Transcriptional repression of the VC2105 protein by Vibrio FadR suggests that it is a new auxiliary member of the fad regulon

Applied and Environmental Microbiology

Volumn 82, Issue 9, 2016, Pages 2819-2832

  Gao, Rongsui ^a   Lin, Jingxia ^a   Zhang, Han ^a   Feng, Youjun ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; BINS; ELECTROPHORETIC MOBILITY; ESCHERICHIA COLI; GENE ENCODING; GENE EXPRESSION; GENES; LIGANDS; PROTEINS; SURFACE PLASMON RESONANCE;

DIRECT INTERACTIONS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EXPRESSION LEVELS; LIGAND-BINDING SITES; REGULATORY PROTEIN; TRANSCRIPTIONAL FUSION; TRANSCRIPTIONAL REGULATION; TRANSCRIPTIONAL REPRESSION;

FATTY ACIDS;

BACTERIUM; BIOASSAY; BIODEGRADATION; ENZYME ACTIVITY; FATTY ACID; GENE EXPRESSION; HOMOGENEITY; LIGAND; PROTEIN;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; VIBRIO; VIBRIO CHOLERAE;

ACYL COENZYME A; BACTERIAL DNA; BACTERIAL PROTEIN; BETA GALACTOSIDASE; ESCHERICHIA COLI PROTEIN; FADR PROTEIN, BACTERIA; FATTY ACID; FIMBRIA PROTEIN; PROTEIN BINDING; REPRESSOR PROTEIN; TCPA PROTEIN, VIBRIO CHOLERAE; TRANSCRIPTION FACTOR;

BINDING SITE; BIOSYNTHESIS; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROCEDURES; PROMOTER REGION; REGULON; SURFACE PLASMON RESONANCE; VIBRIO CHOLERAE;

ACYL COENZYME A; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; BINDING SITES; DNA, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FATTY ACIDS; FIMBRIAE PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REGULON; REPRESSOR PROTEINS; SURFACE PLASMON RESONANCE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VIBRIO CHOLERAE;

EID: 84965165631     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00293-16     Document Type: Article

References (46)

