A new regulatory mechanism for bacterial lipoic acid synthesis

MicrobiologyOpen

Volumn 4, Issue 2, 2015, Pages 282-300

  Zhang, Huimin ^a,c   Luo, Qixia ^b   Gao, Haichun ^b   Feng, Youjun ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

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

Author keywords

Shewanella; cAMP receptor protein (CRP); LipA; LipB; Lipoic acid; Lipoic acid synthesis

Indexed keywords

BETA GALACTOSIDASE; C REACTIVE PROTEIN; CYCLIC AMP; THIOCTIC ACID;

ARTICLE; BACTERIAL GENE; BACTERIUM DETECTION; BINDING SITE; BIOSYNTHESIS; CONTROLLED STUDY; CRP GENE; ENZYME ACTIVITY; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; LACZ GENE; LIPA GENE; LIPB GENE; LIPOYLATION; MOLECULAR INTERACTION; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SHEWANELLA ONEIDENSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; ORYCTOLAGUS CUNICULUS; SHEWANELLA; SHEWANELLA ONEIDENSIS;

EID: 84926408980     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.237     Document Type: Article

References (72)

1. Aiba, H. 1983. Autoregulation of the Escherichia coli crp gene: CRP is a transcriptional repressor for its own gene. Cell 32:141-149.
2. Aiba, H. 1985. Transcription of the Escherichia coli adenylate cyclase gene is negatively regulated by cAMP-cAMP receptor protein. J. Biol. Chem. 260:3063-3070.
3. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, et al. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
4. Beckett, D. 2007. Biotin sensing: universal influence of biotin status on transcription. Annu. Rev. Genet. 41:443-464.
5. Casadaban, M. J., and S. N. Cohen. 1980. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138:179-207.
6. Chandler, M. S. 1992. The gene encoding cAMP receptor protein is required for competence development in Haemophilus influenzae Rd. Proc. Natl. Acad. Sci. USA 89:1626-1630.
7. Christensen, Q. H., and J. E. Cronan. 2010. Lipoic acid synthesis: a new family of octanoyltransferases generally annotated as lipoate protein ligases. Biochemistry 49:10024-10036.
8. Crasnier-Mednansky, M. 2008. Is there any role for cAMP-CRP in carbon catabolite repression of the Escherichia coli lac operon? Nat. Rev. Microbiol. 6:954; author reply 954.
9. 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.
10. Deutscher, J. 2008. The mechanisms of carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 11:87-93.
11. Dong, Y., J. Wang, H. Fu, G. Zhou, M. Shi, and H. Gao. 2012. A Crp-dependent two-component system regulates nitrate and nitrite respiration in Shewanella oneidensis. PLoS One 7:e51643.
12. Douglas, P., M. Kriek, P. Bryant, and P. L. Roach. 2006. Lipoyl synthase inserts sulfur atoms into an octanoyl substrate in a stepwise manner. Angew. Chem. 45:5197-5199.
13. Engel, N., K. van den Daele, U. Kolukisaoglu, K. Morgenthal, W. Weckwerth, T. Parnik, et al. 2007. Deletion of glycine decarboxylase in Arabidopsis is lethal under nonphotorespiratory conditions. Plant Physiol. 144:1328-1335.
14. Feng, Y., and J. E. Cronan. 2009a. Escherichia coli unsaturated fatty acid synthesis: complex transcription of the fabA gene and in vivo identification of the essential reaction catalyzed by FabB. J. Biol. Chem. 284:29526-29535.
