Bacterial Membrane Lipids: Where Do We Stand?

Annual Review of Microbiology

Volumn 57, Issue , 2003, Pages 203-224

  Cronan, John E ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

DNA replication; Fatty acids; Phospholipid function; Phospholipids; Protein modification

Indexed keywords

FATTY ACID; MEMBRANE LIPID; PHOSPHOLIPID;

BACTERIAL GENOME; BACTERIAL MEMBRANE; BACTERIAL METABOLISM; DNA REPLICATION; FATTY ACID METABOLISM; GENE MAPPING; GENOMICS; GROWTH INHIBITION; LIPOGENESIS; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN MODIFICATION; REVIEW; SPECIES DIFFERENTIATION; STEM CELL;

BIOLOGICAL TRANSPORT; CELL MEMBRANE; DNA REPLICATION; ESCHERICHIA COLI; LIPID BILAYERS; MEMBRANE LIPIDS; PHOSPHOLIPIDS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0242693130     PISSN: 00664227     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.micro.57.030502.090851     Document Type: Review

References (109)

1. Asai Y, Katayose Y, Hikita C, Ohta A, Shibuya I. 1989. Suppression of the lethal effect of acidic-phospholipid deficiency by defective formation of the major outer membrane lipoprotein in Escherichia coli. J. Bacteriol. 171:6867-69
2. Attard GS, Templer RH, Smith WS, Hunt AN, Jackowski S. 2000. Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress. Proc. Natl. Acad. Sci. USA 97:9032-36
3. Babinski KJ, Kanjilal SJ, Raetz CR. 2002. Accumulation of the lipid A precursor UDP-2,3-diacylglucosamine in an Escherichia coli mutant lacking the lpxH gene. J. Biol. Chem. 277:25947-56
4. Bibi E, Kaback HR. 1990. In vivo expression of the lacY gene in two segments leads to functional lac permease. Proc. Natl. Acad. Sci. USA 87:4325-29
5. Bogdanov M, Dowhan W. 1995. Phosphatidylethanolamine is required for in vivo function of the membrane-associated lactose permease of Escherichia coli. J. Biol. Chem. 270:732-39
6. Bogdanov M, Dowhan W. 1998. Phospholipid-assisted protein folding: Phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease. EMBO J. 17:5255-64
7. Bogdanov M, Heacock PN, Dowhan W. 2002. A polytopic membrane protein displays a reversible topology dependent on membrane lipid composition. EMBO J. 21:2107-16
8. Bogdanov M, Sun J, Kaback HR, Dowhan W. 1996. A phospholipid acts as a chaperone in assembly of a membrane transport protein. J. Biol. Chem. 271:11615-18
9. Brown AP, Coleman J, Tommey AM, Watson MD, Slabas AR. 1994. Isolation and characterisation of a maize cDNA that complements a 1-acyl sn-glycerol-3-phosphate acyltransferase mutant of Escherichia coli and encodes a protein which has similarities to other acyltransferases. Plant Mol. Biol. 26:211-23
10. Bulawa CE, Raetz CR. 1984. Isolation and characterization of Escherichia coli strains defective in CDP-diglyceride hydrolase. J. Biol. Chem. 259:11257-64
11. Campbell JW, Cronan JE Jr. 2001. Bacterial fatty acid biosynthesis: targets for antibacterial drug discovery. Annu. Rev. Microbiol. 55:305-32
12. Campbell JW, Morgan-Kiss RM, Cronan JE Jr. 2003. A new Escherichia coli metabolic competency: growth on fatty acids by a novel anaerobic β-oxidation pathway. Mol. Microbiol. 47:793-805
13. Cho H, Cronan JE Jr. 1995. Defective export of a periplasmic enzyme disrupts regulation of fatty acid synthesis. J. Biol. Chem. 270:4216-19
