Resistance phenotypes mediated by aminoacyl-phosphatidylglycerol synthases

Journal of Bacteriology

Volumn 194, Issue 6, 2012, Pages 1401-1416

  Arendt, Wiebke ^a   Hebecker, Stefanie ^a   Jäger, Sonja ^a   Nimtz, Manfred ^b   Moser, Jürgen ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINOACYLASE; AMPICILLIN; BETA LACTAM ANTIBIOTIC; CEFSULODIN; COLISTIN; DNA FRAGMENT; LYSINE; OXACILLIN; PHOSPHATIDYLGLYCEROL; POLYLYSINE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTAMINE SULFATE;

AMINO ACID SUBSTITUTION; AMINOACYLATION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACILLUS ANTHRACIS; BACILLUS LICHENIFORMIS; BACILLUS THURINGIENSIS; BACTERIAL STRAIN; BURKHOLDERIA PHYMATUM; CAULOBACTER CRESCENTUS; CLOSTRIDIUM PERFRINGENS; ENTEROCOCCUS FAECIUM; ENZYME SPECIFICITY; GENETIC RESISTANCE; KINEOCOCCUS RADIOTOLERANS; LIPID ANALYSIS; LIPID COMPOSITION; LISTERIA MONOCYTOGENES; METHANOSARCINA BARKERI; MINIMUM INHIBITORY CONCENTRATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPEN READING FRAME; PAENIBACILLUS POLYMYXA; PHENOTYPE; PHYLOGENETIC TREE CONSTRUCTION METHOD; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS PUTIDA; RHIZOBIUM RADIOBACTER; RHIZOBIUM TROPICI; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS THERMOPHILUS;

ALANINE; AMINOACYLTRANSFERASES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; LYSINE; MICROBIAL SENSITIVITY TESTS; PHOSPHATIDYLGLYCEROLS; PHYLOGENY; PSEUDOMONAS AERUGINOSA; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84857981317     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06576-11     Document Type: Article

References (97)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403- 410.
2. Alvarez-Ortega C, Wiegand I, Olivares J, Hancock RE, Martinez JL. 2011. The intrinsic resistome of Pseudomonas aeruginosa to beta-lactams. Virulence 2:144 -146.
3. Andrews JM. 2001. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48(Suppl 1):5-16.
4. Aspedon A, Groisman EA. 1996. The antibacterial action of protamine: evidence for disruption of cytoplasmic membrane energization in Salmonella typhimurium. Microbiology 142(Pt 12):3389 -3397.
5. Bagwell CE, et al. 2008. Survival in nuclear waste, extreme resistance, and potential applications gleaned from the genome sequence of Kineococcus radiotolerans SRS30216. PLoS One 3:e3878.
6. Brazas MD, Hancock RE. 2005. Using microarray gene signatures to elucidate mechanisms of antibiotic action and resistance. Drug Discov. Today 10:1245-1252.
7. Coakley RD, et al. 2003. Abnormal surface liquid pH regulation by cultured cystic fibrosis bronchial epithelium. Proc. Natl. Acad. Sci. U. S. A. 100:16083-16088.
8. Conrad RS, Gilleland HE, Jr. 1981. Lipid alterations in cell envelopes of polymyxin-resistant Pseudomonas aeruginosa isolates. J. Bacteriol. 148: 487-497.
9. Conte M, Aliberti F, Fucci L, Piscopo M. 2007. Antimicrobial activity of various cationic molecules on foodborne pathogens. World J. Microbiol. Biotechnol. 23:1679 -1683.
10. Contreras I, Shapiro L, Henry S. 1978. Membrane phospholipid composition of Caulobacter crescentus. J. Bacteriol. 135:1130 -1136.
11. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188 -1190.
12. Davies J, Spiegelman GB, Yim G. 2006. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 9:445- 453.
13. Delorme C. 2008. Safety assessment of dairy microorganisms: Streptococcus thermophilus. Int. J. Food Microbiol. 126:274 -277.
14. Deppenmeier U, et al. 2002. The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea. J. Mol. Microbiol. Biotechnol. 4:453- 461.
15. Dowhan W, Bogdanov M. 2002. Chapter 1 functional roles of lipids in membranes, p 1-35. In Dennis JEV, Vance E (ed), New comprehensive biochemistry, vol 36. Elsevier, Amsterdam, The Netherlands.
16. Elliott GN, et al. 2007. Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol. 173:168 -180.
17. Enoch DA, Bygott JM, Daly ML, Karas JA. 2007. Daptomycin. J. Infect. 55:205-213.
18. Epand RF, Maloy L, Ramamoorthy A, Epand RM. 2010. Amphipathic helical cationic antimicrobial peptides promote rapid formation of crystalline states in the presence of phosphatidylglycerol: lipid clustering in anionic membranes. Biophys. J. 98:2564 -2573.
