Actinobacterial acyl coenzyme A synthetases involved in steroid side-chain catabolism

Journal of Bacteriology

Volumn 196, Issue 3, 2014, Pages 579-587

  Casabon, Israël ^a   Swain, Kendra ^a   Crowe, Adam M ^a   Eltis, Lindsay D ^a   Mohn, William W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; LONG CHAIN FATTY ACID; LONG CHAIN FATTY ACID COENZYME A LIGASE;

AMINO ACID SEQUENCE; ARTICLE; CARBON CYCLE; CATABOLISM; CHEMICAL STRUCTURE; GENE CLUSTER; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHYLOGENY; PREDICTION; PRIORITY JOURNAL; STEADY STATE; STEROID METABOLISM;

COENZYME A LIGASES; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR STRUCTURE; MYCOBACTERIUM TUBERCULOSIS; PHYLOGENY; STEROIDS;

EID: 84892385885     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01012-13     Document Type: Article

References (57)

1. Gimpl G, Burger K, Fahrenholz F. 1997. Cholesterol as modulator of receptor function. Biochemistry 36:10959-10974. http://dx.doi.org/10.1021/bi963138w.
2. Donova MV, Egorova OV. 2012. Microbial steroid transformations: current state and prospects. Appl. Microbiol. Biotechnol. 94:1423-1447. http://dx.doi.org/10.1007/s00253-012-4078-0.
3. Ouellet H, Johnston JB, Ortiz de Montellano PR. 2011. Cholesterol catabolism as a therapeutic target in Mycobacterium tuberculosis. Trends Microbiol. 19:530-539. http://dx.doi.org/10.1016/j.tim.2011.07.009.
4. Pandey AK, Sassetti CM. 2008. Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl. Acad. Sci. U. S. A. 105:4376-4380. http://dx.doi.org/10.1073/pnas.0711159105.
5. Yam KC, D'Angelo I, Kalscheuer R, Zhu H, Wang JX, Snieckus V, Ly LH, Converse PJ, Jacobs WR, Jr, Strynadka N, Eltis LD. 2009. Studies of a ring-cleaving dioxygenase illuminate the role of cholesterol metabolism in the pathogenesis of Mycobacterium tuberculosis. PLoS Pathog. 5:e1000344. http://dx.doi.org/10.1371/journal.ppat.1000344.
6. Hofmann AF, Mysels KJ. 1988. Bile salts as biological surfactants. Colloids Surf. 30:145-173.
7. Fernandes P, Cruz A, Angelova B, Pinheiro HM, Cabral JMS. 2003. Microbial conversion of steroid compounds: recent developments. Enzyme Microb. Technol. 32:688-705. http://dx.doi.org/10.1016/S0141-0229(03)00029-2.
8. Philipp B. 2011. Bacterial degradation of bile salts. Appl. Microbiol. Biotechnol. 89:903-915. http://dx.doi.org/10.1007/s00253-010-2998-0.
9. Horinouchi M, Hayashi T, Kudo T. 2012. Steroid degradation in Comamonas testosteroni. J. Steroid Biochem. Mol. Biol. 129:4-14. http://dx.doi.org/10.1016/j.jsbmb.2010.10.008.
10. Birkenmaier A, Holert J, Erdbrink H, Moeller HM, Friemel A, Schoenenberger R, Suter MJ, Klebensberger J, Philipp B. 2007. Biochemical and genetic investigation of initial reactions in aerobic degradation of the bile acid cholate in Pseudomonas sp. strain Chol1. J. Bacteriol. 189:7165-7173. http://dx.doi.org/10.1128/JB.00665-07.
11. Birkenmaier A, Möller HM, Philipp B. 2011. Identification of a thiolase gene essential for ß-oxidation of the acyl side chain of the steroid compound cholate in Pseudomonas sp. strain Chol1. FEMS Microbiol. Lett. 318:123-130. http://dx.doi.org/10.1111/j.1574-6968.2011.02250.x.
12. Holert J, Kulic Z, Yucel O, Suvekbala V, Suter MJ, Moller HM, Philipp B. 2013. Degradation of the acyl side chain of the steroid compound cholate in Pseudomonas sp. strain Chol1 proceeds via an aldehyde intermediate. J. Bacteriol. 195:585-595. http://dx.doi.org/10.1128/JB.01961-12.
13. Yam KC, Okamoto S, Roberts JN, Eltis LD. 2011. Adventures in Rhodococcus-from steroids to explosives. Can. J. Microbiol. 57:155-168. http://dx.doi.org/10.1139/W10-115.
