Advertisement

Participation of Bacterial Lipases, Sphingomyelinases, and Phospholipases in Gram-Negative Bacterial Pathogenesis

  • Lauren A. Hinkel
  • Matthew J. WargoEmail author
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Lipid membranes are a ubiquitous property of cellular life. Within the context of infection, Gram-negative bacteria modify and/or destroy host membranes to access intracellular niches or release nutrients. They also modify their own membranes to survive host antimicrobial assault and antibiotic treatment. The key players in the membrane-altering events are secreted sphingomyelinases, lipases, and phospholipases, whose enzymatic activities are important for pathogenesis in a number of Gram-negative bacterial species. Here, we present these lipid-active enzymes based on proposed pathogenic function to emphasize their biological roles during infection.

Notes

Acknowledgments

Research related to this topic was supported by grants from the NIH National Institute of Allergy and Infectious Diseases (R01 AI103003, R03 AI117069) to MJW. LAH was supported by an institutional training grant from the National Institute of Allergy and Infectious Diseases (T32 AI055402).

References

  1. Abbaspour N, Hurrell R, Kelishadi R (2014) Review on iron and its importance for human health. J Res Med Sci 19:164–174PubMedPubMedCentralGoogle Scholar
  2. Abdou L, Chou HT, Haas D, Lu CD (2011) Promoter recognition and activation by the global response regulator CbrB in Pseudomonas aeruginosa. J Bacteriol 193:2784–2792PubMedPubMedCentralCrossRefGoogle Scholar
  3. Albus AM, Pesci EC, Runyen-Janecky LJ, West SE, Iglewski BH (1997) Vfr controls quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179(12):3928–3935.  https://doi.org/10.1128/jb.179.12.3928-3935.1997PubMedPubMedCentralCrossRefGoogle Scholar
  4. Anba J, Bidaud M, Vasil ML, Lazdunski A (1990) Nucleotide sequence of the Pseudomonas aeruginosa phoB gene, the regulatory gene for the phosphate regulon. J Bacteriol 172(8):4685–4689.  https://doi.org/10.1128/jb.172.8.4685-4689.1990PubMedPubMedCentralCrossRefGoogle Scholar
  5. Aragon V, Rossier O, Cianciotto NP (2002) Legionella pneumophila genes that encode lipase and phospholipase C activities. Microbiology 148:2223–2231PubMedCrossRefPubMedCentralGoogle Scholar
  6. Aurass P, Pless B, Rydzewski K, Holland G, Bannert N, Flieger A (2009) bdhA-patD operon as a virulence determinant, revealed by a novel large-scale approach for identification of Legionella pneumophila mutants defective for amoeba infection. Appl Environ Microbiol 75:4506–4515PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aurass P, Schlegel M, Metwally O, Harding CR, Schroeder GN, Frankel G, Flieger A (2013) The Legionella pneumophila Dot/Icm-secreted effector PlcC/CegC1 together with PlcA and PlcB promotes virulence and belongs to a novel zinc metallophospholipase C family present in bacteria and fungi. J Biol Chem 288(16):11080–11092.  https://doi.org/10.1074/jbc.M112.426049PubMedPubMedCentralCrossRefGoogle Scholar
  8. Balasubramanian D, Schneper L, Kumari H, Mathee K (2013) A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res 41(1):1–20.  https://doi.org/10.1093/nar/gks1039PubMedCrossRefPubMedCentralGoogle Scholar