19. Ernst CM, et al. 2009. The bacterial defensin resistance protein MprF consists of separable domains for lipid lysinylation and antimicrobial peptide repulsion. PLoS Pathog. 5:e1000660.
20. Fischer W, Leopold K. 1999. Polar lipids of four Listeria species containing L-lysylcardiolipin, a novel lipid structure, and other unique phospholipids. Int. J. Syst. Bacteriol. 49:653- 662.
21. Fonseca AP, Sousa JC. 2007. Effect of shear stress on growth, adhesion and biofilm formation of Pseudomonas aeruginosa with antibioticinduced morphological changes. Int. J. Antimicrob. Agents 30:236 -241.
22. Friedman L, Alder JD, Silverman JA. 2006. Genetic changes that correlate with reduced susceptibility to daptomycin in Staphylococcus aureus. Antimicrob. Agents Chemother. 50:2137-2145.
23. Grau FH, Wilson PW. 1962. Physiology of nitrogen fixation by Bacillus polymyxa. J. Bacteriol. 83:490-496.
24. Hachmann AB, Angert ER, Helmann JD. 2009. Genetic analysis of factors affecting susceptibility of Bacillus subtilis to daptomycin. Antimicrob. Agents Chemother. 53:1598 -1609.
25. Hachmann AB, et al. 2011. Reduction in membrane phosphatidylglycerol content leads to daptomycin resistance in Bacillus subtilis. Antimicrob. Agents Chemother. 55:4326-4337.
26. Hancock RE, Brinkman FS. 2002. Function of Pseudomonas porins in uptake and efflux. Annu. Rev. Microbiol. 56:17-38.
27. Hancock RE, Woodruff WA. 1988. Roles of porin and beta-lactamase in beta-lactam resistance of Pseudomonas aeruginosa. Rev. Infect. Dis. 10: 770-775.
28. Hartmann W, Galla HJ. 1978. Binding of polylysine to charged bilayer membranes: molecular organization of a lipid.peptide complex. Biochim. Biophys. Acta 509:474-490.
29. Harwood CR, Cutting SM. 1990. Modern microbiological methods: molecular biological methods for Bacillus subtilis. Wiley & Sons, Chichester, United Kingdom.
30. Hebecker S, et al. 2011. Alanyl-phosphatidylglycerol synthase: mechanism of substrate recognition during tRNA-dependent lipid modification in Pseudomonas aeruginosa. Mol. Microbiol. 80:935-950.
31. Heydorn A, et al. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395-2407.
32. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77- 86.
33. Hoang TT, Kutchma AJ, Becher A, Schweizer HP. 2000. Integrationproficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43:59 -72.
34. Houtsmuller UM, van Deenen L. 1963. Identification of a bacterial phospholipid as an O-ornithine ester of phosphatidyl glycerol. Biochim. Biophys. Acta 70:211-213.
35. Houtsmuller UM, van Deenen LL. 1965. On the amino acid esters of phosphatidyl glycerol from bacteria. Biochim. Biophys. Acta 106:564- 576.
36. Ibrahim MA, Griko N, Junker M, Bulla LA. 2010. Bacillus thuringiensis: a genomics and proteomics perspective. Bioeng. Bugs 1:31-50.
37. Irie Y, et al. 2010. Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Mol. Microbiol. 78:158 -172.
38. Johansen C, Verheul A, Gram L, Gill T, Abee T. 1997. Protamineinduced permeabilization of cell envelopes of Gram-positive and Gramnegative bacteria. Appl. Environ. Microbiol. 63:1155-1159.
39. Jones DE, Smith JD. 1979. Phospholipids of the differentiating bacterium Caulobacter crescentus. Can. J. Biochem. 57:424-428.
40. Jones T, et al. 2008. Failures in clinical treatment of Staphylococcus aureus infection with daptomycin are associated with alterations in surface charge, membrane phospholipid asymmetry, and drug binding. Antimicrob. Agents Chemother. 52:269 -278.
41. Julian K, et al. 2007. Characterization of a daptomycin-nonsusceptible vancomycin-intermediate Staphylococcus aureus strain in a patient with endocarditis. Antimicrob. Agents Chemother. 51:3445-3448.
42. Jung D, Powers JP, Straus SK, Hancock RE. 2008. Lipid-specific binding of the calcium-dependent antibiotic daptomycin leads to changes in lipid polymorphism of model membranes. Chem. Phys. Lipids 154:120 -128.
43. Klein S, et al. 2009. Adaptation of Pseudomonas aeruginosa to various conditions includes tRNA-dependent formation of alanylphosphatidylglycerol. Mol. Microbiol. 71:551-565.