14. Casabon I, Crowe AM, Liu J, Eltis LD. 2013. FadD3 is an acyl-CoA synthetase that initiates catabolism of cholesterol rings C and D in actinobacteria. Mol. Microbiol. 87:269-283. http://dx.doi.org/10.1111/mmi.12095.
15. Petrusma M, Hessels G, Dijkhuizen L, van der Geize R. 2011. Multiplicity of 3-ketosteroid-9α-hydroxylase enzymes in Rhodococcus rhodochrous DSM43269 for the specific degradation of different classes of steroids. J. Bacteriol. 193:3931-3940. http://dx.doi.org/10.1128/JB.00274-11.
16. Thomas ST, Sampson NS. 2013. Mycobacterium tuberculosis utilizes a unique heterotetrameric structure for dehydrogenation of the cholesterol side chain. Biochemistry 52:2895-2904. http://dx.doi.org/10.1021/bi4002979.
17. Thomas ST, VanderVen BC, Sherman DR, Russell DG, Sampson NS. 2011. Pathway profiling in Mycobacterium tuberculosis: elucidation of a cholesterol-derived catabolite and the enzymes that catalyze its metabolism. J. Biol. Chem. 286:43668-43678. http://dx.doi.org/10.1074/jbc.M111.313643.
18. Capyk JK, Kalscheuer R, Stewart GR, Liu J, Kwon H, Zhao R, Okamoto S, Jacobs WR, Jr, Eltis LD, Mohn WW. 2009. Mycobacterial cytochrome P450 125 (cyp125) catalyzes the terminal hydroxylation of C27 steroids. J. Biol. Chem. 284:35534-35542. http://dx.doi.org/10.1074/jbc.M109.072132.
19. Rosloniec KZ, Wilbrink MH, Capyk JK, Mohn WW, Ostendorf M, van der Geize R, Dijkhuizen L, Eltis LD. 2009. Cytochrome P450 125 (CYP125) catalyses C26-hydroxylation to initiate sterol side-chain degradation in Rhodococcus jostii RHA1. Mol. Microbiol. 74:1031-1043. http://dx.doi.org/10.1111/j.1365-2958.2009.06915.x.
20. Johnston JB, Ouellet H, Ortiz de Montellano PR. 2010. Functional redundancy of steroid C26-monooxygenase activity in Mycobacterium tuberculosis revealed by biochemical and genetic analyses. J. Biol. Chem. 285:36352-36360. http://dx.doi.org/10.1074/jbc.M110.161117.
21. Ouellet H, Guan S, Johnston JB, Chow ED, Kells PM, Burlingame AL, Cox JS, Podust LM, Ortiz de Montellano PR. 2010. Mycobacterium tuberculosis CYP125A1, a steroid C27 monooxygenase that detoxifies intracellularly generated cholest-4-en-3-one. Mol. Microbiol. 77:730-742. http://dx.doi.org/10.1111/j.1365-2958.2010.07243.x.
22. Groot PHE, Scholte HR, Hulsmann WC. 1976. Fatty acid activation: specificity, localization, and function. Adv. Lipid Res. 14:75-126.
23. Babbitt PC, Kenyon GL, Martin BM, Charest H, Slyvestre M, Scholten JD, Chang KH, Liang PH, Dunaway-Mariano D. 1992. Ancestry of the 4-chlorobenzoate dehalogenase: analysis of amino acid sequence identities among families of acyl:adenyl ligases, enoyl-CoA hydratases/isomerases, and acyl-CoA thioesterases. Biochemistry 31:5594-5604. http://dx.doi.org/10.1021/bi00139a024.
24. Holert J, Jagmann N, Philipp B. 2013. The essential function of genes for a hydratase and an aldehyde dehydrogenase for growth of Pseudomonas sp. strain Chol1 with the steroid compound cholate indicates an aldolytic reaction step for deacetylation of the side chain. J. Bacteriol. 195:3371-3380. http://dx.doi.org/10.1128/JB.00410-13.
25. Mohn WW, Wilbrink MH, Casabon I, Stewart GR, Liu J, van der Geize R, Eltis LD. 2012. Gene cluster encoding cholate catabolism in Rhodococcus spp. J. Bacteriol. 194:6712-6719. http://dx.doi.org/10.1128/JB.01169-12.
26. van der Geize R, Yam K, Heuser T, Wilbrink MH, Hara H, Anderton MC, Sim E, Dijkhuizen L, Davies JE, Mohn WW, Eltis LD. 2007. A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc. Natl. Acad. Sci. U. S. A. 104:1947-1952. http://dx.doi.org/10.1073/pnas.0605728104.