  9. Banerji S, Bewersdorff M, Hermes B, Cianciotto NP, Flieger A (2005) Characterization of the major secreted zinc metalloprotease- dependent glycerophospholipid:cholesterol acyltransferase, PlaC, of Legionella pneumophila. Infect Immun 73:2899–2909PubMedPubMedCentralCrossRefGoogle Scholar
  10. Banerji S, Aurass P, Flieger A (2008) The manifold phospholipases a of legionella pneumophila - identification, export, regulation, and their link to bacterial virulence. Int J Med Microbiol 298:169–181PubMedCrossRefPubMedCentralGoogle Scholar
  11. Barker AP, Vasil AI, Filloux A, Ball G, Wilderman PJ, Vasil ML (2004) A novel extracellular phospholipase C of Pseudomonas aeruginosa is required for phospholipid chemotaxis. Mol Microbiol 53:1089–1098PubMedCrossRefPubMedCentralGoogle Scholar
  12. Berka RM, Vasil ML (1982) Phospholipase C (heat-labile hemolysin) of Pseudomonas aeruginosa: purification and preliminary characterization. J Bacteriol 152(1):239–245. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/6811552PubMedPubMedCentralGoogle Scholar
  13. Bleves S, Viarre V, Salacha R, Michel GP, Filloux A, Voulhoux R (2010) Protein secretion systems in Pseudomonas aeruginosa: a wealth of pathogenic weapons. Int J Med Microbiol 300(8):534–543.  https://doi.org/10.1016/j.ijmm.2010.08.005PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bleves S, Sana TG, Voulhoux R (2014) The target cell genus does not matter. Trends Microbiol 22:304–306PubMedCrossRefPubMedCentralGoogle Scholar
  15. Borgeaud S, Metzger LC, Scrignari T, Blokesch M (2015) The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer. Science 347:63–67PubMedCrossRefPubMedCentralGoogle Scholar
  16. Bruggemann H, Hagman A, Jules M, Sismeiro O, Dillies MA, Gouyette C, Kunst F, Steinert M, Heuner K, Coppee JY, Buchrieser C (2006) Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of legionella pneumophila. Cell Microbiol 8:1228–1240PubMedCrossRefPubMedCentralGoogle Scholar
  17. Buckley JT, Halasa LN, MacIntyre S (1982) Purification and partial characterization of a bacterial phospholipid: cholesterol acyltransferase. J Biol Chem 257:3320–3325PubMedPubMedCentralGoogle Scholar
  18. Chen WW, Chao YJ, Chang WH, Chan JF, Hsu YH (2018) Phosphatidylglycerol incorporates into Cardiolipin to improve mitochondrial activity and inhibits inflammation. Sci Rep 8:4919PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cutter DL, Kreger AS (1990) Cloning and expression of the damselysin gene from Vibrio damsela. Infect Immun 58(1):266–268. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/2294056
  20. Dorrell N, Martino MC, Stabler RA, Ward SJ, Zhang ZW, McColm AA, … Wren BW (1999) Characterization of Helicobacter pylori PldA, a phospholipase with a role in colonization of the gastric mucosa. Gastroenterology 117(5):1098–1104.  https://doi.org/10.1016/s0016-5085(99)70394-xPubMedCrossRefPubMedCentralGoogle Scholar
  21. Dowling JN, Saha AK, Glew RH (1992) Virulence factors of the family Legionellaceae. Microbiol Rev 56:32–60PubMedPubMedCentralGoogle Scholar
  22. Driskell LO, Yu XJ, Zhang L, Liu Y, Popov VL, Walker DH, Tucker AM, Wood DO (2009) Directed mutagenesis of the Rickettsia prowazekii pld gene encoding phospholipase D. Infect Immun 77:3244–3248PubMedPubMedCentralCrossRefGoogle Scholar