1. Marrakchi H, Zhang YM, Rock CO. 2002. Mechanistic diversity and regulation of Type II fatty acid synthesis. Biochem Soc Trans 30:1050-1055. http://dx.doi.org/10.1042/bst0301050.
2. Fujita Y, Matsuoka H, Hirooka K. 2007. Regulation of fatty acid metabolism in bacteria. Mol Microbiol 66:829-839. http://dx.doi.org/10.1111/j.1365-2958.2007.05947.x.
3. Cronan JE. 4 January 2014. Biotin and lipoic acid: synthesis, attachment, and regulation. EcoSal Plus 2014 http://dx.doi.org/10.1128/ecosalplus.ESP-0001-2012.
4. Feng Y, Cronan JE. 2009. 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. http://dx.doi.org/10.1074/jbc.M109.023440.
5. Feng Y, Cronan JE. 2009. A new member of the Escherichia coli fad regulon: transcriptional regulation of fadM (ybaW). J Bacteriol 191:6320-6328. http://dx.doi.org/10.1128/JB.00835-09.
6. Feng Y, Cronan JE. 2012. Crosstalk of Escherichia coli FadR with global regulators in expression of fatty acid transport genes. PLoS One 7:e46275. http://dx.doi.org/10.1371/journal.pone.0046275.
7. Campbell JW, Morgan-Kiss RM, Cronan JE, Jr. 2003. A new Escherichia coli metabolic competency: growth on fatty acids by a novel anaerobic beta-oxidation pathway. Mol Microbiol 47:793-805. http://dx.doi.org/10.1046/j.1365-2958.2003.03341.x.
8. Henry MF, Cronan JE, Jr. 1992. A new mechanism of transcriptional regulation: release of an activator triggered by small molecule binding. Cell 70:671-679. http://dx.doi.org/10.1016/0092-8674(92)90435-F.
9. Henry MF, Cronan JE, Jr. 1991. Escherichia coli transcription factor that both activates fatty acid synthesis and represses fatty acid degradation. J Mol Biol 222:843-849. http://dx.doi.org/10.1016/0022-2836(91)90574-P.
10. Feng Y, Cronan JE. 2011. Complex binding of the FabR repressor of bacterial unsaturated fatty acid biosynthesis to its cognate promoters. Mol Microbiol 80:195-218. http://dx.doi.org/10.1111/j.1365-2958.2011.07564.x.
11. Zhu K, Zhang YM, Rock CO. 2009. Transcriptional regulation of membrane lipid homeostasis in Escherichia coli. J Biol Chem 284:34880-34888. http://dx.doi.org/10.1074/jbc.M109.068239.
12. Zhang YM, Marrakchi H, Rock CO. 2002. The FabR (YijC) transcription factor regulates unsaturated fatty acid biosynthesis in Escherichia coli. J Biol Chem 277:15558-15565. http://dx.doi.org/10.1074/jbc.M201399200.
13. Iram SH, Cronan JE. 2006. The β-oxidation systems of Escherichia coli and Salmonella enterica are not functionally equivalent. J Bacteriol 188:599-608. http://dx.doi.org/10.1128/JB.188.2.599-608.2006.
14. Clark D. 1981. Regulation of fatty acid degradation in Escherichia coli: analysis by operon fusion. J Bacteriol 148:521-526.
15. Feng Y, Cronan JE. 2010. Overlapping repressor binding sites result in additive regulation of Escherichia coli FadH by FadR and ArcA. J Bacteriol 192:4289-4299. http://dx.doi.org/10.1128/JB.00516-10.
16. Campbell JW, Cronan JE, Jr. 2001. Escherichia coli FadR positively regulates transcription of the fabB fatty acid biosynthetic gene. J Bacteriol 183:5982-5990. http://dx.doi.org/10.1128/JB.183.20.5982-5990.2001.
17. Cronan JE, Jr. 1997. In vivo evidence that acyl coenzyme A regulates DNA binding by the Escherichia coli FadR global transcription factor. J Bacteriol 179:1819-1823.
18. Xu Y, Heath RJ, Li Z, Rock CO, White SW. 2001. The FadR·DNA complex: transcriptional control of fatty acid metabolism in Escherichia coli. J Biol Chem 276:17373-17379. http://dx.doi.org/10.1074/jbc.M100195200.
19. van Aalten DM, DiRusso CC, Knudsen J. 2001. The structural basis of acyl coenzyme A-dependent regulation of the transcription factor FadR. EMBO J 20:2041-2050. http://dx.doi.org/10.1093/emboj/20.8.2041.
20. van Aalten DM, DiRusso CC, Knudsen J, Wierenga RK. 2000. Crystal structure of FadR, a fatty acid-responsive transcription factor with a novel acyl coenzyme A-binding fold. EMBO J 19:5167-5177. http://dx.doi.org/10.1093/emboj/19.19.5167.
21. Zhang Y, Gao R, Ye H, Wang Q, Feng Y. 2014. A new glimpse of FadR-DNA crosstalk revealed by deep dissection of the E. coli FadR regulatory protein. Protein Cell 5:928-939. http://dx.doi.org/10.1007/s13238-014-0107-3.
22. Iram SH, Cronan JE. 2005. Unexpected functional diversity among FadR fatty acid transcriptional regulatory proteins. J Biol Chem 280:32148-32156. http://dx.doi.org/10.1074/jbc.M504054200.
23. Thompson FL, Gevers D, Thompson CC, Dawyndt P, Naser S, Hoste B, Munn CB, Swings J. 2005. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl Environ Microbiol 71:5107-5115. http://dx.doi.org/10.1128/AEM.71.9.5107-5115.2005.
24. Boyd EF, Carpenter MR, Chowdhury N, Cohen AL, Haines-Menges BL, Kalburge SS, Kingston JJ, Lubin JB, Ongagna-Yhombi SY, Whitaker WB. 2015. Post-genomic analysis of members of the family Vibrionaceae. Microbiol Spectr 3(5):VE-0009-2014. http://dx.doi.org/10.1128/microbiolspec.VE-0009-2014.
