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Bacterial Metabolism of Steroids

  • Beatriz GalánEmail author
  • Julia García-Fernández
  • Carmen Felpeto-Santero
  • Lorena Fernández-Cabezón
  • José L. García
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Steroids are naturally occurring hydrophobic molecules frequently found in the biosphere. Currently, a considerable amount of steroid hormones are released into the environment as a result of human activity being now considered a new class of pollutants. This fact is generating an increasing concern about its effects in the environment, because in spite of its ubiquity in nature, most of the steroidal compounds are highly recalcitrant to microbial degradation. Bacterial transformation of steroid compounds has attracted increasing interest due to the biotechnological applications since sterol-degrading microorganisms have already been used for industrial production of steroidal drugs from low-cost natural sterols such as phytosterols. In these bacteria, a large set of catabolic genes has been identified based on gene annotation and biochemical and transcriptomic analyses. The recent knowledge on the microbial metabolism of steroids is reviewed by describing the steps involved in the catabolic pathways under both aerobic and anaerobic conditions. This background information will be helpful for metabolic engineering of steroid-transforming bacteria for biotechnological applications.

References

  1. Andor A, Jekkel A, Hopwood DA, Jeanplong F, Ilkoy E, Konya A, Kurucz I, Ambrus G (2006) Generation of useful insertionally blocked sterol degradation pathway mutants of fast-growing mycobacteria and cloning, characterization, and expression of the terminal oxygenase of the 3-ketosteroid 9α-hydroxylase in Mycobacterium smegmatis mc2155. Appl Environ Microbiol 72:6554–6559PubMedPubMedCentralCrossRefGoogle Scholar
  2. Barrientos A, Merino E, Casabon I, Rodríguez J, Crowe AM, Holert J, Philipp B, Eltis LD, Olivera ER, Luengo JM (2015) Functional analyses of three acyl-CoA synthetases involved in bile acid degradation in Pseudomonas putida DOC21. Environ Microbiol 17:47–63PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bergstrand LH, Cardenas E, Holert J, Van Hamme JD, Mohn WW (2016) Delineation of steroid-degrading microorganisms through comparative genomic analysis. MBio 7:e00166PubMedPubMedCentralGoogle Scholar
  4. 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 189:7165–7173PubMedPubMedCentralCrossRefGoogle Scholar
  5. Birkenmaier A, Möller HM, Philipp B (2011) Identification of a thiolase gene essential for β-oxidation of the acyl side chain of the steroid compound cholate in Pseudomonas sp. strain Chol1. FEMS Microbiol Lett 318:123–130PubMedCrossRefPubMedCentralGoogle Scholar
  6. Brzostek A, Sliwiński T, Rumijowska-Galewicz A, Korycka-Machała M, Dziadek J (2005) Identification and targeted disruption of the gene encoding the main 3-ketosteroid dehydrogenase in Mycobacterium smegmatis. Microbiology 151:2393–2402PubMedCrossRefPubMedCentralGoogle Scholar
  7. Brzostek A, Pawelczyk J, Rumijowska-Galewicz A, Dziadek B, Dziadek J (2009) Mycobacterium tuberculosis is able to accumulate and utilize cholesterol. J Bacteriol 191:6584–6591PubMedPubMedCentralCrossRefGoogle Scholar
  8. Brzostek A, Rumijowska-Galewicz A, Dziadek B, Wojcik EA, Dziadek J (2013) ChoD and HsdD can be dispensable for cholesterol degradation in mycobacteria. J Steroid Biochem Mol Biol 134:1–7PubMedCrossRefPubMedCentralGoogle Scholar
  9. Cabrera JE, Pruneda Paz JL, Genti-Raimondi S (2000) Steroid-inducible transcription of the 3beta/17beta-hydroxysteroid dehydrogenase gene (3beta/17beta-hsd) in Comamonas testosteroni. J Steroid Biochem Mol Biol 73:147–152PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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 284:35534–35542PubMedPubMedCentralCrossRefGoogle Scholar
  11. 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 286:40717–40724PubMedPubMedCentralCrossRefGoogle Scholar
  12. 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 89:1201–1212PubMedCrossRefPubMedCentralGoogle Scholar
  13. Casali N, Riley LW (2007) A phylogenomic analysis of the actinomycetales mce operons. BMC Genomics 8:60PubMedPubMedCentralCrossRefGoogle Scholar
  14. Caspi R, Altman T, Billington R, Dreher K, Foerster H, Fulcher CA, Keseler IM, Kothari A, Krummenacker M, Latendresse M, Mueller LA, Ong Q, Paley S, Subhraveti P, Weaver DS, Karp PD (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 42(Database issue):D459–D471PubMedCrossRefPubMedCentralGoogle Scholar
  15. Chen J, Gao X, Hong L, Ma L, Li Y (2015) Expression, purification and functional characterization of a novel 3α-hydroxysteroid dehydrogenase from Pseudomonas aeruginosa. Protein Expr Purif 115:102–108PubMedCrossRefPubMedCentralGoogle Scholar
  16. Chen YL, Wang CH, Yang FC, Ismail W, Wang PH, Shih CJ, Wu YC, Chiang YR (2016) Identification of Comamonas testosteroni as an androgen degrader in sewage. Sci Rep 6:35386PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chiang YR, Ismail W, Müller M, Fuchs G (2007) Initial steps in the anoxic metabolism of cholesterol by the denitrifying Sterolibacterium denitrificans. J Biol Chem 282:13240–13249PubMedCrossRefPubMedCentralGoogle Scholar