  23. Durand E, Cambillau C, Cascales E, Journet L (2014) VgrG, Tae, Tle, and beyond: the versatile arsenal of type VI secretion effectors. Trends Microbiol 22:498–507PubMedCrossRefPubMedCentralGoogle Scholar
  24. Engel J, Eran Y (2011) Subversion of mucosal barrier polarity by Pseudomonas aeruginosa. Front Microbiol 2:114.  https://doi.org/10.3389/fmicb.2011.00114
  25. Fiester SE, Arivett BA, Schmidt RE, Beckett AC, Ticak T, Carrier MV, Ghosh R, Ohneck EJ, Metz ML, Sellin Jeffries MK, Actis LA (2016) Iron-regulated phospholipase C activity contributes to the Cytolytic activity and virulence of Acinetobacter baumannii. PLoS One 11:e0167068PubMedPubMedCentralCrossRefGoogle Scholar
  26. Flieger A, Gongab S, Faigle M, Mayer HA, Kehrer U, Mussotter J, Bartmann P, Neumeister B (2000) Phospholipase a secreted by Legionella pneumophila destroys alveolar surfactant phospholipids. FEMS Microbiol Lett 188:129–133PubMedCrossRefPubMedCentralGoogle Scholar
  27. Flieger A, Rydzewski K, Banerji S, Broich M, Heuner K (2004) Cloning and characterization of the gene encoding the major cell-associated phospholipase A of Legionella pneumophila, plaB, exhibiting hemolytic activity. Infect Immun 72(5):2648–2658.  https://doi.org/10.1128/iai.72.5.2648-2658.2004PubMedPubMedCentralCrossRefGoogle Scholar
  28. Flores-Diaz M, Monturiol-Gross L, Naylor C, Alape-Giron A, Flieger A (2016) Bacterial sphingomyelinases and phospholipases as virulence factors. Microbiol Mol Biol Rev 80:597–628PubMedPubMedCentralCrossRefGoogle Scholar
  29. Freeman JA, Ohl ME, Miller SI (2003) The Salmonella enterica serovar typhimurium translocated effectors SseJ and SifB are targeted to the salmonella-containing vacuole. Infect Immun 71:418–427PubMedPubMedCentralCrossRefGoogle Scholar
  30. Glasser JR, Mallampalli RK (2012) Surfactant and its role in the pathobiology of pulmonary infection. Microbes Infect 14:17–25PubMedCrossRefGoogle Scholar
  31. Grant KA, Belandia IU, Dekker N, Richardson PT, Park SF (1997) Molecular characterization of pldA, the structural gene for a phospholipase A from Campylobacter coli, and its contribution to cell-associated hemolysis. Infect Immun 65(4):1172–1180. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/9119448PubMedPubMedCentralGoogle Scholar
  32. Hammond JH, Dolben EF, Smith TJ, Bhuju S, Hogan DA (2015) Links between Anr and quorum sensing in Pseudomonas aeruginosa biofilms. J Bacteriol 197:2810–2820PubMedPubMedCentralCrossRefGoogle Scholar
  33. Holm BA, Keicher L, Liu MY, Sokolowski J, Enhorning G (1991) Inhibition of pulmonary surfactant function by phospholipases. J Appl Physiol (1985), 71(1):317–321.  https://doi.org/10.1152/jappl.1991.71.1.317CrossRefGoogle Scholar
  34. Homma H, Kobayashi T, Chiba N, Karasawa K, Mizushima H, Kudo I, Inoue K, Ikeda H, Sekiguchi M, Nojima S (1984) The DNA sequence encoding pldA gene, the structural gene for detergent-resistant phospholipase a of E. coli. J Biochem 96:1655–1664PubMedCrossRefGoogle Scholar
  35. Ingham AB, Pemberton JM (1995) A lipase of Aeromonas hydrophila showing nonhemolytic phospholipase C activity. Curr Microbiol 31(1):28–33. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7767226PubMedCrossRefGoogle Scholar
