Xanthomonas campestrisRpfB is a fatty Acyl-CoA ligase required to counteract the thioesterase activity of the RpfF diffusible signal factor (DSF) synthase

Molecular Microbiology

Volumn 93, Issue 2, 2014, Pages 262-275

  Bi, Hongkai ^a   Yu, Yonghong ^b   Dong, Huijuan ^b   Wang, Haihong ^b   Cronan, John E ^a  

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

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL CARRIER PROTEIN; ACYL COENZYME A; DIFFUSIBLE SIGNAL FACTOR SYNTHASE; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FATTY ACID; LONG CHAIN FATTY ACID COENZYME A LIGASE; MEMBRANE LIPID; RPFB PROTEIN; RPFF PROTEIN; SYNTHETASE; THIOL ESTER HYDROLASE; UNCLASSIFIED DRUG; ACYL-COENZYME A SYNTHETASE, E COLI; BACTERIAL PROTEIN; COENZYME A LIGASE; ESCHERICHIA COLI PROTEIN; LIGASE; LONG-CHAIN-FATTY-ACID-(ACYL-CARRIER-PROTEIN) LIGASE; MULTIFUNCTIONAL ENZYME;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIABILITY; CARBON SOURCE; CYTOLYSIS; ENZYME SPECIFICITY; ESCHERICHIA COLI; FATTY ACID OXIDATION; HETEROLOGOUS EXPRESSION; LIPOGENESIS; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; RPFB GENE; RPFF GENE; VIBRIO HARVEYI; XANTHOMONAS CAMPESTRIS; DIFFUSION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; MUTATION; OXIDATION REDUCTION REACTION; PATHOGENICITY; PLANT DISEASE; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA; ESCHERICHIA COLI; VIBRIO HARVEYI; XANTHOMONAS; XANTHOMONAS CAMPESTRIS PV. CAMPESTRIS;

ACYL COENZYME A; BACTERIAL PROTEINS; CARBON-SULFUR LIGASES; COENZYME A LIGASES; DIFFUSION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FATTY ACIDS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; MULTIFUNCTIONAL ENZYMES; MULTIGENE FAMILY; MUTATION; OXIDATION-REDUCTION; PLANT DISEASES; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; THIOLESTER HYDROLASES; XANTHOMONAS CAMPESTRIS;

EID: 84904050427     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12657     Document Type: Article

References (37)

