Chlamydia trachomatis serovar L2 can utilize exogenous lipoic acid through the action of the lipoic acid ligase LplA1

Journal of Bacteriology

Volumn 192, Issue 23, 2010, Pages 6172-6181

  Ramaswamy, Aishwarya V ^a   Maurelli, Anthony T ^a  

^a Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGASE; PROTEIN LIPA; SYNTHETASE; THIOCTIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CELL GROWTH; CELL MATURATION; CHLAMYDIA TRACHOMATIS; ESCHERICHIA COLI; LIPOYLATION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SEROTYPE;

BACTERIAL PROTEINS; CHLAMYDIA TRACHOMATIS; ESCHERICHIA COLI; GENETIC COMPLEMENTATION TEST; LIGASES; LIPOPROTEINS; MEMBRANE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; THIOCTIC ACID;

CHLAMYDIA TRACHOMATIS; CHLAMYDIAE; ESCHERICHIA COLI;

EID: 78649339358     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00717-10     Document Type: Article

References (45)

1. AbdelRahman, Y. M., and R. J. Belland. 2005. The chlamydial developmental cycle. FEMS Microbiol. Rev. 29:949-959.
2. Allary, M., J. Z. Lu, L. Zhu, and S. T. Prigge. 2007. Scavenging of the cofactor lipoate is essential for the survival of the malaria parasite Plasmodium falciparum. Mol. Microbiol. 63:1331-1344.
3. Andersson, S. G., A. Zomorodipour, J. O. Andersson, T. Sicheritz-Ponten, U. C. Alsmark, R. M. Podowski, A. K. Naslund, A. S. Eriksson, H. H. Winkler, and C. G. Kurland. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133-140.
4. Bebear, C., and B. de Barbeyrac. 2009. Genital Chlamydia trachomatis infections. Clin. Microbiol. Infect. 15:4-10.
5. Belland, R. J., D. E. Nelson, D. Virok, D. D. Crane, D. Hogan, D. Sturdevant, W. L. Beatty, and H. D. Caldwell. 2003. Transcriptome analysis of chlamydial growth during IFN-γ-mediated persistence and reactivation. Proc. Natl. Acad. Sci. U. S. A. 100:15971-15976.
6. Belland, R. J., G. Zhong, D. D. Crane, D. Hogan, D. Sturdevant, J. Sharma, W. L. Beatty, and H. D. Caldwell. 2003. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. U. S. A. 100:8478-8483.
7. Binet, R., and A. T. Maurelli. 2007. Frequency of development and associated physiological cost of azithromycin resistance in Chlamydia psittaci 6BC and C. trachomatis L2. Antimicrob. Agents Chemother. 51:4267-4275.
8. Brinkman, F. S., J. L. Blanchard, A. Cherkasov, Y. Av-Gay, R. C. Brunham, R. C. Fernandez, B. B. Finlay, S. P. Otto, B. F. Ouellette, P. J. Keeling, A. M. Rose, R. E. Hancock, S. J. Jones, and H. Greberg. 2002. Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res. 12:1159-1167.
9. Burton, M. J., and D. C. Mabey. 2009. The global burden of trachoma: a review. PLoS Negl. Trop. Dis. 3:e460.
10. Crawford, M. J., N. Thomsen-Zieger, M. Ray, J. Schachtner, D. S. Roos, and F. Seeber. 2006. Toxoplasma gondii scavenges host-derived lipoic acid despite its de novo synthesis in the apicoplast. EMBO J. 25:3214-3222.
11. Cronan, J. E., X. Zhao, and Y. Jiang. 2005. Function, attachment and synthesis of lipoic acid in Escherichia coli. Adv. Microb. Physiol. 50:103-146.
12. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
13. de Kok, A., A. F. Hengeveld, A. Martin, and A. H. Westphal. 1998. The pyruvate dehydrogenase multi-enzyme complex from Gram-negative bacteria. Biochim. Biophys. Acta 1385:353-366.