25. Plecha SC, Withey JH. 2015. Mechanism for inhibition of Vibrio cholerae ToxT activity by the unsaturated fatty acid components of bile. J Bacteriol 197:1716-1725. http://dx.doi.org/10.1128/JB.02409-14.
26. Withey JH, Nag D, Plecha SC, Sinha R, Koley H. 2015. Conjugated linoleic acid reduces cholera toxin production in vitro and in vivo by inhibiting Vibrio cholerae ToxT activity. Antimicrob Agents Chemother 59: 7471-7476. http://dx.doi.org/10.1128/AAC.01029-15.
27. Brown RN, Gulig PA. 2008. Regulation of fatty acid metabolism by FadR is essential for Vibrio vulnificus to cause infection of mice. J Bacteriol 190:7633-7644. http://dx.doi.org/10.1128/JB.01016-08.
28. Ray S, Chatterjee E, Chatterjee A, Paul K, Chowdhury R. 2011. A fadD mutant of Vibrio cholerae is impaired in the production of virulence factors and membrane localization of the virulence regulatory protein TcpP. Infect Immun 79:258-266. http://dx.doi.org/10.1128/IAI.00663-10.
29. Chatterjee E, Chowdhury R. 2013. Reduced virulence of the Vibrio cholerae fadD mutant is due to induction of the extracytoplasmic stress response. Infect Immun 81:3935-3941. http://dx.doi.org/10.1128/IAI.00722-13.
30. Chatterjee A, Dutta PK, Chowdhury R. 2007. Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infect Immun 75:1946-1953. http://dx.doi.org/10.1128/IAI.01435-06.
31. Zhang H, Zheng B, Gao R, Feng Y. 2015. Binding of Shewanella FadR to the fabA fatty acid biosynthetic gene: implications for contraction of the fad regulon. Protein Cell 6:667-679. http://dx.doi.org/10.1007/s13238-015-0172-2.
32. Feng Y, Cronan JE. 2011. 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. http://dx.doi.org/10.1111/j.1365-2958.2011.07748.x.
33. Shi W, Kovacikova G, Lin W, Taylor RK, Skorupski K, Kull FJ. 2015. The 40-residue insertion in Vibrio cholerae FadR facilitates binding of an additional fatty acyl-CoA ligand. Nat Commun 6:6032. http://dx.doi.org/10.1038/ncomms7032.
34. Joelsson A, Liu Z, Zhu J. 2006. Genetic and phenotypic diversity of quorum-sensing systems in clinical and environmental isolates of Vibrio cholerae. Infect Immun 74:1141-1147. http://dx.doi.org/10.1128/IAI.74.2.1141-1147.2006.
35. Metcalf WW, Jiang W, Daniels LL, Kim SK, Haldimann A, Wanner BL.1996. Conditionally replicative and conjugative plasmids carrying lacZα for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35: 1-13. http://dx.doi.org/10.1006/plas.1996.0001.
36. Miller JH. 1992. A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. de Jong A, Pietersma H, Cordes M, Kuipers OP, Kok J. 2012. PePPER: a webserver for prediction of prokaryote promoter elements and regulons. BMC Genomics 13:299. http://dx.doi.org/10.1186/1471-2164-13-299.
38. Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462. http://dx.doi.org/10.1126/science.277.5331.1453.
39. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Umayam L, Gill SR, Nelson KE, Read TD, Tettelin H, Richardson D, Ermolaeva MD, Varnathevan J, Bass S, Haiying W, Dragoi I, Sellers P, McDonald L, Utterback T, Fleishmann RD, Nierman WC, White O, Salzberg SL, Smith HO, Colwell RR, Mekalanos JJ, Venter JC, Fraser CM. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477-483. http://dx.doi.org/10.1038/35020000.
40. Rodionov DA, Novichkov PS, Stavrovskaya ED, Rodionova IA, Li X, Kazanov MD, Ravcheev DA, Gerasimova AV, Kazakov AE, Kovaleva GY, Permina EA, Laikova ON, Overbeek R, Romine MF, Fredrickson JK, Arkin AP, Dubchak I, Osterman AL, Gelfand MS. 2011. Comparative genomic reconstruction of transcriptional networks controlling central metabolism in the Shewanella genus. BMC Genomics 12(Suppl 1):S3. http://dx.doi.org/10.1186/1471-2164-12-S1-S3.
41. Connell TD, Martone AJ, Holmes RK. 1995. A new mobilizable cosmid vector for use in Vibrio cholerae and other gram-negative bacteria. Gene 153:85-87. http://dx.doi.org/10.1016/0378-1119(94)00804-2.
42. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose pBAD promoter. J Bacteriol 177:4121-4130.
43. Haldimann A, Wanner BL. 2001. Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J Bacteriol 183:6384-6393. http://dx.doi.org/10.1128/JB.183.21.6384-6393.2001.
44. Bellair M, Withey JH. 2008. Flexibility of Vibrio cholerae ToxT in transcription activation of genes having altered promoter spacing. J Bacteriol 190:7925-7931. http://dx.doi.org/10.1128/JB.00512-08.
45. Withey JH, Dirita VJ. 2005. Vibrio cholerae ToxT independently activates the divergently transcribed aldA and tagA genes. J Bacteriol 187:7890-7900. http://dx.doi.org/10.1128/JB.187.23.7890-7900.2005.
46. Linn T, St Pierre R. 1990. Improved vector system for constructing transcriptional fusions that ensures independent translation of lacZ. J Bacteriol 172:1077-1084.