  36. Jackson AA, Gross MJ, Daniels EF, Hampton TH, Hammond JH, Vallet-Gely I, Dove SL, Stanton BA, Hogan DA (2013) Anr and its activation by PlcH activity in Pseudomonas aeruginosa host colonization and virulence. J Bacteriol 195:3093–3104PubMedPubMedCentralCrossRefGoogle Scholar
  37. Jacobs AC, Hood I, Boyd KL, Olson PD, Morrison JM, Carson S, … Dunman PM (2010) Inactivation of phospholipase D diminishes Acinetobacter baumannii pathogenesis. Infect Immun 78(5):1952–1962.  https://doi.org/10.1128/IAI.00889-09PubMedPubMedCentralCrossRefGoogle Scholar
  38. Jang KK, Lee ZW, Kim B, Jung YH, Han HJ, Kim MH, … Choi SH (2017) Identification and characterization of Vibrio vulnificus plpA encoding a phospholipase A2 essential for pathogenesis. J Biol Chem 292(41):17129–17143.  https://doi.org/10.1074/jbc.M117.791657PubMedPubMedCentralCrossRefGoogle Scholar
  39. Jiang F, Waterfield NR, Yang J, Yang G, Jin Q (2014) A Pseudomonas aeruginosa type VI secretion phospholipase D effector targets both prokaryotic and eukaryotic cells. Cell Host Microbe 15:600–610PubMedCrossRefGoogle Scholar
  40. Jones C, Allsopp L, Horlick J, Kulasekara H, Filloux A (2013) Subinhibitory concentration of kanamycin induces the Pseudomonas aeruginosa type VI secretion system. PLoS One 8:e81132PubMedPubMedCentralCrossRefGoogle Scholar
  41. Karlyshev AV, Oyston PC, Williams K, Clark GC, Titball RW, Winzeler EA, Wren BW (2001) Application of high-density array-based signature-tagged mutagenesis to discover novel Yersinia virulence-associated genes. Infect Immun 69(12):7810–7819.  https://doi.org/10.1128/IAI.69.12.7810-7819.2001PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kendall MM, Sperandio V (2016) What a dinner party! Mechanisms and functions of Interkingdom signaling in host-pathogen associations. MBio 7:e01748PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kerrinnes T, Young BM, Leon C, Roux CM, Tran L, Atluri VL, Winter MG, Tsolis RM (2015) Phospholipase A1 modulates the cell envelope phospholipid content of Brucella melitensis, contributing to polymyxin resistance and pathogenicity. Antimicrob Agents Chemother 59:6717–6724PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kida Y, Shimizu T, Kuwano K (2011) Cooperation between LepA and PlcH contributes to the in vivo virulence and growth of Pseudomonas aeruginosa in mice. Infect Immun 79:211–219PubMedCrossRefGoogle Scholar
  45. Kreger AS, Bernheimer AW, Etkin LA, Daniel LW (1987) Phospholipase D activity of Vibrio damsela cytolysin and its interaction with sheep erythrocytes. Infect Immun 55:3209–3212PubMedPubMedCentralGoogle Scholar
  46. Krol E, Becker A (2004) Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011. Mol Genet Genomics 272(1):1–17.  https://doi.org/10.1007/s00438-004-1030-8PubMedCrossRefGoogle Scholar
  47. Kulasekara BR, Kulasekara HD, Wolfgang MC, Stevens L, Frank DW, Lory S (2006) Acquisition and evolution of the exoU locus in Pseudomonas aeruginosa. J Bacteriol 188:4037–4050PubMedPubMedCentralCrossRefGoogle Scholar
  48. LaBauve AE, Wargo MJ (2014) Detection of host-derived sphingosine by Pseudomonas aeruginosa is important for survival in the murine lung. PLoS Pathog 10:e1003889PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lang C, Flieger A (2011) Characterisation of Legionella pneumophila phospholipases and their impact on host cells. Eur J Cell Biol 90:903–912.  https://doi.org/10.1016/j.ejcb.2010.12.003PubMedCrossRefPubMedCentralGoogle Scholar
