan BO, Sauer RT. Control of Pseudomonas aeruginosa AlgW protease cleavage of MucA by peptide signals and MucB. Mol Microbiol 2009; 72:368–379 [View Article]
    [Google Scholar]
  68. Qiu D, Eisinger VM, Rowen DW, Yu HD. Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 2007; 104:8107–8112 [View Article][PubMed]
    [Google Scholar]
  69. Damron FH, Yu HD. Pseudomonas aeruginosa MucD regulates the alginate pathway through activation of MucA degradation via MucP proteolytic activity. J Bacteriol 2011; 193:286–291 [View Article][PubMed]
    [Google Scholar]
  70. Qiu D, Eisinger VM, Head NE, Pier GB, Yu HD. ClpXP proteases positively regulate alginate overexpression and mucoid conversion in Pseudomonas aeruginosa. Microbiology 2008; 154:2119–2130 [View Article][PubMed]
    [Google Scholar]
  71. Yin Y, Withers TR, Wang X, Yu HD. Evidence for sigma factor competition in the regulation of alginate production by Pseudomonas aeruginosa. PLoS One 2013; 8:e72329 [View Article][PubMed]
    [Google Scholar]
  72. Wood LF, Ohman DE. Independent regulation of MucD, an HtrA-like protease in Pseudomonas aeruginosa, and the role of its proteolytic motif in alginate gene regulation. J Bacteriol 2006; 188:3134–3137 [View Article][PubMed]
    [Google Scholar]
  73. Boucher JC, Schurr MJ, Yu H, Rowen DW, Deretic V. Pseudomonas aeruginosa in cystic fibrosis: role of mucC in the regulation of alginate production and stress sensitivity. Microbiology 1997; 143:3473–3480 [View Article]
    [Google Scholar]
  74. Ohman DE, Mathee K, McPherson CJ, Devries CA, Ma S et al. Regulation of the alginate (algD) operon in Pseudomonas aeruginosa. Molecularbiology of Pseudomonads Washington, DC: American Society for Microbiology; 1996 pp. 472–483
    [Google Scholar]
  75. Reiling SA et al. Prc protease promotes mucoidy in mucA mutants of Pseudomonas aeruginosa. Microbiology 2005; 151:2251–2261 [View Article]
    [Google Scholar]
  76. Sautter R, Ramos D, Schneper L, Ciofu O, Wassermann T et al. A complex multilevel attack on Pseudomonas aeruginosa algT/U expression and algT/U activity results in the loss of alginate production. Gene 2012; 498:242–253 [View Article][PubMed]
    [Google Scholar]
  77. Ponting CP. Evidence for PDZ domains in bacteria, yeast, and plants. Protein Sci 1997; 6:464–468 [View Article][PubMed]
    [Google Scholar]
  78. Min KB, Lee KM, Oh YT, Yoon SS. Nonmucoid conversion of mucoid Pseudomonas aeruginosa induced by sulfate-stimulated growth. FEMS Microbiol Lett 2014; 360:157–166 [View Article][PubMed]
    [Google Scholar]
  79. Ohman DE, Chakrabarty AM. Genetic mapping of chromosomal determinants for the production of the exopolysaccharide alginate in a Pseudomonas aeruginosa cystic fibrosis isolate. Infect Immun 1981; 33:142–148
    [Google Scholar]
  80. Govan JR, Fyfe JA, McMillan C. The instability of mucoid Pseudomonas aeruginosa: fluctuation test and improved stability of the mucoid form in shaken culture. J Gen Microbiol 1979; 110:229–232 [View Article][PubMed]
    [Google Scholar]
  81. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: a Laboratory Manual, 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1989
    [Google Scholar]
  82. 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 [View Article][PubMed]
    [Google Scholar]
  83. Finan TM, Kunkel B, De Vos GF, Signer ER. Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol 1986; 167:66–72 [View Article]
    [Google Scholar]
  84. Huang B, Whitchurch CB, Croft L, Beatson SA, Mattick JS. A minimal tiling path cosmid library for functional analysis of the Pseudomonas aeruginosa PAO1 genome. Microb Comp Genomics 2000; 5:189–203 [View Article]
    [Google Scholar]
  85. Knutson CA, Jeanes A. A new modification of the carbazole analysis: application to heteropolysaccharides. Anal Biochem 1968; 24:470–481 [View Article][PubMed]
    [Google Scholar]
  86. Shanks RM, Caiazza NC, Hinsa SM, Toutain CM, O'Toole GA. Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl Environ Microbiol 2006; 72:5027–5036 [View Article][PubMed]
    [Google Scholar]
  87. Shanks RM, Kadouri DE, MacEachran DP, O'Toole GA. New yeast recombineering tools for bacteria. Plasmid 2009; 62:88–97 [View Article][PubMed]
    [Google Scholar]
  88. Choi KH, Kumar A, Schweizer HP. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 2006; 64:391–397 [View Article][PubMed]
    [Google Scholar]
  89. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH et al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985; 150:76–85 [View Article]