44. Koch C, Hoiby N. 2000. Diagnosis and treatment of cystic fibrosis. Respiration 67:239 -247.
45. Koehler TM. 2009. Bacillus anthracis physiology and genetics. Mol. Aspects Med. 30:386 -396.
46. Koga Y. 2011. Early evolution of membrane lipids: how did the lipid divide occur? J. Mol. Evol. 72:274 -282.
47. Komatsuzawa H, et al. 2001. Cloning and sequencing of the gene, fmtC, which affects oxacillin resistance in methicillin-resistant Staphylococcus aureus. FEMS Microbiol. Lett. 203:49 -54.
48. Koo SP, Bayer AS, Yeaman MR. 2001. Diversity in antistaphylococcal mechanisms among membrane-targeting antimicrobial peptides. Infect. Immun. 69:4916-4922.
49. Koprivnjak T, Peschel A. 2011. Bacterial resistance mechanisms against host defense peptides. Cell. Mol. Life Sci. 68:2243-2254.
50. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
51. Letunic I, Bork P. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127-128.
52. Li M, et al. 2009. Staphylococcus aureus mutant screen reveals interaction of the human antimicrobial peptide dermcidin with membrane phospholipids. Antimicrob. Agents Chemother. 53:4200-4210.
53. Lim LM, et al. 2010. Resurgence of colistin: a review of resistance, toxicity, pharmacodynamics, and dosing. Pharmacotherapy 30:1279 -1291.
54. Lopez D, Kolter R. 2010. Functional microdomains in bacterial membranes. Genes Dev. 24:1893-1902.
55. Lyczak JB, Cannon CL, Pier GB. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194 -222.
56. MacFarlane MG. 1962. Characterization of lipoamino-acids as O-aminoacid esters of phosphatidyl-glycerol. Nature 196:136 -138.
57. Maeder DL, et al. 2006. The Methanosarcina barkeri genome: comparative analysis with Methanosarcina acetivorans and Methanosarcina mazei reveals extensive rearrangement within methanosarcinal genomes. J. Bacteriol. 188:7922-7931.
58. Maloney E, et al. 2011. Alterations in phospholipid catabolism in Mycobacterium tuberculosis lysX mutant. Front. Microbiol. 2:19.
59. Maloney E, et al. 2009. The two-domain LysX protein of Mycobacterium tuberculosis is required for production of lysinylated phosphatidylglycerol and resistance to cationic antimicrobial peptides. PLoS Pathog. 5:e1000534.
60. Mishra NN, et al. 2009. Analysis of cell membrane characteristics of in vitro-selected daptomycin-resistant strains of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 53:2312-2318.
61. Mogi T, Kita K. 2009. Gramicidin S and polymyxins: the revival of cationic cyclic peptide antibiotics. Cell. Mol. Life Sci. 66:3821-3826.
62. Muraih JK, Pearson A, Silverman J, Palmer M. 2011. Oligomerization of daptomycin on membranes. Biochim. Biophys. Acta 1808:1154 -1160.
63. Nestorovich EM, Danelon C, Winterhalter M, Bezrukov SM. 2002. Designed to penetrate: time-resolved interaction of single antibiotic molecules with bacterial pores. Proc. Natl. Acad. Sci. U.S.A. 99:9789 -9794.
64. Nishi H, Komatsuzawa H, Fujiwara T, McCallum N, Sugai M. 2004. Reduced content of lysyl-phosphatidylglycerol in the cytoplasmic membrane affects susceptibility to moenomycin, as well as vancomycin, gentamicin, and antimicrobial peptides, in Staphylococcus aureus. Antimicrob. Agents Chemother. 48:4800-4807.
65. Peschel A, et al. 2001. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with L-lysine. J. Exp. Med. 193:1067-1076.
66. Raza W, Xang W, Shen Q-R. 2008. Paenibacillus polymyxa: antibiotics, hydrolytic enzymes and hazard assessment. J. Plant Pathol. 90: 419 - 430.
67. Reasoner DJ, Geldreich EE. 1985. A new medium for the enumeration and subculture of bacteria from potable water. Appl. Environ. Microbiol. 49:1-7.
68. Reeve WG, et al. 2006. The Sinorhizobium medicae WSM419 lpiA gene is transcriptionally activated by FsrR and required to enhance survival in lethal acid conditions. Microbiology 152:3049 -3059.
69. Riou M, et al. 2010. In vivo development of antimicrobial resistance in Pseudomonas aeruginosa strains isolated from the lower respiratory tract of intensive care unit patients with nosocomial pneumonia and receiving antipseudomonal therapy. Int. J. Antimicrob. Agents 36: 513-522.
70. Rompf A, et al. 1998. Regulation of Pseudomonas aeruginosa hemF and hemN by the dual action of the redox response regulators Anr and Dnr. Mol. Microbiol. 29:985-997.