14. Clark D, Lightner V, Edgar R, Modrich P, Cronan JE Jr, Bell RM. 1980. Regulation of phospholipid biosynthesis in Escherichia coli. Cloning of the structural gene for the biosynthetic sn-glycerol-3-phosphate dehydrogenase. J. Biol. Chem. 255:714-17
15. Coleman J. 1990. Characterization of Escherichia coli cells deficient in 1-acyl-sn-glycerol-3-phosphate acyltransferase activity. J. Biol. Chem. 265:17215-21
16. Cronan JE Jr. 1968. Phospholipid alterations during growth of Escherichia coli. J. Bacteriol. 95:2054-61
17. Cronan JE Jr. 2002. Phospholipid modifications in bacteria. Curr. Opin. Microbiol. 5:202-5
18. Cronan JE Jr, Gelmann EP. 1973. An estimate of the minimum amount of unsaturated fatty acid required for growth of Escherichia coli. J. Biol. Chem. 248:1188-95
19. Cronan JE Jr, Gennis RB, Maloy SR. 1987. Cytoplasmic membrane. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, ed. JL Ingraham FC Neidhardt, KB Low, B Magasanik, M Schaechter, HE Umbarger, pp. 31-55. Washington, DC: ASM
20. Cronan JE Jr, Waldrop GL. 2002. Multi-subunit acetyl-CoA carboxylases. Prog. Lipid Res. 41:407-35
21. Crooke E. 2001. Escherichia coli DnaA protein-phospholipid interactions: in vitro and in vivo. Biochimie 83:19-23
22. Cybulski LE, Albanesi D, Mansilla MC, Altabe S, Aguilar PS, de Mendoza D. 2002. Mechanism of membrane fluidity optimization: isothermal control of the Bacillus subtilis acyl-lipid desaturase. Mol. Microbiol. 45:1379-88
23. Davis MS, Cronan JE Jr. 2001. Inhibition of Escherichia coli acetyl coenzyme A carboxylase by acyl-acyl carrier protein. J. Bacteriol. 183:1499-503
24. Davis MS, Solbiati J, Cronan JE Jr. 2000. Overproduction of acetyl-CoA carboxylase activity increases the rate of fatty acid biosynthesis in Escherichia coli. J. Biol. Chem. 275:28593-98
25. de Kruijff B. 1997. Lipid polymorphism and biomembrane function. Curr. Opin. Chem. Biol. 1:564-69
26. de Mendoza D, Cronan JE Jr. 1983. Temperature regulation of membrane fluidity in bacteria. Trends Biochem. Sci. 8:49-52
27. de Vrije T, de Swart RL, Dowhan W, Tommassen J, de Kruijff B. 1988. Phosphatidylglycerol is involved in protein translocation across Escherichia coli inner membranes. Nature 334:173-75
28. DeChavigny A, Heacock PN, Dowhan W. 1991. Sequence and inactivation of the pss gene of Escherichia coli. Phosphatidylethanolamine may not be essential for cell viability. J. Biol. Chem. 266:5323-32
29. Dillon DA, Wu WI, Riedel B, Wissing JB, Dowhan W, Carman GM. 1996. The Escherichia coli pgpB gene encodes for a diacylglycerol pyrophosphate phosphatase activity. J. Biol. Chem. 271:30548-53
30. Doerrler WT, Raetz CR. 2002. ATPase activity of the MsbA lipid flippase of Escherichia coli. J. Biol. Chem. 277: 36697-705
31. Doerrler WT, Reedy MC, Raetz CR. 2001. An Escherichia coli mutant defective in lipid export. J. Biol. Chem. 276:11461-64
32. Dowhan W. 1997. CDP-diacylglycerol synthase of microorganisms. Biochim. Biophys. Acta 1348:157-65
33. Dowhan W. 1997. Molecular basis for membrane phospholipid diversity: Why are there so many lipids? Annu. Rev. Biochem. 66:199-232
34. Farrell J, Rose A. 1967. Temperature effects on microorganisms. Annu. Rev. Microbiol. 21:101-20