  50. Lanotte P, Mereghetti L, Lejeune B, Massicot P, Quentin R (2003) Pseudomonas aeruginosa and cystic fibrosis: correlation between exoenzyme production and patient's clinical state. Pediatr Pulmonol 36:405–412PubMedCrossRefPubMedCentralGoogle Scholar
  51. LaRock DL, Brzovic PS, Levin I, Blanc MP, Miller SI (2012) A Salmonella typhimurium-translocated glycerophospholipid: cholesterol acyltransferase promotes virulence by binding to the RhoA protein switch regions. J Biol Chem 287(35):29654–29663.  https://doi.org/10.1074/jbc.M112.363598PubMedPubMedCentralCrossRefGoogle Scholar
  52. Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, Monack DM (2006) Genome-wide screen for salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2:e11PubMedPubMedCentralCrossRefGoogle Scholar
  53. Lery LM, Frangeul L, Tomas A, Passet V, Almeida AS, Bialek-Davenet S, Barbe V, Bengoechea JA, Sansonetti P, Brisse S, Tournebize R (2014) Comparative analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor. BMC Biol 12:41PubMedPubMedCentralCrossRefGoogle Scholar
  54. Li L, Mou X, Nelson DR (2013) Characterization of Plp, a phosphatidylcholine-specific phospholipase and hemolysin of Vibrio anguillarum. BMC Microbiol 13:271PubMedPubMedCentralCrossRefGoogle Scholar
  55. Liu L, Ye M, Li X, Li J, Deng Z, Yao YF, Ou HY (2017) Identification and characterization of an antibacterial type VI secretion system in the Carbapenem-resistant strain Klebsiella pneumoniae HS11286. Front Cell Infect Microbiol 7:442PubMedPubMedCentralCrossRefGoogle Scholar
  56. Ma L, Chen J, Liu R, Zhang XH, Jiang YA (2009) Mutation of rpoS gene decreased resistance to environmental stresses, synthesis of extracellular products and virulence of Vibrio anguillarum. FEMS Microbiol Ecol 70:130–136PubMedCrossRefGoogle Scholar
  57. Malinverni JC, Silhavy TJ (2009) An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane. Proc Natl Acad Sci U S A 106(19):8009–8014.  https://doi.org/10.1073/pnas.0903229106PubMedPubMedCentralCrossRefGoogle Scholar
  58. Massimelli MJ, Beassoni PR, Forrellad MA, Barra JL, Garrido MN, Domenech CE, Lisa AT (2005) Identification, cloning, and expression of Pseudomonas aeruginosa phosphorylcholine phosphatase gene. Curr Microbiol 50:251–256PubMedCrossRefGoogle Scholar
  59. May KL, Grabowicz M (2018) The bacterial outer membrane is an evolving antibiotic barrier. Proc Natl Acad Sci USA 115:8852–8854PubMedCrossRefGoogle Scholar
  60. May KL, Silhavy TJ (2018) The Escherichia coli phospholipase PldA regulates outer membrane homeostasis via lipid signaling. MBio 9(2).  https://doi.org/10.1128/mBio.00379-18
  61. Naka H, Hirono I, Aoki T (2007) Cloning and characterization of Photobacterium damselae ssp. piscicida phospholipase: an enzyme that shows haemolytic activity. J Fish Dis 30:681–690PubMedCrossRefGoogle Scholar
  62. Nguyen D, Emond MJ, Mayer-Hamblett N, Saiman L, Marshall BC, Burns JL (2007) Clinical response to azithromycin in cystic fibrosis correlates with in vitro effects on Pseudomonas aeruginosa phenotypes. Pediatr Pulmonol 42:533–541PubMedCrossRefGoogle Scholar