27. Swain K, Casabon I, Eltis LD, Mohn WW. 2012. Two transporters essential for reassimilation of novel cholate metabolites by Rhodococcus jostii RHA1. J. Bacteriol. 194:6720-6727. http://dx.doi.org/10.1128/JB.01167-12.
28. Trivedi OA, Arora P, Sridharan V, Tickoo R, Mohanty D, Gokhale RS. 2004. Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 428:441-445. http://dx.doi.org/10.1038/nature02384.
29. Wilbrink MH, Petrusma M, Dijkhuizen L, van der Geize R. 2011. FadD19 of Rhodococcus rhodochrous DSM43269: a steroid-coenzyme A ligase essential for degradation of C-24 branched sterol side chains. Appl. Environ. Microbiol. 77:4455-4464. http://dx.doi.org/10.1128/AEM.00380-11.
30. Horinouchi M, Hayashi T, Koshino H, Kudo T. 2006. ORF18-disrupted mutant of Comamonas testosteroni TA441 accumulates significant amounts of 9,17-dioxo-1,2,3,4,10,19-hexanorandrostan-5-oic acid and its derivatives after incubation with steroids. J. Steroid Biochem. Mol. Biol. 101:78-84. http://dx.doi.org/10.1016/j.jsbmb.2006.06.006.
31. Griffin JE, Gawronski JD, DeJesus MA, Ioerger TR, Akerley BJ, Sassetti CM. 2011. High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog. 7:e1002251. http://dx.doi.org/10.1371/journal.ppat.1002251.
32. Kapust RB, Tözsér J, Fox JD, Anderson DE, Cherry S, Copeland TD, Waugh DS. 2001. Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng. 14:993-1000. http://dx.doi.org/10.1093/protein/14.12.993.
33. Seto M, Kimbara K, Shimura M, Hatta T, Fukuda M, Yano K. 1995. A novel transformation of polychlorinated biphenyls by Rhodococcus sp. strain RHA1. Appl. Environ. Microbiol. 61:3353-3358.
34. Studier FW, Moffatt BA. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130. http://dx.doi.org/10.1016/0022-2836(86)90385-2.
35. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Capyk JK, Casabon I, Gruninger R, Strynadka NC, Eltis LD. 2011. Activity of 3-ketosteroid 9α-hydroxylase (KshAB) indicates cholesterol side chain and ring degradation occur simultaneously in Mycobacterium tuberculosis. J. Biol. Chem. 286:40717-40724. http://dx.doi.org/10.1074/jbc.M111.289975.
37. Horswill AR, Escalante-Semerena JC. 2002. Characterization of the propionyl-CoA synthetase (PrpE) enzyme of Salmonella enterica: residue Lys592 is required for propionyl-AMP synthesis. Biochemistry 41:2379-2387. http://dx.doi.org/10.1021/bi015647q.
38. Cornish-Bowden A. 1994. Analysis of enzyme kinetic data. Oxford University Press, New York, NY.
39. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882. http://dx.doi.org/10.1093/nar/25.24.4876.
40. Mallonee DH, Adams JL, Hylemon PB. 1992. The bile acid-inducible baiB gene from Eubacterium sp. strain VPI 12708 encodes a bile acidcoenzyme A ligase. J. Bacteriol. 174:2065-2071.
41. Starai VJ, Celic I, Cole RN, Boeke JD, Escalante-Semerena JC. 2002. Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298:2390-2392. http://dx.doi.org/10.1126/science.1077650.
42. Xu H, Hegde SS, Blanchard JS. 2011. The reversible acetylation and inactivation of Mycobacterium tuberculosis acetyl-CoA synthetase is dependent on cAMP. Biochemistry 50:5883-5892. http://dx.doi.org/10.1021/bi200156t.
43. Nambi S, Gupta K, Bhattacharyya M, Ramakrishnan P, Ravikumar V, Siddiqui N, Thomas AT, Visweswariah SS. 2013. Cyclic AMP-dependent protein lysine acylation in mycobacteria regulates fatty acid and propionate metabolism. J. Biol. Chem. 288:14114-14124. http://dx.doi.org/10.1074/jbc.M113.463992.