35. Guo D, Tropp BE. 2000. A second Escherichia coli protein with CL synthase activity. Biochim. Biophys. Acta 1483:263-74
36. Hagio M, Gombos Z, Varkonyi Z, Masamoto K, Sato N, et al. 2000. Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis. Plant Physiol. 124:795-804
37. Hanke C, Wolter FP, Coleman J, Peterek G, Frentzen M. 1995. A plant acyltransferase involved in triacylglycerol biosynthesis complements an Escherichia coli sn-1-acylglycerol-3-phosphate acyltransferase mutant. Eur. J. Biochem. 232:806-10
38. Harder ME, Beacham IR, Cronan JE Jr, Beacham K, Honegger JL, Silbert DF. 1972. Temperature-sensitive mutants of Escherichia coli requiring saturated and unsaturated fatty acids for growth: isolation and properties. Proc. Natl. Acad. Sci. USA 69:3105-9
39. Hawrot E, Kennedy EP. 1978. Phospholipid composition and membrane function in phosphatidylserine decarboxylase mutants of Escherichia coli. J. Biol. Chem. 253:8213-20
40. Heacock PN, Dowhan W. 1987. Construction of a lethal mutation in the synthesis of the major acidic phospholipids of Escherichia coli. J. Biol. Chem. 262:13044-49
41. Heacock PN, Dowhan W. 1989. Alteration of the phospholipid composition of Escherichia coli through genetic manipulation. J. Biol. Chem. 264:14972-77
42. Heath RJ, Goldfine H, Rock CO. 1997. A gene (plsD) from Clostridium butyricum that functionally substitutes for the sn-glycerol-3-phosphate acyltransferase gene (plsB) of Escherichia coli. J. Bacteriol. 179:7257-63
43. Heath RJ, Rock CO. 1998. A conserved histidine is essential for glycerolipid acyltransferase catalysis. J. Bacteriol. 180: 1425-30
44. Heath RJ, Rock CO. 2002. The Claisen condensation in biology. Nat. Prod. Rep. 19:581-96
45. Heath RJ, White SW, Rock CO. 2001. Lipid biosynthesis as a target for antibacterial agents. Prog. Lipid Res. 40:467-97
46. Hrafnsdottir S, Menon AK. 2000. Reconstitution and partial characterization of phospholipid flippase activity from detergent extracts of the Bacillus subtilis cell membrane. J. Bacteriol. 182:4198-206
47. Huijbregts RP, de Kroon AI, de Kruijff B. 1996. Rapid transmembrane movement of C6-NBD-labeled phospholipids across the inner membrane of Escherichia coli. Biochim. Biophys. Acta 1280:41-50
48. Huijbregts RP, de Kroon AI, de Kruijff B. 2000. Topology and transport of membrane lipids in bacteria. Biochim. Biophys. Acta 1469:43-61
49. Inoue K, Matsuzaki H, Matsumoto K, Shibuya I. 1997. Unbalanced membrane phospholipid compositions affect transcriptional expression of certain regulatory genes in Escherichia coli. J. Bacteriol. 179:2872-78
50. Jackson BJ, Gennity JM, Kennedy EP. 1986. Regulation of the balanced synthesis of membrane phospholipids. Experimental test of models for regulation in Escherichia coli. J. Biol. Chem. 261:13464-68
51. Jiang P, Cronan JE Jr. 1994. Inhibition of fatty acid synthesis in Escherichia coli in the absence of phospholipid synthesis and release of inhibition by thioesterase action. J. Bacteriol. 176:2814-21
52. Jin AJ, Edidin M, Nossal R, Gershfeld NL. 1999. A singular state of membrane lipids at cell growth temperatures. Biochemistry 38:13275-78
53. Kikuchi S, Shibuya I, Matsumoto K. 2000. Viability of an Escherichia coli pgsA null mutant lacking detectable phosphatidylglycerol and cardiolipin. J. Bacteriol. 182:371-76
