Biosynthesis and Function of Membrane Lipids

Deigo de Mendoza; Roberto Grau; John E. Cronan, Jr.

doi:10.1128/9781555818388.ch28

Chapter 28 : Biosynthesis and Function of Membrane Lipids

Authors: Deigo de Mendoza¹, Roberto Grau¹, John E. Cronan, Jr.²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Departamento de Microbiologia, Facultad de Ciencias Bioquimicas y Farmaceuticas, Universidad Nacional de Rosario, Suipacha 531, 2000 Rosario, Argentina; 2: Department of Microbiology and Department of Biochemistry, University of Illinois, Urbana, Illinois 61801

Content Type: Monograph

Publication Year: 1993

Category: Bacterial Pathogenesis; Microbial Genetics and Molecular Biology

Book DOI: 10.1128/9781555818388

Chapter DOI: 10.1128/9781555818388.ch28

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Biosynthesis and Function of Membrane Lipids, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555818388/9781555810535_Chap28-1.gif /docserver/preview/fulltext/10.1128/9781555818388/9781555810535_Chap28-2.gif

Abstract:

Bacillus spp.especially Bacillus subtilis, have major advantages for the study of the function of membrane lipids in bacterial membrane physiology. Bacillus spp. offer two additional biological phenomena to membrane lipid research. The first is sporulation, during which membrane lipid phenomena accompanying differentiation could be studied. The second is temperature-induced control of the composition of the membrane lipids, in which detectable amounts of unsaturated fatty acids (UFAs) are synthesized by Bacillus spp. only at low growth temperatures. This chapter focuses on the aspects of lipid metabolism that differ from those of the better studied gram-negative bacteria. The primary focus is on B. subtilis, because of its advantages in genetic analysis. Fatty acid synthesis is the best-studied aspect of Bacillus lipid metabolism. The chapter first focuses on the aspects of the pathway utilized in other bacteria and then discusses the product diversification reactions that result in the distinctive fatty acid compositions of bacilli. Two efforts that used E. coli as a model organism have contributed substantially for understanding of membrane lipids in bacteria. The first was the isolation of a growing collection of well-characterized mutants affecting lipid metabolism. The second is the continuing progress in molecular cloning of the lipid metabolism genes of this organism.

Citation: de Mendoza D, Grau R, Cronan, Jr. J. 1993. Biosynthesis and Function of Membrane Lipids, p 411-421. In Sonenshein A, Hoch J, Losick R (ed), Bacillus subtilis and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch28

Key Concept Ranking

Unsaturated Fatty Acids: 0.56016004
Fatty Acids: 0.50575817
Acetyl Coenzyme A: 0.5041322
Fatty Acid Synthase: 0.47480133

0.56016004

Highlighted Text: Show | Hide

Full text loading...

Figures

Biosynthesis and Function of Membrane Lipids

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818388.chap28-1,webId=/content/author/10.1128/9781555818388.chap28-1,properties={foaf_givenname=Deigo, foaf_name=Deigo de Mendoza, foaf_surname=de Mendoza, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818388.chap28-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818388.chap28-2,webId=/content/author/10.1128/9781555818388.chap28-2,properties={foaf_givenname=Roberto, foaf_name=Roberto Grau, foaf_surname=Grau, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818388.chap28-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818388.chap28-3,webId=/content/author/10.1128/9781555818388.chap28-3,properties={foaf_givenname=John E., foaf_name=John E. Cronan, Jr., foaf_surname=Cronan, Jr., pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818388.chap28-aff2]]}]]

/content/10.1128/9781555818388.chap28.fig28-1

Figure 1

Acylation of sn-G3P by two successive transfers of acyl groups from acyl-ACP. This pathway has been demonstrated in E. coli and clostridia. sn-G3P is probably synthesized by reduction of a glycolytic intermediate such as dihydroxyacetone phosphate or glyceraldehyde 3-phosphate.