  63. Oglesby AG, Farrow JM 3rd, Lee JH, Tomaras AP, Greenberg EP, Pesci EC, Vasil ML (2008) The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J Biol Chem 283:15558–15567PubMedPubMedCentralCrossRefGoogle Scholar
  64. Oglesby-Sherrouse AG, Vasil ML (2010) Characterization of a heme-regulated non-coding RNA encoded by the prrF locus of Pseudomonas aeruginosa. PLoS One 5:e9930PubMedPubMedCentralCrossRefGoogle Scholar
  65. Oh WS, Im YS, Yeon KY, Yoon YJ, Kim JW (2007) Phosphate and carbon source regulation of alkaline phosphatase and phospholipase in Vibrio vulnificus. J Microbiol 45:311–317PubMedGoogle Scholar
  66. Ohlson MB, Fluhr K, Birmingham CL, Brumell JH, Miller SI (2005) SseJ deacylase activity by Salmonella enterica serovar typhimurium promotes virulence in mice. Infect Immun 73:6249–6259PubMedPubMedCentralCrossRefGoogle Scholar
  67. Ostroff RM, Vasil AI, Vasil ML (1990) Molecular comparison of a nonhemolytic and a hemolytic phospholipase C from Pseudomonas aeruginosa. J Bacteriol 172:5915–5923PubMedPubMedCentralCrossRefGoogle Scholar
  68. Pasteur L (1878) La Theorie des Germes. Comptes Rendus l’Academie des Science 86:1037–1043Google Scholar
  69. Powers MJ, Trent MS (2018) Phospholipid retention in the absence of asymmetry strengthens the outer membrane permeability barrier to last-resort antibiotics. Proc Natl Acad Sci USA 115(36):E8518–E8527.  https://doi.org/10.1073/pnas.1806714115CrossRefGoogle Scholar
  70. Ramirez JC, Fleiszig SM, Sullivan AB, Tam C, Borazjani R, Evans DJ (2012) Traversal of multilayered corneal epithelia by cytotoxic Pseudomonas aeruginosa requires the phospholipase domain of exoU. Invest Ophthalmol Vis Sci 53:448–453PubMedPubMedCentralCrossRefGoogle Scholar
  71. Reinhart AA, Powell DA, Nguyen AT, O'Neill M, Djapgne L, Wilks A, Ernst RK, Oglesby-Sherrouse AG (2015) The prrF-encoded small regulatory RNAs are required for iron homeostasis and virulence of Pseudomonas aeruginosa. Infect Immun 83:863–875PubMedPubMedCentralCrossRefGoogle Scholar
  72. Rock JL, Nelson DR (2006) Identification and characterization of a hemolysin gene cluster in Vibrio anguillarum. Infect Immun 74(5):2777–2786.  https://doi.org/10.1128/IAI.74.5.2777-2786.2006PubMedPubMedCentralCrossRefGoogle Scholar
  73. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475(7356):343–347.  https://doi.org/10.1038/nature10244PubMedPubMedCentralCrossRefGoogle Scholar
  74. Russell AB, LeRoux M, Hathazi K, Agnello DM, Ishikawa T, Wiggins PA, … Mougous JD (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496(7446):508–512.  https://doi.org/10.1038/nature12074PubMedPubMedCentralCrossRefGoogle Scholar
  75. Sana TG, Berni B, Bleves S (2016) The T6SSs of Pseudomonas aeruginosa strain PAO1 and their effectors: beyond bacterial-cell targeting. Front Cell Infect Microbiol 6:61PubMedPubMedCentralCrossRefGoogle Scholar
  76. Santos-Beneit F (2015) The pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:402PubMedPubMedCentralCrossRefGoogle Scholar
  77. Sato H, Frank DW (2014) Intoxication of host cells by the T3SS phospholipase ExoU: PI(4,5)P2-associated, cytoskeletal collapse and late phase membrane blebbing. PLoS One 9(7):e103127.  https://doi.org/10.1371/journal.pone.0103127PubMedPubMedCentralCrossRefGoogle Scholar