1. Almeida, R.P., Killiny, N., Newman, K.L., Chatterjee, S., Ionescu, M., and Lindow, S.E. (2012) Contribution of rpfB to cell-to-cell signal synthesis, virulence, and vector transmission of Xylella fastidiosa. Mol Plant Microbe Interact 25: 453-462.
2. An, S.Q., Febrer, M., McCarthy, Y., Tang, D.J., Clissold, L., Kaithakottil, G., etal. (2013) High-resolution transcriptional analysis of the regulatory influence of cell-to-cell signalling reveals novel genes that contribute to Xanthomonas phytopathogenesis. Mol Microbiol 88: 1058-1069.
3. Bar-Tana, J., Rose, G., and Shapiro, B. (1971) The purification and properties of microsomal palmitoyl-coenzyme A synthetase. Biochem J 122: 353-362.
4. Barber, C.E., Tang, J.L., Feng, J.X., Pan, M.Q., Wilson, T.J., Slater, H., etal. (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24: 555-566.
5. Bi, H., Christensen, Q.H., Feng, Y., Wang, H., and Cronan, J.E. (2012) The Burkholderia cenocepacia BDSF quorum sensing fatty acid is synthesized by a bifunctional crotonase homologue having both dehydratase and thioesterase activities. Mol Microbiol 83: 840-855.
6. Bishop, R.E. (2008) Structural biology of membrane-intrinsic beta-barrel enzymes: sentinels of the bacterial outer membrane. Biochim Biophys Acta 1778: 1881-1896.
7. Black, P.N., and DiRusso, C.C. (2003) Transmembrane movement of exogenous long-chain fatty acids: proteins, enzymes, and vectorial esterification. Microbiol Mol Biol Rev 67: 454-472.
8. Brok, R.G., Boots, A.P., Dekker, N., Verheij, H.M., and Tommassen, J. (1998) Sequence comparison of outer membrane phospholipases A: implications for structure and for the catalytic mechanism. Res Microbiol 149: 703-710.
9. Campbell, J.W., and Cronan, J.E., Jr (2002) The enigmatic Escherichia coli fadE gene is yafH. J Bacteriol 184: 3759-3764.
10. Campbell, J.W., Morgan-Kiss, R.M., and Cronan, J.E., Jr (2003) A new Escherichia coli metabolic competency: growth on fatty acids by a novel anaerobic beta-oxidation pathway. Mol Microbiol 47: 793-805.
11. Cheng, Z., He, Y.W., Lim, S.C., Qamra, R., Walsh, M.A., Zhang, L.H., and Song, H. (2010) Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. Structure 18: 1199-1209.
12. Cronan, J.E., and Thomas, J. (2009) Bacterial fatty acid synthesis and its relationships with polyketide synthetic pathways. Methods Enzymol 459: 395-433.
13. Daniels, M.J., Barber, C.E., Turner, P.C., Sawczyc, M.K., Byrde, R.J., and Fielding, A.H. (1984) Cloning of genes involved in pathogenicity of Xanthomonas campestris pv. campestris using the broad host range cosmid pLAFR1. EMBO J 3: 3323-3328.
14. Deng, Y., Wu, J., Tao, F., and Zhang, L.H. (2011) Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem Rev 111: 160-173.
15. Dow, M. (2008) Diversification of the function of cell-to-cell signaling in regulation of virulence within plant pathogenic xanthomonads. Sci Signal 1: pe23.
16. Feng, Y., and Cronan, J.E. (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.
17. Gulick, A.M. (2009) Conformational dynamics in the Acyl-CoA synthetases, adenylation domains of non-ribosomal peptide synthetases, and firefly luciferase. ACS Chem Biol 4: 811-827.
18. He, Y.W., Wang, C., Zhou, L., Song, H., Dow, J.M., and Zhang, L.H. (2006) Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein interaction. J Biol Chem 281: 33414-33421.
19. Hisanaga, Y., Ago, H., Nakagawa, N., Hamada, K., Ida, K., Yamamoto, M., etal. (2004) Structural basis of the substrate-specific two-step catalysis of long chain fatty acyl-CoA synthetase dimer. J Biol Chem 279: 31717-31726.
20. Huang, T.P., and Wong, A.C. (2007) Extracellular fatty acids facilitate flagella-independent translocation by Stenotrophomonas maltophilia. Res Microbiol 158: 702-711.
21. Ionescu, M., Baccari, C., Da Silva, A.M., Garcia, A., Yokota, K., and Lindow, S.E. (2013) Diffusible signal factor (DSF) synthase RpfF of Xylella fastidiosa is a multifunction protein also required for response to DSF. J Bacteriol 195: 5273-5284.
22. Jiang, Y., Chan, C.H., and Cronan, J.E. (2006) The soluble acyl-acyl carrier protein synthetase of Vibrio harveyi B392 is a member of the medium chain acyl-CoA synthetase family. Biochemistry 45: 10008-10019.
23. Jiang, Y., Morgan-Kiss, R.M., Campbell, J.W., Chan, C.H., and Cronan, J.E. (2010) Expression of Vibrio harveyi acyl-ACP synthetase allows efficient entry of exogenous fatty acids into the Escherichia coli fatty acid and lipid A synthetic pathways. Biochemistry 49: 718-726.
24. Kang, Y., Zarzycki-Siek, J., Walton, C.B., Norris, M.H., and Hoang, T.T. (2010) Multiple FadD acyl-CoA synthetases contribute to differential fatty acid degradation and virulence in Pseudomonas aeruginosa. PLoS ONE 5: e13557.
25. Kazakov, A.E., Rodionov, D.A., Alm, E., Arkin, A.P., Dubchak, I., and Gelfand, M.S. (2009) Comparative genomics of regulation of fatty acid and branched-chain amino acid utilization in proteobacteria. J Bacteriol 191: 52-64.
26. Lennen, R.M., Politz, M.G., Kruziki, M.A., and Pfleger, B.F. (2013) Identification of transport proteins involved in free fatty acid efflux in Escherichia coli. J Bacteriol 195: 135-144.
27. Morgan-Kiss, R.M., and Cronan, J.E. (2004) The Escherichia coli fadK (ydiD) gene encodes an anerobically regulated short chain acyl-CoA synthetase. J Biol Chem 279: 37324-37333.
28. Overath, P., Pauli, G., and Schairer, H.U. (1969) Fatty acid degradation in Escherichia coli. An inducible acyl-CoA synthetase, the mapping of old-mutations, and the isolation of regulatory mutants. Eur J Biochem 7: 559-574.
29. Post-Beittenmiller, D., Jaworski, J.G., and Ohlrogge, J.B. (1991) In vivo pools of free and acylated acyl carrier proteins in spinach. Evidence for sites of regulation of fatty acid biosynthesis. J Biol Chem 266: 1858-1865.
30. Ryan, R.P. (2013) Cyclic di-GMP signalling and the regulation of bacterial virulence. Microbiology 159: 1286-1297.
31. Ryan, R.P., and Dow, J.M. (2011) Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol 19: 145-152.
32. Trivedi, O.A., Arora, P., Sridharan, V., Tickoo, R., Mohanty, D., and Gokhale, R.S. (2004) Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 428: 441-445.
33. Wang, L.H., He, Y., Gao, Y., Wu, J.E., Dong, Y.H., He, C., etal. (2004) A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51: 903-912.
34. Weimar, J.D., DiRusso, C.C., Delio, R., and Black, P.N. (2002) Functional role of fatty acyl-coenzyme A synthetase in the transmembrane movement and activation of exogenous long-chain fatty acids. Amino acid residues within the ATP/AMP signature motif of Escherichia coli FadD are required for enzyme activity and fatty acid transport. J Biol Chem 277: 29369-29376.
35. Wengelnik, K., Marie, C., Russel, M., and Bonas, U. (1996) Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction ofthe hypersensitive reaction. J Bacteriol 178: 1061-1069.
36. Zhang, Y.M., and Rock, C.O. (2008) Thematic review series: glycerolipids. Acyltransferases in bacterial glycerophospholipid synthesis. J Lipid Res 49: 1867-1874.
37. Zhu, L., Lin, J., Ma, J., Cronan, J.E., and Wang, H. (2010) Triclosan resistance of Pseudomonas aeruginosa PAO1 is due to FabV, a triclosan-resistant enoyl-acyl carrier protein reductase. Antimicrob Agents Chemother 54: 689-698.