    [Google Scholar]
  90. Horton RM, Cai ZL, Ho SN, Pease LR. Gene-splicing by overlap extension – tailor-made genes using the polymerase chain-reaction. Biotechniques 1990; 8:528–525
    [Google Scholar]
  91. Rietsch A, Vallet-Gely I, Dove SL, Mekalanos JJ. ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 2005; 102:8006–8011 [View Article][PubMed]
    [Google Scholar]
  92. Balasubramanian D, Schneper L, Merighi M, Smith R, Narasimhan G et al. The regulatory repertoire of Pseudomonas aeruginosa AmpC ß-lactamase regulator AmpR includes virulence genes. PLoS One 2012; 7:e34067 [View Article][PubMed]
    [Google Scholar]
  93. Brencic A, McFarland KA, McManus HR, Castang S, Mogno I et al. The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol Microbiol 2009; 73:434–445 [View Article][PubMed]
    [Google Scholar]
  94. Winsor GL, Griffiths EJ, Lo R, Dhillon BK, Shay JA et al. Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database. Nucleic Acids Res 2016; 44:D646–D653 [View Article][PubMed]
    [Google Scholar]
  95. Vertommen D, Ruiz N, Leverrier P, Silhavy TJ, Collet JF. Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics. Proteomics 2009; 9:2432–2443 [View Article][PubMed]
    [Google Scholar]
  96. Lazar SW, Almiron M, Tormo A, Kolter R. Role of the Escherichia coli SurA protein in stationary-phase survival. J Bacteriol 1998; 180:5704–5711
    [Google Scholar]
  97. Rouvière PE, Gross CA. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev 1996; 10:3170–3182 [View Article][PubMed]
    [Google Scholar]
  98. Tormo A, Almirón M, Kolter R. surA, an Escherichia coli gene essential for survival in stationary phase. J Bacteriol 1990; 172:4339–4347 [View Article][PubMed]
    [Google Scholar]
  99. Banks J, Cane DE. Biosynthesis of vitamin B6: direct identification of the product of the PdxA-catalyzed oxidation of 4-hydroxy-l-threonine-4-phosphate using electrospray ionization mass spectrometry. Bioorg Med Chem Lett 2004; 14:1633–1636 [View Article]
    [Google Scholar]
  100. Laber B, Maurer W, Scharf S, Stepusin K, Schmidt FS. Vitamin B6 biosynthesis: formation of pyridoxine 5'-phosphate from 4-(phosphohydroxy)-L-threonine and 1-deoxy-D-xylulose-5-phosphate by PdxA and PdxJ protein. FEBS Lett 1999; 449:45–48 [View Article][PubMed]
    [Google Scholar]
  101. Chimalakonda G, Ruiz N, Chng SS, Garner RA, Kahne D et al. Lipoprotein LptE is required for the assembly of LptD by the beta-barrel assembly machine in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 2011; 108:2492–2497 [View Article][PubMed]
    [Google Scholar]
  102. Chng SS, Ruiz N, Chimalakonda G, Silhavy TJ, Kahne D. Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc Natl Acad Sci USA 2010; 107:5363–5368 [View Article][PubMed]
    [Google Scholar]
  103. Grabowicz M, Yeh J, Silhavy TJ. Dominant negative lptE mutation that supports a role for LptE as a plug in the LptD barrel. J Bacteriol 2013; 195:1327–1334 [View Article][PubMed]
    [Google Scholar]
  104. Jahn M, Vorpahl C, Hübschmann T, Harms H, Müller S. Copy number variability of expression plasmids determined by cell sorting and droplet digital PCR. Microb Cell Fact 2016; 15:211 [View Article][PubMed]
    [Google Scholar]
  105. Werneburg M, Zerbe K, Juhas M, Bigler L, Stalder U et al. Inhibition of lipopolysaccharide transport to the outer membrane in Pseudomonas aeruginosa by peptidomimetic antibiotics. Chembiochem 2012; 13:1767–1775 [View Article][PubMed]
    [Google Scholar]
  106. Bos MP, Tefsen B, Geurtsen J, Tommassen J. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci USA 2004; 101:9417–9422 [View Article][PubMed]
    [Google Scholar]
  107. Braun M, Silhavy TJ. Imp/OstA is required for cell envelope biogenesis in Escherichia coli. Mol Microbiol 2002; 45:1289–1302 [View Article][PubMed]
    [Google Scholar]
  108. Dartigalongue C, Missiakas D, Raina S. Characterization of the Escherichia coli sigma E regulon. J Biol Chem 2001; 276:20866–20875 [View Article][PubMed]
    [Google Scholar]
  109. Abe S, Okutsu T, Nakajima H, Kakuda N, Ohtsu I et al. n-Hexane sensitivity of Escherichia coli due to low expression of imp/ostA encoding a 87-kDa minor protein associated with the outer membrane. Microbiology 2003; 149:1265–1273 [View Article][PubMed]
    [Google Scholar]
  110. Aono R, Negishi T, Aibe K, Inoue A, Horikoshi K. Mapping of organic solvent tolerance gene ostA in Escherichia coli K-12. Biosci Biotechnol Biochem 1994; 58:1231–1235 [View Article][PubMed]