15. Feng, Y., and J. E. Cronan. 2009b. A new member of the Escherichia coli fad regulon: transcriptional regulation of fadM (ybaW). J. Bacteriol. 191:6320-6328.
16. Feng, Y., and J. E. Cronan. 2010. Overlapping repressor binding sites result in additive regulation of Escherichia coli FadH by FadR and ArcA. J. Bacteriol. 192:4289-4299.
17. Feng, Y., and J. E. Cronan. 2011a. Complex binding of the FabR repressor of bacterial unsaturated fatty acid biosynthesis to its cognate promoters. Mol. Microbiol. 80:195-218.
18. Feng, Y., and J. E. Cronan. 2011b. The Vibrio cholerae fatty acid regulatory protein, FadR, represses transcription of plsB, the gene encoding the first enzyme of membrane phospholipid biosynthesis. Mol. Microbiol. 81:1020-1033.
19. Feng, Y., and J. E. Cronan. 2012. Crosstalk of Escherichia coli FadR with global regulators in expression of fatty acid transport genes. PLoS One 7:e46275.
20. Feng, Y., and J. E. Cronan. 2014. PdhR, the pyruvate dehydrogenase repressor, does not regulate lipoic acid synthesis. Res. Microbiol. 165:429-438.
21. Feng, Y., J. Xu, H. Zhang, Z. Chen, and S. Srinivas. 2013a. Brucella BioR regulator defines a complex regulatory mechanism for bacterial biotin metabolism. J. Bacteriol. 195:3451-3467.
22. Feng, Y., H. Zhang, and J. E. Cronan. 2013b. Profligate biotin synthesis in α-proteobacteria - a developing or degenerating regulatory system? Mol. Microbiol. 88:77-92.
23. Feng, Y., B. A. Napier, M. Manandhar, S. K. Henke, D. S. Weiss, and J. E. Cronan. 2014. A Francisella virulence factor catalyses an essential reaction of biotin synthesis. Mol. Microbiol. 91:300-314.
24. Fredrickson, J. K., and M. F. Romine. 2005. Genome-assisted analysis of dissimilatory metal-reducing bacteria. Curr. Opin. Biotechnol. 16:269-274.
25. Fredrickson, J. K., M. F. Romine, A. S. Beliaev, J. M. Auchtung, M. E. Driscoll, T. S. Gardner, et al. 2008. Towards environmental systems biology of Shewanella. Nat. Rev. Microbiol. 6:592-603.
26. Fu, H., H. Chen, J. Wang, G. Zhou, H. Zhang, L. Zhang, et al. 2013. Crp-dependent cytochrome bd oxidase confers nitrite resistance to Shewanella oneidensis. Environ. Microbiol. 15:2198-2212.
27. Fu, H., M. Jin, L. Ju, Y. Mao, and H. Gao. 2014. Evidence for function overlapping of CymA and the cytochrome bc1 complex in the Shewanella oneidensis nitrate and nitrite respiration. Environ. Microbiol. 16:3181-3195.
28. Gao, H., X. Wang, Z. Yang, T. Palzkill, and J. Zhou. 2008. Probing regulon of ArcA in Shewanella oneidensis MR-1 by integrated genomic analyses. BMC Genom. 9:42.
29. Gao, H., X. Wang, Z. K. Yang, J. Chen, Y. Liang, H. Chen, et al. 2010. Physiological roles of ArcA, Crp, and EtrA and their interactive control on aerobic and anaerobic respiration in Shewanella oneidensis. PLoS One 5:e15295.
30. Goble, A. M., Y. Feng, F. M. Raushel, and J. E. Cronan. 2013. Discovery of a cAMP deaminase that quenches cyclic AMP-dependent regulation. ACS Chem. Biol. 8:2622-2629.
31. Gohler, A. K., O. Kokpinar, W. Schmidt-Heck, R. Geffers, R. Guthke, U. Rinas, et al. 2011. More than just a metabolic regulator-elucidation and validation of new targets of PdhR in Escherichia coli. BMC Syst. Biol. 5:197.
32. Gorke, B., and J. Stulke. 2008. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat. Rev. Microbiol. 6:613-624.