14. Gunther, S., P. J. McMillan, L. J. Wallace, and S. Muller. 2005. Plasmodium falciparum possesses organelle-specific alpha-keto acid dehydrogenase complexes and lipoylation pathways. Biochem. Soc. Trans. 33:977-980.
15. Gunther, S., J. Storm, and S. Muller. 2009. Plasmodium falciparum: organelle-specific acquisition of lipoic acid. Int. J. Biochem. Cell Biol. 41:748-752.
16. Guyer, M. S., R. R. Reed, J. A. Steitz, and K. B. Low. 1981. Identification of a sex-factor-affinity site in Escherichia coli as gamma delta. Cold Spring Harbor Symp. Quant. Biol. 45:135-140.
17. Guzman, L. M., D. Belin, M. J. Carson, and J. Beckwith. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
18. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
19. Hatch, G. M., and G. McClarty. 1998. Cardiolipin remodeling in eukaryotic cells infected with Chlamydia trachomatis is linked to elevated mitochondrial metabolism. Biochem. Biophys. Res. Commun. 243:356-360.
20. Heinzen, R. A., and T. Hackstadt. 1997. The Chlamydia trachomatis parasitophorous vacuolar membrane is not passively permeable to low-molecularweight compounds. Infect. Immun. 65:1088-1094.
21. Hermes, F. A., and J. E. Cronan. 2009. Scavenging of cytosolic octanoic acid by mutant LplA lipoate ligases allows growth of Escherichia coli strains lacking the LipB octanoyltransferase of lipoic acid synthesis. J. Bacteriol. 191:6796-6803.
22. Jiang, Y., and J. E. Cronan. 2005. Expression cloning and demonstration of Enterococcus faecalis lipoamidase (pyruvate dehydrogenase inactivase) as a Ser-Ser-Lys triad amidohydrolase. J. Biol. Chem. 280:2244-2256.
23. Jordan, S. W., and J. E. Cronan, Jr. 1997. Biosynthesis of lipoic acid and posttranslational modification with lipoic acid in Escherichia coli. Methods Enzymol. 279:176-183.
24. Keeney, K. M., J. A. Stuckey, and M. X. O'Riordan. 2007. LplA1-dependent utilization of host lipoyl peptides enables Listeria cytosolic growth and virulence. Mol. Microbiol. 66:758-770.
25. Ma, Q., X. Zhao, A. N. Eddine, A. Geerlof, X. Li, J. E. Cronan, S. H. Kaufmann, and M. Wilmanns. 2006. The Mycobacterium tuberculosis LipB enzyme functions as a cysteine/lysine dyad acyltransferase. Proc. Natl. Acad. Sci. U. S. A. 103:8662-8667.
26. Martin, N., E. Lombardia, S. G. Altabe, D. de Mendoza, and M. C. Mansilla. 2009. A lipA (yutB) mutant, encoding lipoic acid synthase, provides insight into the interplay between branched-chain and unsaturated fatty acid biosynthesis in Bacillus subtilis. J. Bacteriol. 191:7447-7455.
27. McClarty, G. 1994. Chlamydiae and the biochemistry of intracellular parasitism. Trends Microbiol. 2:157-164.
28. Miller, J. R., R. W. Busby, S. W. Jordan, J. Cheek, T. F. Henshaw, G. W. Ashley, J. B. Broderick, J. E. Cronan, Jr., and M. A. Marletta. 2000. Escherichia coli LipA is a lipoyl synthase: in vitro biosynthesis of lipoylated pyruvate dehydrogenase complex from octanoyl-acyl carrier protein. Biochemistry 39:15166-15178.
29. Moran, N. A. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583-586.
30. Morris, T. W., K. E. Reed, and J. E. Cronan, Jr. 1994. Identification of the gene encoding lipoate-protein ligase A of Escherichia coli. Molecular cloning and characterization of the lplA gene and gene product. J. Biol. Chem. 269:16091-16100.