54. Kitamura E, Nakayama Y, Matsuzaki H, Matsumoto K, Shibuya I. 1994. Acidic-phospholipid deficiency represses the flagellar master operon through a novel regulatory region in Escherichia coli. Biosci. Biotechnol. Biochem. 58:2305-7
55. Kol MA, de Kroon AI, Rijkers DT, Killian JA, de Kruijff B. 2001. Membrane-spanning peptides induce phospholipid flop: a model for phospholipid translocation across the inner membrane of E. coli. Biochemistry 40:10500-6
56. Kol MA, de Kruijff B, de Kroon AI. 2002. Phospholipid flip-flop in biogenic membranes: what is needed to connect opposite sides. Semin. Cell Dev. Biol. 13:163-70
57. Kubelt J, Menon AK, Muller P, Herrmann A. 2002. Transbilayer movement of fluorescent phospholipid analogues in the cytoplasmic membrane of Escherichia coli. Biochemistry 41:5605-12
58. Kusters R, Dowhan W, de Kruijff B. 1991. Negatively charged phospholipids restore prePhoE translocation across phosphatidylglycerol- depleted Escherichia coli inner membranes. J. Biol. Chem. 266:8659-62
59. Langley KE, Hawrot E, Kennedy EP 1982. Membrane assembly: movement of phosphatidylserine between the cytoplasmic and outer membranes of Escherichia coli. J. Bacteriol. 152:1033-41
60. Li SJ, Cronan JE Jr. 1993. Growth rate regulation of Escherichia coli acetyl coenzyme A carboxylase, which catalyzes the first committed step of lipid biosynthesis. J. Bacteriol. 175:332-40
61. Lindblom G, Oradd G, Rilfors L, Morein S. 2002. Regulation of lipid composition in Acholeplasma laidlawii and Escherichia coli membranes: NMR studies of lipid lateral diffusion at different growth temperatures. Biochemistry 41: 11512-15
62. Lobner-Olesen A, Skarstad K, Hansen FG, von Meyenburg K, Boye E. 1989. The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell 57:881-89
63. Marrakchi H, Choi KH, Rock CO. 2002. A new mechanism for anaerobic unsaturated fatty acid formation in Streptococcus pneumoniae. J. Biol. Chem. 277:44809-16
64. Marrakchi H, Zhang YM, Rock CO. 2001. Mechanistic diversity and regulation of Type II fatty acid synthesis. Biochem. Soc. Trans. 30:1050-55
65. Matsumoto K. 2001. Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids. Mol. Microbiol. 39:1427-33
66. Matsumoto K, Okada M, Horikoshi Y, Matsuzaki H, Kishi T, et al. 1998. Cloning, sequencing, and disruption of the Bacillus subtilis psd gene coding for phosphatidylserine decarboxylase. J. Bacteriol. 180:100-6
67. McDevitt D, Rosenberg M. 2001. Exploiting genomics to discover new antibiotics. Trends Microbiol. 9:611-17
68. Messer W. 2002. The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol. Rev. 26:355-74
69. Mikhaleva NI, Golovastov VV, Zolov SN, Bogdanov MV, Dowhan W, Nesmeyanova MA. 2001. Depletion of phosphatidylethanolamine affects secretion of Escherichia coli alkaline phosphatase and its transcriptional expression. FEBS Lett. 493:85-90
70. Mileykovskaya E, Dowhan W. 1997. The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine. J. Bacteriol. 179:1029-34
71. Miyazaki C, Kuroda M, Ohta A, Shibuya I. 1985. Genetic manipulation of membrane phospholipid composition in Escherichia coli: pgsA mutants defective in phosphatidylglycerol synthesis. Proc. Natl. Acad. Sci. USA 82:7530-34