  78. Schlam D, Bagshaw RD, Freeman SA, Collins RF, Pawson T, Fairn GD, Grinstein S (2015) Phosphoinositide 3-kinase enables phagocytosis of large particles by terminating actin assembly through Rac/Cdc42 GTPase-activating proteins. Nat Commun 6:8623PubMedPubMedCentralCrossRefGoogle Scholar
  79. Schmiel DH, Miller VL (1999) Bacterial phospholipases and pathogenesis. Microbes Infect 1(13):1103–1112. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10572314PubMedCrossRefPubMedCentralGoogle Scholar
  80. Schroeder GN, Aurass P, Oates CV, Tate EW, Hartland EL, Flieger A, Frankel G (2015) Legionella pneumophila effector LpdA is a Palmitoylated phospholipase D virulence factor. Infect Immun 83:3989–4002PubMedPubMedCentralCrossRefGoogle Scholar
  81. Shaver CM, Hauser AR (2004) Relative contributions of Pseudomonas aeruginosa ExoU, ExoS, and ExoT to virulence in the lung. Infect Immun 72:6969–6977PubMedPubMedCentralCrossRefGoogle Scholar
  82. Shortridge VD, Lazdunski A, Vasil ML (1992) Osmoprotectants and phosphate regulate expression of phospholipase C in Pseudomonas aeruginosa. Mol Microbiol 6:863–871PubMedCrossRefPubMedCentralGoogle Scholar
  83. Son MS, Matthews WJ Jr, Kang Y, Nguyen DT, Hoang TT (2007) In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect Immun 75:5313–5324PubMedPubMedCentralCrossRefGoogle Scholar
  84. Spencer C, Brown HA (2015) Biochemical characterization of a Pseudomonas aeruginosa phospholipase D. Biochemistry 54(5):1208–1218.  https://doi.org/10.1021/bi501291tPubMedPubMedCentralCrossRefGoogle Scholar
  85. Stahl J, Bergmann H, Gottig S, Ebersberger I, Averhoff B (2015) Acinetobacter baumannii virulence is mediated by the concerted action of three phospholipases D. PLoS One 10:e0138360PubMedPubMedCentralCrossRefGoogle Scholar
  86. Stonehouse MJ, Cota-Gomez A, Parker SK, Martin WE, Hankin JA, Murphy RC, … Vasil ML (2002) A novel class of microbial phosphocholine-specific phospholipases C. Mol Microbiol 46(3):661–676.  https://doi.org/10.1046/j.1365-2958.2002.03194.xPubMedCrossRefPubMedCentralGoogle Scholar
  87. Terceti MS, Ogut H, Osorio CR (2016) Photobacterium damselae subsp. damselae, an emerging fish pathogen in the Black Sea: evidence of a multiclonal origin. Appl Environ Microbiol 82:3736–3745PubMedPubMedCentralCrossRefGoogle Scholar
  88. Thi Khanh Nhu N, Riordan DW, Do Hoang Nhu T, Thanh DP, Thwaites G, Huong Lan NP, Wren BW, Baker S, Stabler RA (2016) The induction and identification of novel Colistin resistance mutations in Acinetobacter baumannii and their implications. Sci Rep 6:28291PubMedPubMedCentralCrossRefGoogle Scholar
  89. Tielen P, Kuhn H, Rosenau F, Jaeger KE, Flemming HC, Wingender J (2013) Interaction between extracellular lipase LipA and the polysaccharide alginate of Pseudomonas aeruginosa. BMC Microbiol 13:159PubMedPubMedCentralCrossRefGoogle Scholar
  90. Tuanyok A, Tom M, Dunbar J, Woods DE (2006) Genome-wide expression analysis of Burkholderia pseudomallei infection in a hamster model of acute melioidosis. Infect Immun 74(10):5465–5476.  https://doi.org/10.1128/IAI.00737-06PubMedPubMedCentralCrossRefGoogle Scholar
  91. Vasil ML, Stonehouse MJ, Vasil AI, Wadsworth SJ, Goldfine H, Bolcome RE 3rd, Chan J (2009) A complex extracellular sphingomyelinase of Pseudomonas aeruginosa inhibits angiogenesis by selective cytotoxicity to endothelial cells. PLoS Pathog 5:e1000420PubMedPubMedCentralCrossRefGoogle Scholar