  18. Chiang YR, Ismail W, Heintz D, Schaeffer C, Van Dorsselaer A, Fuchs G (2008a) Study of anoxic and oxic cholesterol metabolism by Sterolibacterium denitrificans. J Bacteriol 190:905–914PubMedCrossRefPubMedCentralGoogle Scholar
  19. Chiang YR, Ismail W, Gallien S, Heintz D, Van Dorsselaer A, Fuchs G (2008b) Cholest-4-en-3-one-delta 1-dehydrogenase, a flavoprotein catalyzing the second step in anoxic cholesterol metabolism. Appl Environ Microbiol 74:107–113PubMedCrossRefPubMedCentralGoogle Scholar
  20. Chiang YR, Fang JY, Ismail W, Wang PH (2010) Initial steps in anoxic testosterone degradation by Steroidobacter denitrificans. Microbiology 156:2253–2259PubMedCrossRefPubMedCentralGoogle Scholar
  21. Crowe A, Stogios P, casabon I, Evdokimova E, Savchenco A, Eltis L (2015) Structural and functional characterization of a ketosteroid transcriptional regulator of Mycobacterium tuberculosis. J Biol Chem 290:872–82PubMedCrossRefPubMedCentralGoogle Scholar
  22. Dermer J, Fuchs G (2012) Molybdoenzyme that catalyzes the anaerobic hydroxylation of a tertiary carbon atom in the side chain of cholesterol. J Biol Chem 287:36905–36916PubMedPubMedCentralCrossRefGoogle Scholar
  23. Donova MV, Egorova OV (2012) Microbial steroid transformations: current state and prospects. Appl Microbiol Biotechnol 94:1423–1447PubMedCrossRefPubMedCentralGoogle Scholar
  24. Donova MV, Dovbnya DV, Sukhodolskaya GV, Khomutov SM, Nikolayeva VM, Kwon I, Han K (2005a) Microbial conversion of sterol-containing soybean oil production waste. J Chem Technol Biotechnol 80:55–60CrossRefGoogle Scholar
  25. Donova MV, Gulevskaya SA, Dovbnya DV, Puntus IF (2005b) Mycobacterium sp. mutant strain producing 9alpha-hydroxyandrostenedione from sitosterol. Appl Microbiol Biotechnol 67:671–678PubMedCrossRefPubMedCentralGoogle Scholar
  26. Dresen C, Lin LY, D’Angelo I, Tocheva EI, Strynadka N, Eltis LD (2010) A flavin-dependent monooxygenase from mycobacterium tuberculosis involved in cholesterol catabolism. J Biol Chem 285:22264–22275PubMedPubMedCentralCrossRefGoogle Scholar
  27. Drzyzga O, Navarro Llorens JM, Fernández de Las Heras L, García Fernández E, Perera J (2009) Gordonia cholesterolivorans sp. nov., a cholesterol-degrading actinomycete isolated from sewage sludge. Int J Syst Evol Microbiol 59:1011–1015PubMedCrossRefPubMedCentralGoogle Scholar
  28. Drzyzga O, Fernández de las Heras L, Morales V, Navarro Llorens JM, Perera J (2011) Cholesterol degradation by Gordonia cholesterolivorans. Appl Environ Microbiol 77:4802–4810PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fahrbach M (2006) Anaerobic degradation of steroid hormones by novel denitrifying bacteria. Fakultät für Mathematik, Informatik und Naturwissenschaften. Rheinisch-Westfälischen Technischen Hochschule AachenGoogle Scholar
  30. Fahrbach M, Kuever J, Meinke R, Kämpfer P, Hollender J (2006) Denitratisoma oestradiolicum gen. nov., sp. nov., a 17beta-oestradiol-degrading, denitrifying betaproteobacterium. Int J Syst Evol Microbiol 56:1547–1552PubMedCrossRefPubMedCentralGoogle Scholar
  31. Fahrbach M, Krauss M, Preiss A, Kohler HP, Hollender J (2010) Anaerobic testosterone degradation in Steroidobacter denitrificans—identification of transformation products. Environ Pollut 158:2572–2581PubMedCrossRefPubMedCentralGoogle Scholar
  32. Fernandes P, Cruz A, Angelova B, Pinheiro HM, Cabral JMS (2003) Microbial conversion of steroid compounds: recent developments. Enzyme Microb Technol 32:688–705CrossRefGoogle Scholar
  33. Fernández de Las Heras L, García Fernández E, María Navarro Llorens J, Perera J, Drzyzga O (2009) Morphological, physiological, and molecular characterization of a newly isolated steroid-degrading actinomycete, identified as Rhodococcus ruber strain Chol-4. Curr Microbiol 59:548–553PubMedCrossRefPubMedCentralGoogle Scholar
  34. Fernández de Las Heras L, Mascaraque V, García Fernández E, Navarro-Llorens JM, Perera J, Drzyzga O (2011) ChoG is the main inducible extracellular cholesterol oxidase of Rhodococcus sp. strain CECT3014. Microbiol Res 166:403–418PubMedCrossRefPubMedCentralGoogle Scholar
  35. Frank DJ, Waddling CA, La M, Ortiz de Montellano PR (2015a) Cytochrome P450 125A4, the Third Cholesterol C-26 Hydroxylase from Mycobacterium smegmatis. Biochemistry 54:6909–6916PubMedPubMedCentralCrossRefGoogle Scholar
  36. Freier TA, Beitz DC, Li L, Hartman PA (1994) Characterization of Eubacterium coprostanoligenes sp. nov., a cholesterol-reducing anaerobe. Int J Syst Bacteriol 44:137–142PubMedCrossRefPubMedCentralGoogle Scholar
  37. Fujii K, Kikuchi S, Satomi M, Ushio-Sata N, Morita N (2002) Degradation of 17beta-estradiol by a gram-negative bacterium isolated from activated sludge in a sewage treatment plant in Tokyo, Japan. Appl Environ Microbiol 68:2057–2060PubMedPubMedCentralCrossRefGoogle Scholar
  38. Fujii K, Satomi M, Morita N, Motomura T, Tanaka T, Kikuchi S (2003) Novosphingobium tardaugens sp. nov., an oestradiol-degrading bacterium isolated from activated sludge of a sewage treatment plant in Tokyo. Int J Syst Evol Microbiol 53:47–52PubMedCrossRefPubMedCentralGoogle Scholar
  39. Gagné F, Blaise C, André C (2006) Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicol Environ Saf 64:329–336PubMedCrossRefPubMedCentralGoogle Scholar