    [Google Scholar]
  111. Sampson BA, Misra R, Benson SA. Identification and characterization of a new gene of Escherichia coli K-12 involved in outer membrane permeability. Genetics 1989; 122:491–501[PubMed]
    [Google Scholar]
  112. Sperandeo P, Cescutti R, Villa R, di Benedetto C, Candia D et al. Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J Bacteriol 2007; 189:244–253 [View Article][PubMed]
    [Google Scholar]
  113. Charlson ES, Werner JN, Misra R. Differential effects of yfgL mutation on Escherichia coli outer membrane proteins and lipopolysaccharide. J Bacteriol 2006; 188:7186–7194 [View Article][PubMed]
    [Google Scholar]
  114. Balibar CJ, Grabowicz M. Mutant Alleles of lptD increase the permeability of Pseudomonas aeruginosa and define determinants of intrinsic resistance to antibiotics. Antimicrob Agents Chemother 2016; 60:845–854 [View Article][PubMed]
    [Google Scholar]
  115. Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ et al. Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 2006; 103:11754–11759 [View Article][PubMed]
    [Google Scholar]
  116. Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ. Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 2008; 105:5537–5542 [View Article][PubMed]
    [Google Scholar]
  117. Zielinski NA, Chakrabarty AM, Berry A. Characterization and regulation of the Pseudomonas aeruginosa algC gene encoding phosphomannomutase. J Biol Chem 1991; 266:9754–9763[PubMed]
    [Google Scholar]
  118. Olvera C, Goldberg JB, Sánchez R, Soberón-Chávez G. The Pseudomonas aeruginosa algC gene product participates in rhamnolipid biosynthesis. FEMS Microbiol Lett 1999; 179:85–90 [View Article][PubMed]
    [Google Scholar]
  119. Ma L, Wang J, Wang S, Anderson EM, Lam JS et al. Synthesis of multiple Pseudomonas aeruginosa biofilm matrix exopolysaccharides is post-transcriptionally regulated. Environ Microbiol 2012; 14:1995–2005 [View Article][PubMed]
    [Google Scholar]
  120. Lazar SW, Kolter R. SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol 1996; 178:1770–1773 [View Article][PubMed]
    [Google Scholar]
  121. Dong H, Xiang Q, Gu Y, Wang Z, Paterson NG et al. Structural basis for outer membrane lipopolysaccharide insertion. Nature 2014; 511:52–56 [View Article][PubMed]
    [Google Scholar]
  122. Qiao S, Luo Q, Zhao Y, Zhang XC, Huang Y. Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature 2014; 511:108–111 [View Article][PubMed]
    [Google Scholar]
  123. Wollmann P, Zeth K. The structure of RseB: a sensor in periplasmic stress response of E. coli. J Mol Biol 2007; 372:927–941 [View Article][PubMed]
    [Google Scholar]
  124. Wilken C, Kitzing K, Kurzbauer R, Ehrmann M, Clausen T. Crystal structure of the DegS stress sensor: How a PDZ domain recognizes misfolded protein and activates a protease. Cell 2004; 117:483–494[PubMed]
    [Google Scholar]
  125. Lima S, Guo MS, Chaba R, Gross CA, Sauer RT. Dual molecular signals mediate the bacterial response to outer-membrane stress. Science 2013; 340:837–841 [View Article][PubMed]
    [Google Scholar]
  126. Srinivas N, Jetter P, Ueberbacher BJ, Werneburg M, Zerbe K et al. Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa. Science 2010; 327:1010–1013 [View Article][PubMed]
    [Google Scholar]
  127. Bojkovic J, Richie DL, Six DA, Rath CM, Sawyer WS et al. Characterization of an Acinetobacter baumannii lptD Deletion strain: permeability defects and response to inhibition of lipopolysaccharide and fatty acid biosynthesis. J Bacteriol 2015; 198:731–741 [View Article][PubMed]
    [Google Scholar]
  128. Zha Z, Li C, Li W, Ye Z, Pan J. LptD is a promising vaccine antigen and potential immunotherapeutic target for protection against Vibrio species infection. Sci Rep 2016; 6:38577 [View Article][PubMed]
    [Google Scholar]
  129. Zielke RA, Wierzbicki IH, Baarda BI, Gafken PR, Soge OO et al. Proteomics-driven antigen discovery for development of vaccines against gonorrhea. Mol Cell Proteomics 2016; 15:2338–2355 [View Article][PubMed]
    [Google Scholar]
  130. Vecchietti D, di Silvestre D, Miriani M, Bonomi F, Marengo M et al. Analysis of Pseudomonas aeruginosa cell envelope proteome by capture of surface-exposed proteins on activated magnetic nanoparticles. PLoS One 2012; 7:e51062 [View Article][PubMed]
    [Google Scholar]
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