10.1128/9781555818388/fig28-1_thmb.gif

10.1128/9781555818388/fig28-1.gif

Figure 1

/content/10.1128/9781555818388.chap28.fig28-3

Figure 3

Initiation of fatty acid biosynthesis in E. coli. The initiation of new acyl chains is accomplished by the action of three enzymes: 1, acetyl-CoA carboxylase; 2, malonyl-CoA: ACP transacylase; 3, 3-ketoacyl-ACP synthase III.

10.1128/9781555818388/fig28-3_thmb.gif

10.1128/9781555818388/fig28-3.gif

Figure 3

/content/10.1128/9781555818388.chap28.fig28-4

Figure 4

Elongation cycle of fatty acid biosynthesis. The elongation of a growing acyl chains is accomplished by the action of four enzymes: 1, 3-ketoacyl-ACP synthase; 2, 3-ketoacyl-ACP reductase; 3, 3-hydroxyacyl-ACP dehydrase; 4, enoyl reductase (frans-2-acyl-ACP reductase).

10.1128/9781555818388/fig28-4_thmb.gif

10.1128/9781555818388/fig28-4.gif

Figure 4

/content/10.1128/9781555818388.chap28.fig28-5

Figure 5

Proposed pathway for incorporation of branched-chain 2-keto acids into fatty acids in B. subtilis. Branched-chain amino acids are converted to branched-chain 2-keto acids by a branched-chain amino acid transaminase (reaction 1). The branched-chain 2-keto acid can then be converted into a CoA ester by a branched-chain 2-keto acid dehydrogenase (reaction 2) or an aldehyde derivative by a branched-chain 2-keto acid decarboxylase (reaction 3). It is assumed that the primers produced by reactions 2 and 3 could then be condensed with malonyl-ACP (see text and Fig. 6 ).

10.1128/9781555818388/fig28-5_thmb.gif

10.1128/9781555818388/fig28-5.gif

Figure 5

/content/10.1128/9781555818388.chap28.fig28-2

Figure 2

Synthesis of complex lipids. The three phospholipid species found in E. coli are synthesized from phosphatidic acid (top center structure) by a series of reactions catalyzed by six enzymes: 1, CDP-diglyceride synthase (phosphatidate cytidyltransferase); 2, phosphatidylserine synthase; 3, phosphatidylserine decarboxylase; 4, phosphatidylglycerol-phosphate synthase; 5, phosphatidylglycerol-phosphate phosphatase; 6, cardiolipin synthase. The same reactions are believed to occur in bacilli. In addition, diglyceride is synthesized by dephosphorylation of phosphatidic acid by phosphatidic acid phosphatase (reaction 7). A portion of the diglyceride is then glucosylated by one or two transfers of glucose from UDP-glucose (reaction 8 and 9). Reactions 7 through 9 have been detected in other organisms but not bacilli. Not shown is the amino acylation of phosphatidylglycerol (the product of reaction 5) by lysyl-tRNA to form lysylphosphatidylglycerol.

10.1128/9781555818388/fig28-2_thmb.gif

10.1128/9781555818388/fig28-2.gif

Figure 2

/content/10.1128/9781555818388.chap28.fig28-6

Figure 6

Pathways of branched-chain fatty acid and UFA syntheses in B. subtilis. (A) Pathway of synthesis from branched-chain acyl-CoA esters as primers. (B) The other proposed pathway ( 52 ) of synthesis from branched-chain 2-keto acids as primer sources. UFAs are formed by cold-induced desaturation of phospholipids ( 25 ) or acyl-CoAs ( 19 ).

10.1128/9781555818388/fig28-6_thmb.gif

10.1128/9781555818388/fig28-6.gif

Figure 6

References

/content/book/10.1128/9781555818388.chap28

1. Albertlni, A. M.,, C. Scotti,, and A. Galizzi. 1991. The Bacillus subtilis outG locus shows similarity to genes for fatty acids and polyketide biosynthesis. Abstr. 6th Int. Conf. Bacilli 1991.