  40. Galán B, Uhía I, García-Fernández E, Martínez I, Bahíllo E, de la Fuente JL, Barredo JL, Fernández-Cabezón L, García JL (2016) Mycobacterium smegmatis is a suitable cell factory for the production of steroidic synthons. Microb Biotechnol.  https://doi.org/10.1111/1751-7915.12429CrossRefPubMedPubMedCentralGoogle Scholar
  41. Galli R, Braun C (2008) Integrative risk assessment of endocrine disruptors in Switzerland. Chimia 62:417–423CrossRefGoogle Scholar
  42. García JL, Uhía I, Galán B (2012) Catabolism and biotechnological applications of cholesterol degrading bacteria. J Microbial Biotechnol 5:679–699CrossRefGoogle Scholar
  43. Garcia-Fernandez E, Frank DJ, Galán B, Kells PM, Podust LM, Garcia JL, Ortiz de Montellano PR (2013) A highly conserved mycobacterial cholesterol catabolic pathway. Environ Microbiol 15:2342–2359PubMedPubMedCentralCrossRefGoogle Scholar
  44. García-Fernández J, Galán B, Medrano FJ, García JL (2015) Characterization of the KstR2 regulator responsible of the lower cholesterol degradative pathway in Mycobacterium smegmatis. Environ Microbiol Rep 7:155–163PubMedCrossRefPubMedCentralGoogle Scholar
  45. Göhler A, Xiong G, Paulsen S, Trentmann G, Maser E (2008) Testosterone-inducible regulator is a kinase that drives steroid sensing and metabolism in Comamonas testosteroni. J Biol Chem 283:17380–17390PubMedCrossRefPubMedCentralGoogle Scholar
  46. Gong W, Xiong G, Maser E (2012a) Cloning, expression and characterization of a novel short-chain dehydrogenase/reductase (SDRx) in Comamonas testosteroni. J Steroid Biochem Mol Biol 129:15–21PubMedCrossRefPubMedCentralGoogle Scholar
  47. Gong W, Xiong G, Maser E (2012b) Identification and characterization of the LysR-type transcriptional regulator HsdR for steroid-inducible expression of the 3α-hydroxysteroid dehydrogenase/carbonyl reductase gene in Comamonas testosteroni. Appl Environ Microbiol 78:941–950PubMedPubMedCentralCrossRefGoogle Scholar
  48. Griffin JE, Pandey AK, Gilmore SA, Mizrahi V, McKinney JD, Bertozzi CR, Sassetti CM (2012) Cholesterol catabolism by Mycobacterium tuberculosis requires transcriptional and metabolic adaptations. Chem Biol 19:218–227PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hannedouche S, Zhang J, Yi T, Shen W, Nguyen D, Pereira JP et al (2011) Oxysterols direct immune cell migration via EBI2. Nature 475:524–527PubMedPubMedCentralCrossRefGoogle Scholar
  50. Harder J, Probian C (1997) Anaerobic mineralization of cholesterol by a novel type of denitrifying bacterium. Arch Microbiol 167:269–274PubMedCrossRefPubMedCentralGoogle Scholar
  51. Hayakawa S (1982) Microbial transformation of bile acids. A unified scheme for bile acid degradation, and hydroxylation of bile acids. Z Allg Mikrobiol 22:309–326PubMedCrossRefPubMedCentralGoogle Scholar
  52. Ho N, Dawes S, Crowe A, casabon I, Gao C, Kendall S, Baker E, Eltis L, Lott J (2016) The structure of the transcriptional repressor KstR in complex with CoA thioester cholesterol metabolites sheds light on the regulation of cholesterol catabolism in Mycobacterium tuberculosis. J Biol Chem 291:7256–66PubMedCrossRefPubMedCentralGoogle Scholar
  53. Holert J, Alam I, Larsen M, Antunes A, Bajic VB, Stingl U, Philipp B (2013a) Genome sequence of Pseudomonas sp. strain Chol1, a model organism for the degradation of bile salts and other steroid compounds. Genome Announc 1(1). pii: e00014–12Google Scholar
  54. Holert J, Jagmann N, Philipp B (2013b) 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 195:3371–3380PubMedPubMedCentralCrossRefGoogle Scholar
  55. Holert J, Kulić Ž, Yücel O, Suvekbala V, Suter MJ, Möller HM, Philipp B (2013c) Degradation of the acyl side chain of the steroid compound cholate in Pseudomonas sp. strain Chol1 proceeds via an aldehyde intermediate. J Bacteriol 195:585–595PubMedPubMedCentralCrossRefGoogle Scholar
  56. Holert J, Yücel O, Suvekbala V, Kulić Z, Möller H, Philipp B (2014) Evidence of distinct pathways for bacterial degradation of the steroid compound cholate suggests the potential for metabolic interactions by interspecies cross-feeding. Environ Microbiol 16:1424–1440PubMedCrossRefPubMedCentralGoogle Scholar
  57. Holert J, Yücel O, Jagmann N, Prestel A, Möller HM, Philipp B (2016) Identification of bypass reactions leading to the formation of one central steroid degradation intermediate in metabolism of different bile salts in Pseudomonas sp. strain Chol1. Environ Microbiol 18:3373–3389PubMedCrossRefPubMedCentralGoogle Scholar
  58. Horinouchi S, Ishizuka H, Beppu T (1991) Cloning, nucleotide sequence, and transcriptional analysis of the NAD(P)-dependent cholesterol dehydrogenase gene from a Nocardia sp. and its hyperexpression in Streptomyces spp. Appl Environ Microbiol 57:1386–1393PubMedPubMedCentralGoogle Scholar
  59. Horinouchi M, Yamamoto T, Taguchi K, Arai H, Kudo T (2001) Meta-cleavage enzyme gene tesB is necessary for testosterone degradation in Comamonas testosteroni TA441. Microbiology 147:3367–3375PubMedCrossRefPubMedCentralGoogle Scholar
  60. Horinouchi M, Hayashi T, Koshino H, Yamamoto T, Kudo T (2003a) Gene encoding the hydrolase for the product of the meta-cleavage reaction in testosterone degradation by Comamonas testosteroni. Appl Environ Microbiol 69:2139–2152PubMedPubMedCentralCrossRefGoogle Scholar