31. Nicolet, Y., and C. L. Drennan. 2004. AdoMet radical proteins from structure to evolution: alignment of divergent protein sequences reveals strong secondary structure element conservation. Nucleic Acids Res. 32:4015-4025.
32. O'Riordan, M., M. A. Moors, and D. A. Portnoy. 2003. Listeria intracellular growth and virulence require host-derived lipoic acid. Science 302:462-464.
33. Pilatz, S., K. Breitbach, N. Hein, B. Fehlhaber, J. Schulze, B. Brenneke, L. Eberl, and I. Steinmetz. 2006. Identification of Burkholderia pseudomallei genes required for the intracellular life cycle and in vivo virulence. Infect. Immun. 74:3576-3586.
34. Reche, P., and R. N. Perham. 1999. Structure and selectivity in posttranslational modification: attaching the biotinyl-lysine and lipoyl-lysine swinging arms in multifunctional enzymes. EMBO J. 18:2673-2682.
35. Reche, P. A. 2000. Lipoylating and biotinylating enzymes contain a homologous catalytic module. Protein Sci. 9:1922-1929.
36. Saka, H. A., and R. H. Valdivia. 2010. Acquisition of nutrients by chlamydiae: unique challenges of living in an intracellular compartment. Curr. Opin. Microbiol. 13:4-10.
37. Sasaki, M., A. Ansari, N. Pumford, J. Van De Water, P. S. Leung, K. M. Humphries, L. I. Szweda, Y. Nakanuma, T. E. Roche, R. L. Coppel, J. F. Bach, and M. E. Gershwin. 2000. Comparative immunoreactivity of antitrifluoroacetyl (TFA) antibody and anti-lipoic acid antibody in primary biliary cirrhosis: searching for a mimic. J. Autoimmun. 15:51-60.
38. Schonauer, M. S., A. J. Kastaniotis, V. A. Kursu, J. K. Hiltunen, and C. L. Dieckmann. 2009. Lipoic acid synthesis and attachment in yeast mitochondria. J. Biol. Chem. 284:23234-23242.
39. Smith, A. R., S. V. Shenvi, M. Widlansky, J. H. Suh, and T. M. Hagen. 2004. Lipoic acid as a potential therapy for chronic diseases associated with oxidative stress. Curr. Med. Chem. 11:1135-1146.
40. Sofia, H. J., G. Chen, B. G. Hetzler, J. F. Reyes-Spindola, and N. E. Miller. 2001. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 29:1097-1106.
41. Spalding, M. D., and S. T. Prigge. 2010. Lipoic acid metabolism in microbial pathogens. Microbiol. Mol. Biol. Rev. 74:200-228.
42. Thomson, N. R., M. T. Holden, C. Carder, N. Lennard, S. J. Lockey, P. Marsh, P. Skipp, C. D. O'Connor, I. Goodhead, H. Norbertzcak, B. Harris, D. Ormond, R. Rance, M. A. Quail, J. Parkhill, R. S. Stephens, and I. N. Clarke. 2008. Chlamydia trachomatis: genome sequence analysis of lymphogranuloma venereum isolates. Genome Res. 18:161-171.
43. Wang, S. A., J. R. Papp, W. E. Stamm, R. W. Peeling, D. H. Martin, and K. K. Holmes. 2005. Evaluation of antimicrobial resistance and treatment failures for Chlamydia trachomatis: a meeting report. J. Infect. Dis. 191:917-923.
44. Wrenger, C., and S. Muller. 2004. The human malaria parasite Plasmodium falciparum has distinct organelle-specific lipoylation pathways. Mol. Microbiol. 53:103-113.
45. Zhao, X., J. R. Miller, and J. E. Cronan. 2005. The reaction of LipB, the octanoyl-[acyl carrier protein]:protein N-octanoyltransferase of lipoic acid synthesis, proceeds through an acyl-enzyme intermediate. Biochemistry 44:16737-16746.