71. Rossetti FF, et al. 2004. Interaction of poly(L-lysine)-g-poly(ethylene glycol) with supported phospholipid bilayers. Biophys. J. 87:1711-1721.
72. Roy H. 2009. Tuning the properties of the bacterial membrane with aminoacylated phosphatidylglycerol. IUBMB Life 61:940 -953.
73. Roy H, Ibba M. 2009. Broad range amino acid specificity of RNAdependent lipid remodeling by multiple peptide resistance factors. J. Biol. Chem. 284:29677-29683.
74. Roy H, Ibba M. 2008. Monitoring Lys-tRNALys phosphatidylglycerol transferase activity. Methods 44:164 -169.
75. Roy H, Ibba M. 2008. RNA-dependent lipid remodeling by bacterial multiple peptide resistance factors. Proc. Natl. Acad. Sci. U.S.A. 105:4667- 4672.
76. Sacre MM, El Mashak EM, Tocanne JF. 1977. A monolayer (π,ΔV) study of the ionic properties of alanylphosphatidylglycerol: effects of pH and ions. Chem. Phys Lipids 20:305-318.
77. Samant S, Hsu FF, Neyfakh AA, Lee H. 2009. The Bacillus anthracis protein MprF is required for synthesis of lysylphosphatidylglycerols and for resistance to cationic antimicrobial peptides. J. Bacteriol. 191:1311- 1319.
78. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
79. Schreiber K, et al. 2006. Anaerobic survival of Pseudomonas aeruginosa by pyruvate fermentation requires an Usp-type stress protein. J. Bacteriol. 188:659-668.
80. Sievers S, et al. 2010. Changing the phospholipid composition of Staphylococcus aureus causes distinct changes in membrane proteome and membrane-sensory regulators. Proteomics 10:1685-1693.
81. Soboh F, Khoury AE, Zamboni AC, Davidson D, Mittelman MW. 1995. Effects of ciprofloxacin and protamine sulfate combinations against catheter-associated Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 39:1281-1286.
82. Sohlenkamp C, et al. 2007. The lipid lysyl-phosphatidylglycerol is present in membranes of Rhizobium tropici CIAT899 and confers increased resistance to polymyxin B under acidic growth conditions. Mol. Plant Microbe Interact. 20:1421-1430.
83. Staubitz P, Neumann H, Schneider T, Wiedemann I, Peschel A. 2004. MprF-mediated biosynthesis of lysylphosphatidylglycerol, an important determinant in staphylococcal defensin resistance. FEMS Microbiol. Lett. 231:67-71.
84. Stover CK, et al. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959 -964.
85. Strateva T, Yordanov D. 2009. Pseudomonas aeruginosa-a phenomenon of bacterial resistance. J. Med. Microbiol. 58:1133-1148.
86. Taylor JR. 1997. An introduction to error analysis: the study of uncertainties in physical measurements, 2nd ed. University Science Books, Sausalito, CA.
87. Thedieck K, et al. 2006. The MprF protein is required for lysinylation of phospholipids in listerial membranes and confers resistance to cationic antimicrobial peptides (CAMPs) on Listeria monocytogenes. Mol. Microbiol. 62:1325-1339.
88. Thoma S, Schobert M. 2009. An improved Escherichia coli donor strain for diparental mating. FEMS Microbiol. Lett. 294:127-132.
89. Tocanne JF, Ververgaert PH, Verkleij AJ, van Deenen LL. 1974. A monolayer and freeze-etching study of charged phospholipids. II. Ionic properties of mixtures of phosphatidylglycerol and lysylphosphatidylglycerol. Chem. Phys Lipids 12:220 -231.
90. van Delden C, Iglewski BH. 1998. Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg. Infect. Dis. 4:551-560.
91. Veith B, et al. 2004. The complete genome sequence of Bacillus licheniformis DSM13, an organism with great industrial potential. J. Mol. Microbiol. Biotechnol. 7:204 -211.
92. Vidal S, Bredin J, Pages JM, Barbe J. 2005. Beta-lactam screening by specific residues of the OmpF eyelet. J. Med. Chem. 48:1395-1400.
93. Wenzel M, Bandow JE. 2011. Proteomic signatures in antibiotic research. Proteomics 11:3256 -3268.
94. Wright AJ. 1999. The penicillins. Mayo Clin. Proc. 74:290 -307.
95. Yoshimura F, Nikaido H. 1985. Diffusion of beta-lactam antibiotics through the porin channels of Escherichia coli K-12. Antimicrob. Agents Chemother. 27:84 -92.
96. Yousef AE, Carlstrom C. 2003. Food microbiology: a laboratory manual. John Wiley & Sons, Hoboken, NJ.
97. Zasloff M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415:389 -395.