  61. Horinouchi M, Hayashi T, Yamamoto T, Kudo T (2003b) A new bacterial steroid degradation gene cluster in Comamonas testosteroni TA441 which consists of aromatic-compound degradation genes for seco-steroids and 3-ketosteroid dehydrogenase genes. Appl Environ Microbiol 69:4421–4430PubMedPubMedCentralCrossRefGoogle Scholar
  62. Horinouchi M, Hayashi T, Kudo T (2004a) The genes encoding the hydroxylase of 3-hydroxy-9,10-secoandrosta-1,3,5(10)-triene-9,17-dione in steroid degradation in Comamonas testosteroni TA441. J Steroid Biochem Mol Biol 92:143–154PubMedCrossRefPubMedCentralGoogle Scholar
  63. Horinouchi M, Kurita T, Yamamoto T, Hatori E, Hayashi T, Kudo T (2004b) Steroid degradation gene cluster of Comamonas testosteroni consisting of 18 putative genes from meta-cleavage enzyme gene tesB to regulator gene tesR. Biochem Biophys Res Commun 324:597–604PubMedCrossRefPubMedCentralGoogle Scholar
  64. Horinouchi M, Hayashi T, Koshino H, Kurita T, Kudo T (2005) Identification of 9,17-dioxo-1,2,3,4,10,19-hexanorandrostan-5-oic acid, 4-hydroxy-2-oxohexanoic acid, and 2-hydroxyhexa-2,4-dienoic acid and related enzymes involved in testosterone degradation in Comamonas testosteroni TA441. Appl Environ Microbiol 71:5275–5281PubMedPubMedCentralCrossRefGoogle Scholar
  65. 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 101:78–84PubMedCrossRefPubMedCentralGoogle Scholar
  66. Horinouchi M, Hayashi T, Koshino H, Malon M, Yamamoto T, Kudo T (2008) Identification of genes involved in inversion of stereochemistry of a C-12 hydroxyl group in the catabolism of cholic acid by Comamonas testosteroni TA441. J Bacteriol 190:5545–5554PubMedPubMedCentralCrossRefGoogle Scholar
  67. Horinouchi M, Kurita T, Hayashi T, Kudo T (2010) Steroid degradation genes in Comamonas testosteroni TA441: isolation of genes encoding a Δ4(5)-isomerase and 3α- and 3β-dehydrogenases and evidence for a 100 kb steroid degradation gene hot spot. J Steroid Biochem Mol Biol 122:253–263PubMedCrossRefPubMedCentralGoogle Scholar
  68. Horinouchi M, Hayashi T, Kudo T (2012) Steroid degradation in Comamonas testosteroni. J Steroid Biochem Mol Biol 129:4–14PubMedCrossRefPubMedCentralGoogle Scholar
  69. Hu A, He J, Chu KH, Yu CP (2011) Genome sequence of the 17β-estradiol-utilizing bacterium Sphingomonas strain KC8. J Bacteriol 193:4266–4267PubMedPubMedCentralCrossRefGoogle Scholar
  70. Isabelle M, Villemur R, Juteau P, Lépine F (2011) Isolation of estrogen-degrading bacteria from an activated sludge bioreactor treating swine waste, including a strain that converts estrone to β-estradiol. Can J Microbiol 57:559–568PubMedCrossRefPubMedCentralGoogle Scholar
  71. Ishizaki T, Hirayama N, Shinkawa H, Nimi O, Murooka Y (1989) Nucleotide sequence of the gene for cholesterol oxidase from a Streptomyces sp. J Bacteriol 171:596–601PubMedPubMedCentralCrossRefGoogle Scholar
  72. Ismail W, Chiang YR (2011) Oxic and anoxic metabolism of steroids by bacteria. Bioremed Biodegrad S1:001Google Scholar
  73. Ji W, Chen Y, Zhang H, Zhang X, Li Z, Yu Y (2014) Cloning, expression and characterization of a putative 7alpha-hydroxysteroid dehydrogenase in Comamonas testosteroni. Microbiol Res 169:148–154PubMedCrossRefPubMedCentralGoogle Scholar
  74. Jiang L, Yang J, Chen J (2010) Isolation and characteristics of 17beta-estradiol-degrading Bacillus spp. strains from activated sludge. Biodegradation 21:729–736PubMedCrossRefPubMedCentralGoogle Scholar
  75. Joshi SM, Pandey AK, Capite N, Fortune SM, Rubin EJ, Sassetti CM (2006) Characterization of mycobacterial virulence genes through genetic interaction mapping. Proc Natl Acad Sci 103:11760–11765PubMedCrossRefPubMedCentralGoogle Scholar
  76. Ke J, Zhuang W, Gin KY, Reinhard M, Hoon LT, Tay JH (2007) Characterization of estrogen-degrading bacteria isolated from an artificial sandy aquifer with ultrafiltered secondary effluent as the medium. Appl Microbiol Biotechnol 75:1163–1171PubMedCrossRefPubMedCentralGoogle Scholar
  77. Kendall SL, Withers M, Soffair CN, Moreland NJ, Gurcha S, Sidders B, Frita R, Ten Bokum A, Besra GS, Lott JS, Stoker NG (2007) A highly conserved transcriptional repressor controls a large regulon involved in lipid degradation in Mycobacterium smegmatis and Mycobacterium tuberculosis. Mol Microbiol 65:684–699PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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 156:1362–1371PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kieslich K (1985) Microbial side-chain degradation of sterols. J Basic Microbiol 7:461–474CrossRefGoogle Scholar
  80. Klepp LI, Forrellad MA, Osella AV, Blanco FC, Stella EJ, Bianco MV, Santangelo ML, Kurisu F, Ogura M, Saitoh S, Yamazoe A, Yagi O (2010) Degradation of natural estrogen and identification of the metabolites produced by soil isolates of Rhodococcus sp. and Sphingomonas sp. J Biosci Bioeng 109:576–582CrossRefGoogle Scholar
  81. Klepp LI, Forrellad MA, Osella AV, Blanco FC, Stella EJ, Bianco MV, Santangelo Mde L, Sassetti C, Jackson M, Cataldi AA, Bigi F, Morbidoni HR (2012) Impact of the deletion of the six mce operons in Mycobacterium smegmatis. Microbes Infect 14:590–599PubMedPubMedCentralCrossRefGoogle Scholar
  82. Kurisu F, Zang K, Kasuga I, Furumai H, Yagi O (2015) Identification of estrone-degrading Betaproteobacteria in activated sludge by microautoradiography fluorescent in situ hybridization. Lett Appl Microbiol 61:28–35PubMedCrossRefPubMedCentralGoogle Scholar