2. Baigori, M.,, R. Grau,, H. R. Morbidonl,, and D. de Mendoza. 1991. Isolation and characterization of Bacillus subtilis mutants blocked in the synthesis of pantothenic acid. J. Bacteriol. 173: 4240– 4242.

3. Bell, R. M. 1975. Mutants of Escherichia coli defective in membrane phospholipid synthesis. Properties of wild type and K m defective sn-glycerol-3-phosphate acyl-transferase activities. J. Biol. Chem. 250: 7147– 7152.

4. Bishop, D. G.,, L. Rutberg,, and B. Samuelson. 1967. The chemical composition of the cytoplasmic membrane of Bacillus subtilis. Eur. J. Biochem. 2: 448– 453.

5. Bloch, K. 1970. ^-Hydroxydecanoyl thioester dehydrase. Enzymes 5: 441– 464.

6. Boudreaux, D. P.,, E. Eisenstat,, T. Ijima,, and E. Freese. 1981. Biochemical and genetic characterization of an auxotroph of Bacillus subtilis altered in the acyl CoA: acyl-carrier-protein-transacylase. Eur. J. Biochem. 115: 175– 181.

7. Boudreaux, D. P.,, and E. Freese. 1981. Sporulation in Bacillus subtilis is independent of membrane fatty acid composition. J. Bacteriol. 148: 480– 486.

8. Bulla, L. A.,, K. W. Nickerson,, T. L. Mount,, and J. J. Iandolo,. 1975. Biosynthesis of fatty acids during germination and outgrowth of Bacillus thuringiensis spores, p. 520– 525. In P. Gerhardt,, R. N. Costilow,, and H. L. Sadof (ed.), Spores VI. American Society for Microbiology, Washington, D.C.

9. Butterworth, P. H. W.,, and K. Bloch. 1970. Comparative aspects of fatty acid synthesis in Bacillus subtilis and Escherichia coli. Eur. J. Biochem. 12: 496– 501.

10. Clejan, S.,, T. A. Krulwich,, K. R. Mondrus,, and D. Seto-Young. 1986. Membrane lipid composition of obligately and facultatively alkalophilic strains of Bacillus spp. J. Bacteriol. 168: 334– 340.

11. Cronan, J. E., Jr. 1978. Molecular biology of bacterial membrane lipids. Annu. Rev. Biochem. 47: 163– 189.

12. Cronan, J. E., Jr.,, and R. M. Bell. 1974. Mutants of Escherichia coli defective in membrane phospholipid synthesis: mapping of the structural gene for L-glycerol-3-phosphate dehydrogenase. J. Bacteriol. 118: 598– 605.

13. Cronan, J. E., Jr.,, and C. O. Rock,. 1987. Biosynthesis of membrane lipids, p. 474— 497. In F. C. Neidhart,, J. L. Ingrahan,, K. B. Low,, B. Magasanik,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, vol. 1. American Society for Microbiology, Washington, D.C.

14. Cronan, J. E., Jr.,, L. J. Weisberg,, and R. G. Allen. 1975. Regulation of membrane lipid synthesis in Escherichia coli: accumulation of free fatty acids of abnormal length during inhibition of phospholipid synthesis. J. Biol. Chem. 250: 5835– 5840.

15. de Mendoza, D.,, and J. E. Cronan, Jr. 1983. Thermal regulation of membrane lipid fluidity in bacteria. Trends Biochem. Sci. 8: 49– 52.

16. de Mendoza, D.,, and R. N. Farias,. 1988. Effect of fatty acid supplementation on membrane fluidity in microorganisms, p. 119– 149. In R. C. Aloia,, C. C. Curtain,, and L. M. Gordon (ed.), Physiological Regulation of Membrane Fluidity, vol. 3. Alan R. Liss, Inc., New York.