44. Crosby HA, Rank KC, Rayment I, Escalante-Semerena JC. 2012. Structural insights into the substrate specificity of the Rhodopseudomonas palustris protein acetyltransferase RpPat: identification of a loop critical for recognition by RpPat. J. Biol. Chem. 287:41392-41404. http://dx.doi.org/10.1074/jbc.M112.417360.
45. Chen HP, Zhu SH, Casabon I, Hallam SJ, Crocker FH, Mohn WW, Indest KJ, Eltis LD. 2012. Genomic and transcriptomic studies of an RDX (hexahydro-1,3,5-trinitro-1,3,5-triazine)-degrading actinobacterium. Appl. Environ. Microbiol. 78:7798-7800. http://dx.doi.org/10.1128/AEM.02120-12.
46. McLeod MP, Warren RL, Hsiao WW, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanjh M, Hara H, Petrescu A, Morin RD, Yang G, Stott JM, Schein JE, Shin H, Smailus D, Siddiqui AS, Marra MA, Jones SJ, Holt R, Brinkman FS, Miyauchi K, Fukuda M, Davies JE, Mohn WW, Eltis LD. 2006. The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc. Natl. Acad. Sci. U. S. A. 103:15582-15587. http://dx.doi.org/10.1073/pnas.0607048103.
47. Nesbitt NM, Yang X, Fontán P, Kolesnikova I, Smith I, Sampson NS, Dubnau E. 2010. A thiolase of Mycobacterium tuberculosis is required for virulence and production of androstenedione and androstadienedione from cholesterol. Infect. Immun. 78:275-282. http://dx.doi.org/10.1128/IAI.00893-09.
48. Zou Z, DiRusso CC, Ctrnacta V, Black PN. 2002. Fatty acid transport in Saccharomyces cerevisiae. Directed mutagenesis of FAT1 distinguishes the biochemical activities associated with Fat1p. J. Biol. Chem. 277:31062-31071. http://dx.doi.org/10.1074/jbc.M205034200.
49. Hirsch D, Stahl A, Lodish HF. 1998. A family of fatty acid transporters conserved from mycobacterium to man. Proc. Natl. Acad. Sci. U. S. A. 95:8625-8629. http://dx.doi.org/10.1073/pnas.95.15.8625.
50. Stahl A, Gimeno RE, Tartaglia LA, Lodish HF. 2001. Fatty acid transport proteins: a current view of a growing family. Trends Endocrinol. Metab. 12:266-273. http://dx.doi.org/10.1016/S1043-2760(01)00427-1.
51. Zou Z, Tong F, Faergeman NJ, Borsting C, Black PN, DiRusso CC. 2003. Vectorial acylation in Saccharomyces cerevisiae. Fat1p and fatty acyl-CoA synthetase are interacting components of a fatty acid import complex. J. Biol. Chem. 278:16414-16422. http://dx.doi.org/10.1074/jbc.M210557200.
52. DiRusso CC, Darwis D, Obermeyer T, Black PN. 2008. Functional domains of the fatty acid transport proteins: studies using protein chimeras. Biochim. Biophys. Acta 1781:135-143. http://dx.doi.org/10.1016/j.bbalip.2008.01.002.
53. Lee W, Vanderven BC, Fahey RJ, Russell DG. 2013. Intracellular Mycobacterium tuberculosis exploits host-derived fatty acids to limit metabolic stress. J. Biol. Chem. 288:6788-6800. http://dx.doi.org/10.1074/jbc.M112.445056.
54. Casabon I, Zhu SH, Otani H, Liu J, Mohn WW, Eltis LD. 2013. Regulation of the KstR2 regulon of Mycobacterium tuberculosis by a cholesterol catabolite. Mol. Microbiol. 89:1201-1212. http://dx.doi.org/10.1111/mmi.12340.
55. Kendall SL, Burgess P, Balhana R, Withers M, ten Bokum A, Lott JS, Gao C, Uhia-Castro I, Stoker NG. 2010. Cholesterol utilization in mycobacteria is controlled by two TetR-type transcriptional regulators: kstR and kstR2. Microbiology 156:1362-1371. http://dx.doi.org/10.1099/mic.0.034538-0.
56. Wang Q, Zhang Y, Yang C, Xiong H, Lin Y, Yao J, Li H, Xie L, Zhao W, Yao Y, Ning ZB, Zeng R, Xiong Y, Guan KL, Zhao S, Zhao GP. 2010. Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327:1004-1007. http://dx.doi.org/10.1126/science.1179687.
57. Zhang J, Sprung R, Pei J, Tan X, Kim S, Zhu H, Liu CF, Grishin NV, Zhao Y. 2009. Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli. Mol. Cell. Proteomics 8:215-225. http://dx.doi.org/10.1074/mcp.M800187-MCP200.