  83. Lack N, Lowe ED, Liu J, Eltis LD, Noble ME, Sim E, Westwood IM (2008) Structure of HsaD, a steroid-degrading hydrolase, from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 64:2–7PubMedCrossRefPubMedCentralGoogle Scholar
  84. Lack NA, Yam KC, Lowe ED, Horsman GP, Owen RL, Sim E, Eltis LD (2010) Characterization of a carbon-carbon hydrolase from Mycobacterium tuberculosis involved in cholesterol metabolism. J Biol Chem 285:434–443PubMedCrossRefPubMedCentralGoogle Scholar
  85. Leu YL, Wang PH, Shiao MS, Ismail W, Chiang YR (2011) A novel testosterone catabolic pathway in bacteria. J Bacteriol 193:4447–4455PubMedPubMedCentralCrossRefGoogle Scholar
  86. Li J, Vrielink A, Brick P, Blow DM (1993) Crystal structure of cholesterol oxidase complexed with a steroid substrate: implications for flavin adenine dinucleotide dependent alcohol oxidases. Biochemistry 32:11507–11515PubMedCrossRefPubMedCentralGoogle Scholar
  87. Li L, Freier TA, Hartman PA, Young JW, Beitz DC (1995) A resting-cell assay for cholesterol reductase activity in Eubacterium coprostanoligenes ATCC 51222. Appl Microbiol Biotechnol 43:887–892CrossRefGoogle Scholar
  88. Li Z, Nandakumar R, Madayiputhiya N, Li X (2012) Proteomic analysis of 17β-estradiol degradation by Stenotrophomonas maltophilia. Environ Sci Technol 46:5947–5955PubMedCrossRefPubMedCentralGoogle Scholar
  89. Li M, Xiong G, Maser E (2013) A novel transcriptional repressor PhaR for the steroid-inducible expression of the 3,17β-hydroxysteroid dehydrogenase gene in Comamonas testosteroni ATCC11996. Chem Biol Interact 202:116–125PubMedCrossRefPubMedCentralGoogle Scholar
  90. Liang R, Liu H, Tao F, Liu Y, Ma C, Liu X, Liu J (2012) Genome sequence of Pseudomonas putida strain SJTE-1, a bacterium capable of degrading estrogens and persistent organic pollutants. J Bacteriol 194:4781–4782PubMedPubMedCentralCrossRefGoogle Scholar
  91. Lin CW, Wang PH, Ismail W, Tsai YW, El Nayal A, Yang CY, Yang FC, Wang CH, Chiang YR (2015) Substrate uptake and subcellular compartmentation of anoxic cholesterol catabolism in Sterolibacterium denitrificans. J Biol Chem 290:1155–1169PubMedCrossRefPubMedCentralGoogle Scholar
  92. Linares M, Pruneda-Paz JL, Reyna L, Genti-Raimondi S (2008) Regulation of testosterone degradation in Comamonas testosteroni. J Steroid Biochem Mol Biol 112:145–150PubMedCrossRefPubMedCentralGoogle Scholar
  93. Liu C, Yang XV, Wu J, Kuei C, Mani NS, Zhang L, Yu J, Sutton SW, Qin N, Banie H, Karlsson L, Sun S, Lovenberg TW (2011) Oxysterols direct B-cell migration through EBI2. Nature 475:519–523PubMedCrossRefPubMedCentralGoogle Scholar
  94. Ma C, Qin D, Sun Q, Zhang F, Liu H, Yu CP (2016) Removal of environmental estrogens by bacterial cell immobilization technique. Chemosphere 144:607–614PubMedCrossRefPubMedCentralGoogle Scholar
  95. Machang’u RS, Prescott JF (1991) Purification and properties of cholesterol oxidase and choline phosphohydrolase from Rhodococcus equi. Can J Vet Res 55:332–340PubMedPubMedCentralGoogle Scholar
  96. Mallonee DH, Hylemon PB (1996) Sequencing and expression of a gene encoding a bile acid transporter from Eubacterium sp. strain VPI 12708. J Bacteriol 178:7053–7058PubMedPubMedCentralCrossRefGoogle Scholar
  97. Marsheck WJ, Kraychy S, Muir RD (1972) Microbial degradation of sterols. Appl Microbiol 23:72–77PubMedPubMedCentralGoogle Scholar
  98. Maser E, Xiong G, Grimm C, Ficner R, Reuter K (2001) 3alpha-Hydroxysteroid dehydrogenase/carbonyl reductase from Comamonas testosteroni: biological significance, three-dimensional structure and gene regulation. Chem Biol Interact 130-132:707–722PubMedCrossRefPubMedCentralGoogle Scholar
  99. McLean KJ, Lafite P, Levy C, Cheesman MR, Mast N, Pikuleva IA, Leys D, Munro AW (2009) The structure of Mycobacterium tuberculosis CYP125: molecular basis for cholesterol binding in a P450 needed for host infection. J Biol Chem 284:35524–35533PubMedPubMedCentralCrossRefGoogle Scholar
  100. Merino E, Barrientos A, Rodríguez J, Naharro G, Luengo JM, Olivera ER (2013) Isolation of cholesterol- and deoxycholate-degrading bacteria from soil samples: evidence of a common pathway. Appl Microbiol Biotechnol 97:891–904PubMedCrossRefPubMedCentralGoogle Scholar
  101. Möbus E, Maser E (1998) Molecular cloning, overexpression, and characterization of steroid-inducible 3alpha-hydroxysteroid dehydrogenase/carbonyl reductase from Comamonas testosteroni. A novel member of the short-chain dehydrogenase/reductase superfamily. J Biol Chem 273:30888–30896PubMedCrossRefPubMedCentralGoogle Scholar
  102. Möbus E, Jahn M, Schmid R, Jahn D, Maser E (1997) Testosterone-regulated expression of enzymes involved in steroid and aromatic hydrocarbon catabolism in Comamonas testosteroni. J Bacteriol 179:5951–5955PubMedPubMedCentralCrossRefGoogle Scholar
  103. Mohn WW, van der Geize R, Stewart GR, Okamoto S, Liu J, Dijkhuizen L, Eltis LD (2008) The actinobacterial mce4 locus encodes a steroid transporter. J Biol Chem 283:35368–35374PubMedPubMedCentralCrossRefGoogle Scholar
  104. 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 194:6712–6719PubMedPubMedCentralCrossRefGoogle Scholar
  105. Muller M, Patureau D, Godon JJ, Delgenès JP, Hernandez-Raquet G (2010) Molecular and kinetic characterization of mixed cultures degrading natural and synthetic estrogens. Appl Microbiol Biotechnol 85:691–701PubMedCrossRefPubMedCentralGoogle Scholar