33. Green, J., M. R. Stapleton, L. J. Smith, P. J. Artymiuk, C. Kahramanoglou, D. M. Hunt, et al. 2014. Cyclic-AMP and bacterial cyclic-AMP receptor proteins revisited: adaptation for different ecological niches. Curr. Opin. Microbiol. 18:1-7.
34. Haldimann, A., and B. L. Wanner. 2001. Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J. Bacteriol. 183:6384-6393.
35. Hanamura, A., and H. Aiba. 1991. Molecular mechanism of negative autoregulation of Escherichia coli crp gene. Nucleic Acids Res. 19:4413-4419.
36. Hanamura, A., and H. Aiba. 1992. A new aspect of transcriptional control of the Escherichia coli crp gene: positive autoregulation. Mol. Microbiol. 6:2489-2497.
37. Hantke, K., K. Winkler, and J. E. Schultz. 2011. Escherichia coli exports cyclic AMP via TolC. J. Bacteriol. 193:1086-1089.
38. 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.
39. Imamura, R., K. Yamanaka, T. Ogura, S. Hiraga, N. Fujita, A. Ishihama, et al. 1996. Identification of the cpdA gene encoding cyclic 3′, 5′-adenosine monophosphate phosphodiesterase in Escherichia coli. J. Biol. Chem. 271:25423-25429.
40. Ishizuka, H., A. Hanamura, T. Inada, and H. Aiba. 1994. Mechanism of the down-regulation of cAMP receptor protein by glucose in Escherichia coli: role of autoregulation of the crp gene. EMBO J. 13:3077-3082.
41. Jin, M., Y. Jiang, L. Sun, J. Yin, H. Fu, G. Wu, et al. 2013. Unique organizational and functional features of the cytochrome c maturation system in Shewanella oneidensis. PLoS One 8:e75610.
42. Jordan, S. W., and J. E. Cronan, Jr. 2003. The Escherichia coli lipB gene encodes lipoyl (octanoyl)-acyl carrier protein:protein transferase. J. Bacteriol. 185:1582-1589.
43. Kaleta, C., A. Gohler, S. Schuster, K. Jahreis, R. Guthke, and S. Nikolajewa. 2010. Integrative inference of gene-regulatory networks in Escherichia coli using information theoretic concepts and sequence analysis. BMC Syst. Biol. 4:116.
44. Kozlov, G., D. Elias, A. Semesi, A. Yee, M. Cygler, and K. Gehring. 2004. Structural similarity of YbeD protein from Escherichia coli to allosteric regulatory domains. J. Bacteriol. 186:8083-8088.
45. -ΔΔCT method. Methods 25:402-408.
46. Miller, J. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Miller, J. H. 1992. A short course in bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
48. 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.
49. Morris, T. W., K. E. Reed, and J. E. Cronan, Jr. 1995. Lipoic acid metabolism in Escherichia coli: the lplA and lipB genes define redundant pathways for ligation of lipoyl groups to apoprotein. J. Bacteriol. 177:1-10.
50. Narang, A. 2009. cAMP does not have an important role in carbon catabolite repression of the Escherichia coli lac operon. Nat. Rev. Microbiol. 7:250.
51. Novichkov, P. S., O. N. Laikova, E. S. Novichkova, M. S. Gelfand, A. P. Arkin, I. Dubchak, et al. 2010a. RegPrecise: a database of curated genomic inferences of transcriptional regulatory interactions in prokaryotes. Nucleic Acids Res. 38:D111-D118.
52. Novichkov, P. S., D. A. Rodionov, E. D. Stavrovskaya, E. S. Novichkova, A. E. Kazakov, M. S. Gelfand, et al. 2010b. RegPredict: an integrated system for regulon inference in prokaryotes by comparative genomics approach. Nucleic Acids Res. 38:W299-W307.