17. de Mendoza, D.,, A. Klages-Ulrich,, and J. E. Cronan, Jr. 1983. Thermal regulation of membrane fluidity in Escherichia coli: effects of overproduction of 0-keto-acyl-acyl-carrier protein synthase I. J. Biol. Chem. 258: 2098– 2101.

18. Dreher, R.,, K. Poralla,, and W. A. Konlng. 1976. Synthesis of ω-alicyclic fatty acids from cyclic precursors in Bacillus subtilis. J. Bacteriol. 127: 1136– 1140.

19. Dunkley, E. A.,, Jr., S. Clejan,, and T. A. Krulwich. 1991. Mutants of Bacillus species isolated on the basis of protonophore resistance are deficient in fatty acid desaturase activity. J. Bacteriol. 173: 7750– 7755.

20. Fujil, D. K.,, and A. J. Fulco. 1977. Biosynthesis of unsaturated fatty acids by Bacilli: hyperinduction and modulation of desaturase synthesis. J. Biol. Chem. 252: 3660– 3670.

21. Fulco, A. J. 1969. The biosynthesis of unsaturated fatty acids by Bacilli. I. Temperature induction of the desaturation reaction. J. Biol. Chem. 244: 889– 895.

22. Fulco, A. J. 1983. Fatty acid metabolism in bacteria. Prog. Lipid Res. 22: 133– 160.

23. Garwln, J. L.,, and J. E. Cronan, Jr. 1980. Thermal modulation of fatty acid synthesis in Escherichia coli does not involve de novo synthesis. J. Bacteriol. 141: 1457– 1459.

24. Grau, R.,, and D. de Mendoza. 1993. Ph.D. thesis. University of Rosario, Rosario, Argentina.

25. Grau, R.,, and D. de Mendoza. Regulation of the synthesis of unsaturated fatty acids by growth temperature in Bacillus subtilis: evidence that phospholipids are substrates of a cold-inducible fatty acid desaturation pathway. Mol. Microbiol., in press.

26. GuCfanti, A. A.,, S. Clejan,, L. H. Falk,, D. B. Hicks,, and T. A. Krulwich. 1987. Isolation and characterization of uncoupler resistant mutants of Bacillus subtilis. J. Bacteriol. 169: 4479– 4485.

27. Holgrem, E. 1978. A mutant of Bacillus subtilis with temperature sensitive synthesis of fatty acids. FEMS Microbiol. Lett. 3: 327– 329.

28. Jackowskl, S.,, C. M. Murphy,, J. E. Cronan, Jr.,, and C. O. Rock, 1989. Acetoacetyl-acyl carrier protein synthase: a target for the antibiotic thiolactomycin. J. Biol. Chem. 264: 7624– 7629.

29. Jackowskl, S.,, and C. O. Rock. 1987. Acetoacetyl-acyl carrier protein synthase as potential regulator of fatty acid biosynthesis in bacteria. J. Biol. Chem. 262: 7927– 7931.

30. Kaneda, T. 1963. Biosynthesis of branched-chain fatty acids. I. Isolation and identification of fatty acids from Bacillus subtilis (ATCC 7059). J. Biol. Chem. 238: 1222– 1228.

31. Kaneda, T. 1967. Fatty acids in the genus Bacillus. I. Iso-and anteiso-fatty acids as characteristic constituents of lipids in 10 species. J. Bacteriol. 93: 894– 903.

32. Kaneda, T. 1973. Biosynthesis of branched long-chain fatty acids from the related short-chain α-keto acid substrates by a cell free system of Bacillus subtilis. Can. J. Microbiol. 19: 87– 96.

33. Kaneda, T. 1977. Fatty acids of the genus Bacillus: an example of branched-chain preference. Bacteriol. Rev. 41: 391– 418.

34. Kaneda, T. 1991. Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55: 288– 302.

35. Kaneda, T.,, and E. J. Smith. 1980. Relationship of primer specificity of fatty acid de novo synthetase to fatty acid composition in ten species of bacteria and yeast. Can. J. Microbiol. 26: 893– 898.