  106. Navas J, González-Zorn B, Ladrón N, Garrido P, Vázquez-Boland JA (2001) Identification and mutagenesis by allelic exchange of choE, encoding a cholesterol oxidase from the intracellular pathogen Rhodococcus equi. J Bacteriol 183:4796–4805PubMedPubMedCentralCrossRefGoogle Scholar
  107. 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 78:275–282PubMedCrossRefPubMedCentralGoogle Scholar
  108. Oppermann UC, Maser E (1996) Characterization of a 3 alpha-hydroxysteroid dehydrogenase/carbonyl reductase from the gram-negative bacterium Comamonas testosteroni. Eur J Biochem 241:744–749PubMedCrossRefPubMedCentralGoogle Scholar
  109. Ouellet H, Johnston JB, Chow E, Kells PM, Burlingame AL, Cox JS, Podust ML, Ortiz de Montellano PR (2010) Mycobacterium tuberculosis CYP125A1, a steroid C27 monooxygenase that detoxifies intracellularly generated cholest-4-en-3-one. Mol Microbiol 77(3):730–742PubMedPubMedCentralCrossRefGoogle Scholar
  110. Pan T, Huang P, Xiong G, Maser E (2015) Isolation and identification of a repressor TetR for 3,17β-HSD expressional regulation in Comamonas testosteroni. Chem Biol Interact 234:205–212PubMedCrossRefPubMedCentralGoogle Scholar
  111. Pandey AK, Sassetti CM (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105:4376–4380PubMedCrossRefPubMedCentralGoogle Scholar
  112. Pauwels B, Wille K, Noppe H, De Brabander H, Van de Wiele T, Verstraete W, Boon N (2008) 17alpha-ethinylestradiol cometabolism by bacteria degrading estrone, 17beta-estradiol and estriol. Biodegradation 19:683–693PubMedCrossRefPubMedCentralGoogle Scholar
  113. Penfield JS, Worrall LJ, Strynadka NC, Eltis LD (2014) Substrate specificities and conformational flexibility of 3-ketosteroid 9α-hydroxylases. J Biol Chem 289:25523–25536PubMedPubMedCentralCrossRefGoogle Scholar
  114. Philipp B (2011) Bacterial degradation of bile salts. Appl Microbiol Biotechnol 89:903–915PubMedCrossRefPubMedCentralGoogle Scholar
  115. Philipp B, Erdbrink H, Suter MJ, Schink B (2006) Degradation of and sensitivity to cholate in Pseudomonas sp. strain Chol1. Arch Microbiol 185:192–201PubMedCrossRefPubMedCentralGoogle Scholar
  116. Plésiat P, Nikaido H (1992) Outer membranes of gram-negative bacteria are permeable to steroid probes. Mol Microbiol 6:1323–1333PubMedCrossRefPubMedCentralGoogle Scholar
  117. Pruneda-Paz JL, Linares M, Cabrera JE, Genti-Raimondi S (2004a) Identification of a novel steroid inducible gene associated with the beta hsd locus of Comamonas testosteroni. J Steroid Biochem Mol Biol 88:91–100PubMedCrossRefPubMedCentralGoogle Scholar
  118. Pruneda-Paz JL, Linares M, Cabrera JE, Genti-Raimondi S (2004b) TeiR, a LuxR-type transcription factor required for testosterone degradation in Comamonas testosteroni. J Bacteriol 186:1430–1437PubMedPubMedCentralCrossRefGoogle Scholar
  119. Ribeiro AR, Carvalho MF, Afonso CM, Tiritan ME, Castro PM (2010) Microbial degradation of 17beta -estradiol and 17alpha-ethinylestradiol followed by a validated HPLC-DAD method. J Environ Sci Health B 45:265–273PubMedCrossRefPubMedCentralGoogle Scholar
  120. Ridlon JM, Kang OJ, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47:241–259PubMedCrossRefPubMedCentralGoogle Scholar
  121. Roh H, Chu KH (2010) A 17beta-estradiol-utilizing bacterium, Sphingomonas strain KC8: part I characterization and abundance in wastewater treatment plants. Environ Sci Technol 44:4943–4950PubMedCrossRefPubMedCentralGoogle Scholar
  122. Rösch V, Denger K, Schleheck D, Smits TH, Cook AM (2008) Different bacterial strategies to degrade taurocholate. Arch Microbiol 190:11–18PubMedCrossRefPubMedCentralGoogle Scholar
  123. Rosloniec KZ, Wilbrink M, Capyk JK, Mohn WW, Ostendorf M, van der Geize R, Dijkhuizen L, Eltis LD (2009) Cytochrome P450 125 (CYP125) catalyzes C26-hydroxylation to initiate sterol side chain degradation in Rhodococcus jostii RHA1. Mol Microbiol 74:1031–1043PubMedPubMedCentralCrossRefGoogle Scholar
  124. Sassetti C, Jackson M, Cataldi AA, Bigi F, Morbidoni HR (2012) Impact of the deletion of the six mce operons in Mycobacterium smegmatis. Microbes Infect 14:590–599PubMedPubMedCentralCrossRefGoogle Scholar
  125. Schaefer C, Lu R, Nesbitt NM, Schiebel J, Sampson NS, Kisker C (2015) FadA5 a thiolase from Mycobacterium tuberculosis – a unique steroid-binding pocket reveals the potential for drug development against tuberculosis. Structure 23:21–33PubMedCrossRefPubMedCentralGoogle Scholar
  126. Shi JH, Suzuki Y, Nakai S, Hosomi M (2004) Microbial degradation of estrogens using activated sludge and night soil-composting microorganisms. Water Sci Technol 50:153–159PubMedCrossRefPubMedCentralGoogle Scholar
  127. Shi W, Wang L, Rousseau DP, Lens PN (2010) Removal of estrone, 17alpha-ethinylestradiol, and 17beta-estradiol in algae and duckweed-based wastewater treatment systems. Environ Sci Pollut Res Int 17:824–833PubMedCrossRefPubMedCentralGoogle Scholar
  128. Skowasch D, Möbus E, Maser E (2002) Identification of a novel Comamonas testosteroni gene encoding a steroid-inducible extradiol dioxygenase. Biochem Biophys Res Commun 294:560–566PubMedCrossRefPubMedCentralGoogle Scholar
  129. Somalinga V, Mohn WW (2013) Rhodococcus jostii porin A (RjpA) functions in cholate uptake. Appl Environ Microbiol 79:6191–6193PubMedPubMedCentralCrossRefGoogle Scholar