53. Novichkov, P. S., A. E. Kazakov, D. A. Ravcheev, S. A. Leyn, G. Y. Kovaleva, R. A. Sutormin, et al. 2013. RegPrecise 3.0 - a resource for genome-scale exploration of transcriptional regulation in bacteria. BMC Genom. 14:745.
54. Pastan, I., and R. Perlman. 1970. Cyclic adenosine monophosphate in bacteria. Science 169:339-344.
55. Perham, R. N. 2000. Swinging arms and swinging domains in multifunctional enzymes: catalytic machines for multistep reactions. Annu. Rev. Biochem. 69:961-1004.
56. Qu, S., Y. Zhang, L. Liu, L. Wang, Y. Han, R. Yang, et al. 2013. Cyclic AMP receptor protein is a repressor of adenylyl cyclase gene cyaA in Yersinia pestis. Can. J. Microbiol. 59:304-310.
57. Reche, P. A. 2000. Lipoylating and biotinylating enzymes contain a homologous catalytic module. Protein Sci. 9:1922-1929.
58. Reed, L. J. 2001. A trail of research from lipoic acid to alpha-keto acid dehydrogenase complexes. J. Biol. Chem. 276:38329-38336.
59. Reed, K. E., and J. E. Cronan, Jr. 1993. Lipoic acid metabolism in Escherichia coli: sequencing and functional characterization of the lipA and lipB genes. J. Bacteriol. 175:1325-1336.
60. Reed, K. E., T. W. Morris, and J. E. Cronan, Jr. 1994. Mutants of Escherichia coli K-12 that are resistant to a selenium analog of lipoic acid identify unknown genes in lipoate metabolism. Proc. Natl. Acad. Sci. USA 91:3720-3724.
61. Rock, C. O. 2009. Opening a new path to lipoic acid. J. Bacteriol. 191:6782-6784.
62. Rodionov, D. A., C. Yang, X. Li, I. A. Rodionova, Y. Wang, A. Y. Obraztsova, et al. 2010. Genomic encyclopedia of sugar utilization pathways in the Shewanella genus. BMC Genom. 11:494.
63. Rodionov, D. A., P. S. Novichkov, E. D. Stavrovskaya, I. A. Rodionova, X. Li, M. D. Kazanov, et al. 2011. Comparative genomic reconstruction of transcriptional networks controlling central metabolism in the Shewanella genus. BMC Genom. 12(Suppl. 1):S3.
64. Romine, M. F., T. S. Carlson, A. D. Norbeck, L. A. McCue, and M. S. Lipton. 2008. Identification of mobile elements and pseudogenes in the Shewanella oneidensis MR-1 genome. Appl. Environ. Microbiol. 74:3257-3265.
65. Saffarini, D. A., R. Schultz, and A. Beliaev. 2003. Involvement of cyclic AMP (cAMP) and cAMP receptor protein in anaerobic respiration of Shewanella oneidensis. J. Bacteriol. 185:3668-3671.
66. Schultz, S. C., G. C. Shields, and T. A. Steitz. 1991. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science 253:1001-1007.
67. Wu, L., J. Wang, P. Tang, H. Chen, and H. Gao. 2011. Genetic and molecular characterization of flagellar assembly in Shewanella oneidensis. PLoS One 6:e21479.
68. You, C., H. Okano, S. Hui, Z. Zhang, M. Kim, C. W. Gunderson, et al. 2013. Coordination of bacterial proteome with metabolism by cyclic AMP signalling. Nature 500:301-306.
69. Zhao, X., J. R. Miller, Y. Jiang, M. A. Marletta, and J. E. Cronan. 2003. Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem. Biol. 10:1293-1302.
70. 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.
71. Zheng, D., C. Constantinidou, J. L. Hobman, and S. D. Minchin. 2004. Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res. 32:5874-5893.
72. Zhou, G., J. Yin, H. Chen, Y. Hua, L. Sun, and H. Gao. 2013. Combined effect of loss of the caa 3 oxidase and Crp regulation drives Shewanella to thrive in redox-stratified environments. ISME J. 7:1752-1763.