72. Mohan S, Kelly TM, Eveland SS, Raetz CR, Anderson MS. 1994. An Escherichia coli gene (fabZ) encoding (3R)-hydroxymyristoyl acyl carrier protein dehydrase. Relation to fabA and suppression of mutations in lipid A biosynthesis. J. Biol. Chem. 269:32896-903
73. Morbidoni HR, de Mendoza D, Cronan JE Jr. 1995. Synthesis of sn-glycerol 3-phosphate, a key precursor of membrane lipids, in Bacillus subtilis. J. Bacteriol. 177:5899-905
74. More MI, Finger LD, Stryker JL, Fuqua C, Eberhard A, Winans SC. 1996. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science 272:1655-58
75. Morein S, Andersson A, Rilfors L, Lindblom G. 1996. Wild-type Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures. J. Biol. Chem. 271:6801-9
76. Monta YS, Paul KS, Englund PT. 2000. Specialized fatty acid synthesis in African trypanosomes: myristate for GPI anchors. Science 288:140-43
77. Nishijima S, Asami Y, Uetake N, Yamagoe S, Ohta A, Shibuya I. 1988. Disruption of the Escherichia coli els gene responsible for cardiolipin synthesis. J. Bacteriol. 170:775-80
78. Ohta A, Shibuya I. 1977. Membrane phospholipid synthesis and phenotypic correlation of an Escherichia coli pss mutant. J. Bacteriol. 132:434-43
79. Okada M, Matsuzaki H, Shibuya I, Matsumoto K. 1994. Cloning, sequencing, and expression in Escherichia coli of the Bacillus subtilis gene for phosphatidylserine synthase. J. Bacteriol. 176:7456-61
80. Paul KS, Jiang D, Morita YS, Englund PT. 2001. Fatty acid synthesis in African trypanosomes: a solution to the myristate mystery. Trends Parasitol. 17:381-87
81. Payne DJ, Warren PV, Holmes DJ, Ji Y, Lonsdale JT. 2001. Bacterial fatty-acid biosynthesis: a genomics-driven target for antibacterial drug discovery. Drug Discov. Today 6:537-44
82. Pedersen S, Bloch PL, Reeh S, Neidhardt FC. 1978. Patterns of protein synthesis in E. coli: a catalog of the amount of 140 individual proteins at different growth rates. Cell 14:179-90
83. Raetz CR, Foulds J. 1977. Envelope composition and antibiotic hypersensitivity of Escherichia coli mutants defective in phosphatidylserine synthetase. J. Biol. Chem. 252:5911-15
84. Raetz CR, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700
85. Rehm BH, Mitsky TA, Steinbuchel A. 2001. Role of fatty acid de novo biosynthesis in polyhydroxyalkanoic acid (PHA) and rhamnolipid synthesis by pseudomonads: establishment of the transacylase (PhaG)-mediated pathway for PHA biosynthesis in Escherichia coli. Appl. Environ. Microbiol. 67:3102-9
86. Rietveld AG, Chupin VV, Koorengevel MC, Wienk HL, Dowhan W, de Kruijff B. 1994. Regulation of lipid polymorphism is essential for the viability of phosphatidylethanolamine-deficient Escherichia coli cells. J. Biol. Chem. 269:28670-75
87. Rietveld AG, Killian JA, Dowhan W, de Kruijff B. 1993. Polymorphic regulation of membrane phospholipid composition in Escherichia coli. J. Biol. Chem. 268:12427-33
88. Rietveld AG, Koorengevel MC, de Kruijff B. 1995. Non-bilayer lipids are required for efficient protein transport across the plasma membrane of Escherichia coli. EMBO J. 14:5506-13
89. Rilfors L, Niemi A, Haraldsson S, Edwards K, Andersson AS, Dowhan W. 1999. Reconstituted phosphatidylserine synthase from Escherichia coli is activated by anionic phospholipids and micelle-forming amphiphiles. Biochim. Biophys. Acta 1438:281-94