  130. Song H, Sandie R, Wang Y, Andrade-Navarro MA, Niederweis M (2008) Identification of outer membrane proteins of Mycobacterium tuberculosis. Tuberculosis 88:526–544PubMedCrossRefPubMedCentralGoogle Scholar
  131. Swain K, Casabon I, Eltis LD, Mohn WW (2012) Two transporters essential for reassimilation of novel cholate metabolites by Rhodococcus jostii RHA1. J Bacteriol 194:6720–6727PubMedPubMedCentralCrossRefGoogle Scholar
  132. Tarlera S, Denner EB (2003) Sterolibacterium denitrificans gen. nov., sp. nov., a novel cholesterol-oxidizing, denitrifying member of the beta-Proteobacteria. Int J Syst Evol Microbiol 53:1085–1091PubMedCrossRefPubMedCentralGoogle Scholar
  133. Thomas ST, Sampson NS (2013) Mycobacterium tuberculosis utilizes a unique heterotetrameric structure for dehydrogenation of the cholesterol side chain. Biochemistry 52:2895–2904PubMedPubMedCentralCrossRefGoogle Scholar
  134. Thomas ST, Vander Ven BC, Sherman DR, Russell DG, Sampson NS (2011) Pathway profiling in Mycobacterium tuberculosis: elucidation of cholesterol-derived catabolite and enzymes that catalyze its metabolism. J Biol Chem 286:43668–43678PubMedPubMedCentralCrossRefGoogle Scholar
  135. Uhia I, Galán B, Medrano FJ, García JL (2011a) Characterization of the KstR-dependent promoter of the gene for the first step of the cholesterol degradative pathway in Mycobacterium smegmatis. Microbiology 157:2670–2680PubMedCrossRefPubMedCentralGoogle Scholar
  136. Uhia I, Galán B, Morales V, García JL (2011b) Initial step in the catabolism of cholesterol by Mycobacterium smegmatis mc2155. Environ Microbiol 13:943–959PubMedCrossRefPubMedCentralGoogle Scholar
  137. Uhia I, Galán B, Kendall SL, Stoker NG, García JL (2012) Cholesterol metabolism in Mycobacterium smegmatis. Environ Microbiol Rep 4:168–182PubMedCrossRefPubMedCentralGoogle Scholar
  138. Van der Geize R, Hessels GI, van Gerwen R, Vrijbloed JW, van Der Meijden P, Dijkhuizen L (2000) Targeted disruption of the kstD gene encoding a 3-kestosteroid delta(1)-dehydrogenase isoenzyme of Rhodococcus erythropolis strain SQ1. Appl Environ Microbiol 66:2029–2036PubMedPubMedCentralCrossRefGoogle Scholar
  139. Van der Geize R, Hessels GI, van Gerwen R, van der Meijden P, Dijkhuizen L (2001) Unmarked gene deletion mutagenesis of kstD, encoding 3-ketosteroid Delta1-dehydrogenase, in Rhodococcus erythropolis SQ1 using sacB as counter-selectable marker. FEMS Microbiol Lett 205:197–202PubMedCrossRefPubMedCentralGoogle Scholar
  140. Van der Geize R, Hessels GI, Dijkhuizen L (2002a) Molecular and functional characterization of the kstD2 gene of Rhodococcus erythropolis SQ1 encoding a second 3-ketosteroid Δ1-dehydrogenase isoenzyme. Microbiology 148:3285–3292PubMedCrossRefPubMedCentralGoogle Scholar
  141. Van der Geize R, Hessels GI, Gerwen RV, Meijden PVD, Dijkhuizen L (2002b) Molecular and functional characterization of kshA and kshB, encoding two components of 3-ketosteroid 9α-hydroxylase, a class IA monooxygenase, in Rhodococcus erythropolis strain SQ1. Mol Microbiol 45:1007–1018PubMedCrossRefPubMedCentralGoogle Scholar
  142. 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 USA 104:1947–1952PubMedCrossRefPubMedCentralGoogle Scholar
  143. Van der Geize R, Hessels GI, Nienhuis-Kuiper M, Dijkhuizen L (2008) Characterization of a second Rhodococcus erythropolis SQ1 3-ketosteroid 9alpha-hydroxylase activity comprising a terminal oxygenase homologue, KshA2, active with oxygenase-reductase component KshB. Appl Environ Microbiol 74:7197–7203PubMedPubMedCentralCrossRefGoogle Scholar
  144. Van der Geize R, Grommen AW, Hessels GI, Jacobs AA, Dijkhuizen L (2011) The steroid catabolic pathway of the intracellular pathogen Rhodococcus equi is important for pathogenesis and a target for vaccine development. PLoS Pathog 7:e1002181PubMedPubMedCentralCrossRefGoogle Scholar
  145. Villemur R, Dos Santos SC, Ouellette J, Juteau P, Lépine F, Déziel E (2013) Biodegradation of endocrine disruptors in solid-liquid two-phase partitioning systems by enrichment cultures. Appl Environ Microbiol 79:4701–4711PubMedPubMedCentralCrossRefGoogle Scholar
  146. Wang PH, Lee TH, Ismail W, Tsai CY, Lin CW, Tsai YW, Chiang YR (2013) An oxygenase-independent cholesterol catabolic pathway operates under oxic conditions. PLoS One 8:e66675PubMedPubMedCentralCrossRefGoogle Scholar
  147. Wang PH, Yu CP, Lee TH, Lin CW, Ismail W, Wey SP, Kuo AT, Chiang YR (2014) Anoxic androgen degradation by the denitrifying bacterium Sterolibacterium denitrificans via the 2,3-seco pathway. Appl Environ Microbiol 80:3442–3452PubMedPubMedCentralCrossRefGoogle Scholar
  148. Weber S, Leuschner P, Kämpfer P, Dott W, Hollender J (2005) Degradation of estradiol and ethinyl estradiol by activated sludge and by a defined mixed culture. Appl Microbiol Biotechnol 67:106–112PubMedCrossRefPubMedCentralGoogle Scholar
  149. 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 77:4455–4464PubMedPubMedCentralCrossRefGoogle Scholar
  150. Wipperman MF, Yang M, Thomas ST, Sampson NS (2013) Shrinking the FadE proteome of Mycobacterium tuberculosis: insights into cholesterol metabolism through identification of an α2β2 heterotetrameric acyl coenzyme A dehydrogenase family. J Bacteriol 195:4331–4341PubMedPubMedCentralCrossRefGoogle Scholar