36. Krulwich, T. A.,, S. Clejan,, L. Falk,, and A. A. GuCfanti. 1987. Incorporation of specific exogenous fatty acids into membrane lipids modulates protonophore resistance in Bacillus subtilis. J. Bacteriol. 169: 4479– 4485.

37. Krulwlch, T. A.,, P. G. Quish,, and A. A. Guffantl. 1990. Uncoupler-resistant mutants of bacteria. Microbiol. Rev. 54: 52– 65.

38. Lennarz, W. J., 1970. Bacterial lipids, p. 210– 270. In J. J. Wakil (ed.), Lipid Metabolism. Academic Press, Inc., New York.

39. Lombard!, F. J.,, and A. J. Fulco. 1980. Temperature-mediated hyperinduction of fatty acid desaturation in pre-existing and newly formed fatty acid synthesized endogenously in Bacillus megaterium. Biochim. Biophys. Acta 618: 359– 363.

40. Lowe, P. N.,, J. A. Hodgson,, and R. N. Perham. 1983. Dual role of a single multienzyme complex in the oxidative decarboxylation of pyruvate and branched-chain 2-oxoacids in Bacillus subtilis. Biochem. J. 215: 133– 140.

41. McElhaney, R. N. 1982. Effects of membrane lipids on transport and enzymic activities. Curr. Top. Membr. Transp. 17: 317– 380.

42. Mclntyre, T. M.,, B. K. Chamberlain,, R. E. Webster,, and R. M. Bell. 1977. Mutants of Escherichia coli defective in membrane phospholipid synthesis. Effects of cessation and reinitiation of phospholipid synthesis on macromolecular synthesis and phospholipid turnover. J. Biol. Chem. 252: 4487– 4493.

43. Mindlch, L. 1970. Membrane synthesis in Bacillus subtilis. I. Isolation and properties of strains bearing mutations in glycerol metabolism. J. Mol. Biol. 49: 415– 432.

44. Mindlch, L. 1970. Membrane synthesis in Bacillus subtilis. II. Integration of membrane proteins in the absence of lipid synthesis. J. Mol. Biol. 49: 433– 439.

45. Mindlch, L. 1971. Induction of Staphylococcus aureus lactose permease in the absence of glycerolipid synthesis. Proc. Natl. Acad. Sci. USA 68: 420– 424.

46. Mindlch, L. 1972. Control of fatty acid synthesis in bacteria. J. Bacteriol. 110: 96– 102.

47. Mindlch, L., 1975. Studies on bacterial membrane biogenesis using glycerol auxotrophs, p. 429– 455. In A. Tzagolof (ed.), Membrane Biogenesis: Mitochondria, Chloroplasts and Bacteria. Plenum Press, New York.

48. Morbidoni, R.,, M. Baigori,, D. de Mendoza,, and J. E. Cronan, Jr. Unpublished results.

49. Naik, D. N.,, and T. Kaneda. 1974. Biosynthesis of branched long-chain fatty acids by species of Bacillus: relative activities of three α-keto acids substrates and factors affecting chain length. Can. J. Microbiol. 20:1701— 1708.

50. Namba, Y.,, K. Yoshizawa,, A. Ejima,, T. Hayashi,, and T. Kaneda. 1969. Coenzyme A and nicotinamide adenine dinucleotide-dependent branched chain α-keto acid dehydrogenase. I. Purification and properties of the enzyme from Bacillus subtilis. J. Biol. Chem. 244: 4437– 4447.

51. Nunn, W. D.,, D. L. Kelley,, and N. Y. Stumfall. 1977. Regulation of fatty acid synthesis during glycerol starvation of glycerol auxotrophs of Escherichia coli. J. Bacteriol. 132: 526– 531.