90. Saha SK, Nishijima S, Matsuzaki H, Shibuya I, Matsumoto K. 1996. A regulatory mechanism for the balanced synthesis of membrane phospholipid species in Escherichia coli. Biosci. Biotechnol. Biochem. 60:111-16
91. Sato N, Hagio M, Wada H, Tsuzuki M. 2000. Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc. Natl. Acad. Sci. USA 97:10655-60
92. Schaefer AL, Val DL, Hanzelka BL, Cronan JE Jr, Greenberg EP. 1996. Generation of cell-to-cell signals in quorum sensing: acylhomoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Natl. Acad. Sci. USA 93:9505-9
93. Sekimizu K, Kornberg A. 1988. Cardiolipin activation of DnaA protein, the initiation protein of replication in Escherichia coli. J. Biol. Chem. 263:7131-35
94. Silbert DF, Cronan JE Jr, Beacham IR, Harder ME. 1974. Genetic engineering of membrane lipid. Fed. Proc. 33:1725-32
95. Silbert DF, Vagelos PR. 1974. Systems for membrane alteration: unsaturated fatty acid auxotroph of Escherichia coli. Methods Enzymol. 32:856-64
96. Stanley P, Koronakis V, Hughes C. 1998. Acylation of Escherichia coli hemolysin: a unique protein lipidation mechanism underlying toxin function. Microbiol. Mol. Biol. Rev. 62:309-33
97. Surolia N, RamachandraRao SP, Surolia A. 2002. Paradigm shifts in malaria parasite biochemistry and anti-malarial chemotherapy. Bioessays 24:192-96
98. Suzuki M, Hara H, Matsumoto K. 2002. Envelope disorder of Escherichia coli cells lacking phosphatidylglycerol. J. Bacteriol. 184:5418-25
99. Tropp BE. 1997. Cardiolipin synthase from Escherichia coli. Biochim. Biophys. Acta 1348:192-200
100. Tropp BE, Ragolia L, Xia W, Dowhan W, Milkman R, et al. 1995. Identity of the Escherichia coli cls and nov genes. J. Bacteriol. 177:5155-57
101. Val DL, Cronan JE Jr. 1998. In vivo evidence that S-adenosylmethionine and fatty acid synthesis intermediates are the substrates for the LuxI family of autoinducer synthases. J. Bacteriol. 180:2644-51
102. Van Voorst F, De Kruijff B. 2000. Role of lipids in the translocation of proteins across membranes. Biochem. J. 347:601-12
103. Vanden Boom T, Cronan JE Jr. 1989. Genetics and regulation of bacterial lipid metabolism. Annu. Rev. Microbiol. 43:317-43
104. Wang X, Bogdanov M, Dowhan W. 2002. Topology of polytopic membrane protein subdomains is dictated by membrane phospholipid composition. EMBO J. 21:5673-81
105. Waters N, Kopydlowski K, Guszczynski T, Wei L, Sellers P, et al. 2002. Functional characterization of the acyl carrier protein (PfACP) and β-ketoacyl ACP synthase III (PfKASIII) from Plasmodium falciparum. Mol. Biochem. Parasitol. 123:85-94
106. West J, Tompkins CK, Balantac N, Nudelman E, Meengs B, et al. 1997. Cloning and expression of two human lysophosphatidic acid acyltransferase cDNAs that enhance cytokine-induced signaling responses in cells. DNA Cell Biol. 16:691-701
107. Wilson RJ. 2002. Progress with parasite plastids. J. Mol. Biol. 319:257-74
108. Xia W, Dowhan W. 1995. In vivo evidence for the involvement of anionic phospholipids in initiation of DNA replication in Escherichia coli. Proc. Natl. Acad. Sci. USA 92:783-87
109. Zheng W, Li Z, Skarstad K, Crooke E. 2001. Mutations in DnaA protein suppress the growth arrest of acidic phospholipid-deficient Escherichia coli cells. EMBO J. 20:1164-72