  151. Wu Y, Huang P, Xiong G, Maser E (2015) Identification and isolation of a regulator protein for 3,17β-HSD expressional regulation in Comamonas testosteroni. Chem Biol Interact 234:197–204PubMedCrossRefPubMedCentralGoogle Scholar
  152. Wülfing C, Plückthun A (1994) Correctly folded T-cell receptor fragments in the periplasm of Escherichia coli. Influence of folding catalysts. J Mol Biol 242:655–669PubMedCrossRefPubMedCentralGoogle Scholar
  153. Xiong G, Maser E (2001) Regulation of the steroid-inducible 3alpha-hydroxysteroid dehydrogenase/carbonyl reductase gene in Comamonas testosteroni. J Biol Chem 276:9961–9970PubMedCrossRefPubMedCentralGoogle Scholar
  154. Xiong G, Martin H, Blum A, Schäfers C, Maser E (2001) A model on the regulation of 3alpha-hydroxysteroid dehydrogenase/carbonyl reductase expression in Comamonas testosteroni. Chem Biol Interact 130–132:723–736PubMedCrossRefPubMedCentralGoogle Scholar
  155. Xiong G, Martin HJ, Maser E (2003a) Characterization and recombinant expression of the translational repressor RepB of 3alpha-hydroxysteroid dehydrogenase/carbonyl reductase in Comamonas testosteroni. Chem Biol Interact 143–144:425–433PubMedCrossRefPubMedCentralGoogle Scholar
  156. Xiong G, Martin HJ, Maser E (2003b) Identification and characterization of a novel translational repressor of the steroid-inducible 3 alpha-hydroxysteroid dehydrogenase/carbonyl reductase gene in Comamonas testosteroni. J Biol Chem 278:47400–47407PubMedCrossRefPubMedCentralGoogle Scholar
  157. Xu LQ, Liu YJ, Yao K, Liu HH, Tao XY, Wang FQ, Wei DZ (2016) Unraveling and engineering the production of 23,24-bisnorcholenic steroids in sterol metabolism. Sci Rep 6:21928PubMedPubMedCentralCrossRefGoogle Scholar
  158. 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:e1000344PubMedPubMedCentralCrossRefGoogle Scholar
  159. Yang X, Dubnau E, Smith I, Sampson NS (2007) Rv1106c from Mycobacterium tuberculosis is a 3β-hydroxysteroid dehydrogenase. Biochemistry 46:9058–9067PubMedPubMedCentralCrossRefGoogle Scholar
  160. Yang M, Guja KE, Thomas ST, Garcia-Diaz M, Sampson NS (2014) A distinct MaoC-like enoyl-CoA hydratase architecture mediates cholesterol catabolism in Mycobacterium tuberculosis. ACS Chem Biol 9:2632–2645PubMedPubMedCentralCrossRefGoogle Scholar
  161. Yang M, Lu R, Guja KE, Wipperman MF, St Clair JR, Bonds AC, Garcia-Diaz M, Sampson NS (2015) Unraveling cholesterol catabolism in Mycobacterium tuberculosis: ChsE4-ChsE5 α2β2 Acyl-CoA dehydrogenase initiates β-oxidation of 3-oxo-cholest-4-en-26-oyl CoA (2015). ACS Infect Dis 1:100–125Google Scholar
  162. Yeh CH, Kuo YS, Chang CM, Liu WH, Sheu ML, Meng M (2014) Deletion of the gene encoding the reductase component of 3-ketosteroid 9α-hydroxylase in Rhodococcus equi USA-18 disrupts sterol catabolism, leading to the accumulation of 3-oxo-23,24-bisnorchola-1,4-dien-22-oic acid and 1,4-androstadiene-3,17-dione. Microb Cell Fact 13:130PubMedPubMedCentralGoogle Scholar
  163. Yoshimoto T, Nagai F, Fujimoto J, Watanabe K, Mizukoshi H, Makino T, Kimura K, Saino H, Sawada H, Omura H (2004) Degradation of estrogens by Rhodococcus zopfii and Rhodococcus equi isolates from activated sludge in wastewater treatment plants. Appl Environ Microbiol 70:5283–5289PubMedPubMedCentralCrossRefGoogle Scholar
  164. Yu CP, Roh H, Chu KH (2007) 17beta-estradiol-degrading bacteria isolated from activated sludge. Environ Sci Technol 41:486–492PubMedCrossRefPubMedCentralGoogle Scholar
  165. Yu Y, Liu C, Wang B, Li Y, Zhang H (2015) Characterization of 3,17β-hydroxysteroid dehydrogenase in Comamonas testosteroni. Chem Biol Interact 234:221–228PubMedCrossRefPubMedCentralGoogle Scholar
  166. Yücel O, Drees S, Jagmann N, Patschkowski T, Philipp B (2016) An unexplored pathway for degradation of cholate requires a 7α-hydroxysteroid dehydratase and contributes to a broad metabolic repertoire for the utilization of bile salts in Novosphingobium sp. strain Chol11. Environ Microbiol.  https://doi.org/10.1111/1462-2920.13534CrossRefPubMedPubMedCentralGoogle Scholar
  167. Zang K, Kurisu F, Kasuga I, Furumai H, Yagi O (2008) Analysis of the phylogenetic diversity of estrone-degrading bacteria in activated sewage sludge using microautoradiography-fluorescence in situ hybridization. Syst Appl Microbiol 31:206–214PubMedCrossRefPubMedCentralGoogle Scholar
  168. Zhang T, Xiong G, Maser E (2011) Characterization of the steroid degrading bacterium S19-1 from the Baltic Sea at Kiel, Germany. Chem Biol Interact 191:83–88PubMedCrossRefPubMedCentralGoogle Scholar
  169. Zhang T, Xiong G, Maser E (2013) Analysis and characterization of eight estradiol inducible genes and a strong promoter from the steroid degrading marine bacterial strain S19-1. Chem Biol Interact 202:159–167PubMedCrossRefPubMedCentralGoogle Scholar
  170. Zhang H, Ji Y, Wang Y, Zhang X, Yu Y (2015) Cloning and characterization of a novel β-ketoacyl-ACP reductase from Comamonas testosteroni. Chem Biol Interact 234:213–220PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Beatriz Galán
    • 1
    Email author
  • Julia García-Fernández
    • 1
  • Carmen Felpeto-Santero
    • 1
  • Lorena Fernández-Cabezón
    • 1
  • José L. García
    • 1
  1. 1.Department of Environmental BiologyCentro de Investigaciones Biológicas, Consejo Superior de Investigaciones CientíficasMadridSpain

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