52. Oku, H.,, and T. Kaneda. 1988. Biosynthesis of branched-chain fatty acids in Bacillus subtilis. A decarboxylase is essential for branched-chain fatty acid synthetase. J. Biol. Chem. 263: 18386– 18396.

53. Op den Kamp, J. A. F.,, I. Redai,, and L. L. M. van Deenen. 1969. Phospholipid composition of Bacillus subtilis. J. Bacteriol. 99: 298– 303.

54. Platt, M. W.,, K. J. Miller,, W. S. Lane,, and E. P. Kennedy. 1990. Isolation and characterization of the constitutive acyl carrier protein from Rhizobium meliloti. J. Bacteriol. 172: 5440– 5444.

55. Revill, W. P.,, and P. F. Leadlay. 1991. Cloning, characterization, and high-level expression in Escherichia coli of the Saccharopolyspora erythraea gene encoding an acyl carrier protein potentially involved in fatty acid biosynthesis. J. Bacteriol. 173: 4379– 4385.

56. Rigomier, D.,, and B. Lubochinsky. 1974. Metabolisme des phospholipides chez des mutants asporogenes de Bacillus subtilis au cours de la croissance exponentialle. Ann. Microbiol. 125B: 295– 303.

57. Rock, C. O.,, and S. Jackowskl. 1982. Regulation of phospholipid synthesis in Escherichia coli. Composition of the acyl-acyl carrier protein pool in vivo. J. Biol. Chem. 257: 10759– 10765.

58. Rothman, J. E.,, and E. P. Kennedy. 1977. Asymmetrical distribution of phospholipids in the membrane of Bacillus megaterium. J. Mol. Biol. 110: 603– 618.

59. Rothman, J. E.,, and E. P. Kennedy. 1977. Rapid trans-membrane movement of newly synthesized phospholipids during membrane assembly. Proc. Natl. Acad. Sci. USA 74: 1821– 1825.

60. Russell, N. J. 1984. Mechanisms of thermal adaptation in bacteria: blueprints for survival. Trends Biochem. Sci. 9: 108– 112.

61. Saito, K. 1960. Chromatographic studies on bacterial fatty acids. J. Biochem. 47: 699– 719.

62. Scandella, C. J.,, and A. Kornberg. 1969. Biochemical studies of bacterial sporulation and germination. XV. Fatty acids in growth and sporulation of Bacillus megaterium. J. Bacteriol. 98: 82– 86.

63. Silvius, J. R.,, and R. X. McElhaney. 1979. Effects of phospholipid acyl chain structure on physical properties. I. Isobranched phosphatidylcholines. Chem. Phys. Lipids 24: 287– 296.

64. Vanden Boom, T.,, and J. E. Cronan, Jr. 1989. Genetics and regulation of bacterial lipid metabolism. Annu. Rev. Microbiol. 43: 317– 343.

65. Wille, W.,, E. Eisenstand,, and K. Willecke. 1975. Inhibition of the de novo fatty acid biosynthesis by the antibiotic cerulenin in Bacillus subtilis: effect of citrate-Mg 2+ transport and synthesis of macromolecules. Antimicrob. Agents Chemother. 8: 231– 237.

66. Willecke, K.,, and L. Mindlch. 1971. Induction of citrate transport in Bacillus subtilis during the absence of phospholipid synthesis. J. Bacteriol. 106: 514– 518.

67. Willecke, K.,, and A. B. Pardee. 1971. Fatty acid requiring mutants of Bacillus subtilis defective in branched chain keto acid dehydrogenase. J. Biol. Chem. 246: 5264– 5272.

Tables

Biosynthesis and Function of Membrane Lipids

/content/10.1128/9781555818388.chap28.tab28-1

Table 1

Fatty acid composition of total membrane lipid extracts from B. subtilis a

10.1128/9781555818388/tab28-1_thmb.gif

10.1128/9781555818388/tab28-1.gif

Table 1

Fatty acid composition of total membrane lipid extracts from B. subtilis a