  92. Wang Z, Notter RH (1998) Additivity of protein and nonprotein inhibitors of lung surfactant activity. Am J Respir Crit Care Med 158(1) 28–35.  https://doi.org/10.1164/ajrccm.158.1.9709041PubMedCrossRefGoogle Scholar
  93. Wargo MJ (2013a) Choline catabolism to Glycine betaine contributes to Pseudomonas aeruginosa survival during murine lung infection. PLoS One 8(2):e56850.  https://doi.org/10.1371/journal.pone.0056850PubMedPubMedCentralCrossRefGoogle Scholar
  94. Wargo MJ (2013b) Homeostasis and catabolism of choline and glycine betaine: lessons from Pseudomonas aeruginosa. Appl Environ Microbiol 79:2112–2120PubMedPubMedCentralCrossRefGoogle Scholar
  95. Wargo MJ, Ho TC, Gross MJ, Whittaker LA, Hogan DA (2009) GbdR regulates Pseudomonas aeruginosa plcH and pchP transcription in response to choline catabolites. Infect Immun 77:1103–1111PubMedCrossRefPubMedCentralGoogle Scholar
  96. Wargo MJ, Gross MJ, Rajamani S, Allard JL, Lundblad LK, Allen GB, Vasil ML, Leclair LW, Hogan DA (2011) Hemolytic phospholipase C inhibition protects lung function during Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 184:345–354PubMedPubMedCentralCrossRefGoogle Scholar
  97. Whitworth T, Popov VL, Yu XJ, Walker DH, Bouyer DH (2005) Expression of the rickettsia prowazekii pld or tlyC gene in Salmonella enterica serovar typhimurium mediates phagosomal escape. Infect Immun 73:6668–6673PubMedPubMedCentralCrossRefGoogle Scholar
  98. Wilderman PJ, Vasil AI, Johnson Z, Vasil ML (2001) Genetic and biochemical analyses of a eukaryotic-like phospholipase D of Pseudomonas aeruginosa suggest horizontal acquisition and a role for persistence in a chronic pulmonary infection model. Mol Microbiol 39:291–303PubMedCrossRefPubMedCentralGoogle Scholar
  99. Winkler HH, Miller ET (1980) Phospholipase A activity in the hemolysis of sheep and human erythrocytes by Rickettsia prowazeki. Infect Immun 29(2):316–321. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/6783529PubMedPubMedCentralGoogle Scholar
  100. Yahr TL, Wolfgang MC (2006) Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol Microbiol 62(3):631–640.  https://doi.org/10.1111/j.1365-2958.2006.05412.xPubMedCrossRefPubMedCentralGoogle Scholar
  101. Yuan ZC, Zaheer R, Morton R, Finan TM (2006) Genome prediction of PhoB regulated promoters in Sinorhizobium meliloti and twelve proteobacteria. Nucleic Acids Res 34(9):2686–2697.  https://doi.org/10.1093/nar/gkl365PubMedPubMedCentralCrossRefGoogle Scholar
  102. Yun NR, Kim DM (2018) Vibrio vulnificus infection: a persistent threat to public health. Korean J Intern Med 33:1070–1078PubMedPubMedCentralCrossRefGoogle Scholar
  103. Zavaleta-Pastor M, Sohlenkamp C, Gao JL, Guan Z, Zaheer R, Finan TM, … Geiger O (2010) Sinorhizobium meliloti phospholipase C required for lipid remodeling during phosphorus limitation. Proc Natl Acad Sci U S A 107(1):302–307.  https://doi.org/10.1073/pnas.0912930107PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Microbiology & Molecular Genetics, Larner College of Medicine, College of Agriculture and Life SciencesUniversity of VermontBurlingtonUSA

Personalised recommendations