Anoxic Androgen Degradation by the Denitrifying Bacterium Sterolibacterium denitrificans via the 2,3-seco Pathway

Wang, Po Hsiang; Yu, Changping; Lee, Tzong‐Huei; Lin, Ching Wen; Ismail, Wael; Wey, Shiaw-Pyng; Kuo, An Ti; Chiang, Yin-Ru

doi:10.1128/aem.03880-13

Cited by 41 publications

(42 citation statements)

References 63 publications

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“… Genes involved in ring AB degradation – The degradation of ring A in the oxygen‐independent 2,3‐ seco pathway involves the Mo‐enzyme AtcABC converting androst‐1‐en‐3,17‐dione to a 1,3‐di‐keton (Wang et al ., ; Yang et al ., ). Highly homologous genes are present in the acd 3 gene cluster (SDENv1_10172‐4; Fig.…”

Section: Resultsmentioning

confidence: 99%

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A patchwork pathway for oxygenase‐independent degradation of side chain containing steroids

Warnke

Jacoby

Jung

et al. 2017

Environmental Microbiology

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The denitrifying betaproteobacterium Sterolibacterium denitrificans serves as model organism for studying the oxygen-independent degradation of cholesterol. Here, we demonstrate its capability of degrading various globally abundant side chain containing zoo-, phyto- and mycosterols. We provide the complete genome that empowered an integrated genomics/proteomics/metabolomics approach, accompanied by the characterization of a characteristic enzyme of steroid side chain degradation. The results indicate that individual molybdopterin-containing steroid dehydrogenases are involved in C25-hydroxylations of steroids with different isoprenoid side chains, followed by the unusual conversion to C26-oic acids. Side chain degradation to androsta-1,4-diene-3,17-dione (ADD) via aldolytic C-C bond cleavages involves acyl-CoA synthetases/dehydrogenases specific for the respective 26-, 24- and 22-oic acids/-oyl-CoAs and promiscuous MaoC-like enoyl-CoA hydratases, aldolases and aldehyde dehydrogenases. Degradation of rings A and B depends on gene products uniquely found in anaerobic steroid degraders, which after hydrolytic cleavage of ring A, again involves CoA-ester intermediates. The degradation of the remaining CD rings via hydrolytic cleavage appears to be highly similar in aerobic and anaerobic bacteria. Anaerobic cholesterol degradation employs a composite repertoire of more than 40 genes partially known from aerobic degradation in gammaproteobacteria/actinobacteria, supplemented by unique genes that are required to circumvent oxygenase-dependent reactions.

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Section: Resultsmentioning

confidence: 99%

“…denitrificans (Yang et al ., ). The A ring is then hydrolytically cleaved to 1,17‐dioxo‐2,3‐ seco ‐androstan‐3‐oic acid (DSAO), the name‐giving key intermediate of this 2,3‐ seco ‐pathway (Wang et al ., ). The genes and enzymes involved in DSAO formation/degradation are unknown.…”

Section: Introductionmentioning

confidence: 97%

A patchwork pathway for oxygenase‐independent degradation of side chain containing steroids

Warnke

Jacoby

Jung

et al. 2017

Environmental Microbiology

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“…strain Aa7, that is able to grow with bile salts as sole carbon source under anoxic conditions with nitrate as electron acceptor. There are only a few studies on the bacterial degradation of steroid compounds under denitrifying conditions, which mainly focused on the metabolism of cholesterol and testosterone (Chiang et al ., ; Fahrbach et al ., ; Wang et al ., ; ; Yang et al ., ; Warnke et al ., ; ). To the best of our knowledge, this is the first study showing bacterial degradation of the steroid skeleton of bile salts under denitrifying conditions.…”

Section: Discussionmentioning

confidence: 99%

The 7α‐hydroxysteroid dehydratase Hsh2 is essential for anaerobic degradation of the steroid skeleton of 7α‐hydroxyl bile salts in the novel denitrifying bacterium Azoarcus sp. strain Aa7

Yücel

Borgert

Niermann

et al. 2019

Environmental Microbiology

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Summary Bile salts are steroid compounds from the digestive tract of vertebrates and enter the environment via defecation. Many aerobic bile‐salt degrading bacteria are known but no bacteria that completely degrade bile salts under anoxic conditions have been isolated so far. In this study, the facultatively anaerobic Betaproteobacterium Azoarcus sp. strain Aa7 was isolated that grew with bile salts as sole carbon source under anoxic conditions with nitrate as electron acceptor. Phenotypic and genomic characterization revealed that strain Aa7 used the 2,3‐seco pathway for the degradation of bile salts as found in other denitrifying steroid‐degrading bacteria such as Sterolibacterium denitrificans. Under oxic conditions strain Aa7 used the 9,10‐seco pathway as found in, for example, Pseudomonas stutzeri Chol1. Metabolite analysis during anaerobic growth indicated a reductive dehydroxylation of 7α‐hydroxyl bile salts. Deletion of the gene hsh2 Aa7 encoding a 7‐hydroxysteroid dehydratase led to strongly impaired growth with cholate and chenodeoxycholate but not with deoxycholate lacking a hydroxyl group at C7. The hsh2 Aa7 deletion mutant degraded cholate and chenodeoxycholate to the corresponding C19‐androstadienediones only while no phenotype change was observed during aerobic degradation of cholate. These results showed that removal of the 7α‐hydroxyl group was essential for cleavage of the steroid skeleton under anoxic conditions.

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“…Stl. denitrificans uses the 2,3-seco pathway (see Figure 1b for detailed information) to degrade androgens regardless of oxygen conditions (Wang et al, 2013a;Wang et al, 2014), and no genes encoding steroid catabolic oxygenases are found in the Stl. denitrificans genome (Dermer and Fuchs, 2012).…”

Section: Sdomentioning

confidence: 99%

“…denitrificans DSMZ 18526 (gammaproteobacterium) and Sterolibacterium (Stl.) denitrificans DSMZ 13999 (betaproteobacterium) as model microorganisms (Wang et al, 2013b(Wang et al, , 2014 (Figure 1b). However, information regarding the catabolic genes and enzymes involved in the anaerobic catabolic pathway is scant.…”

Section: Introductionmentioning

confidence: 99%

Integrated multi-omics analyses reveal the biochemical mechanisms and phylogenetic relevance of anaerobic androgen biodegradation in the environment

et al. 2016

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Steroid hormones, such as androgens, are common surface-water contaminants. However, literature on the ecophysiological relevance of steroid-degrading organisms in the environment, particularly in anoxic ecosystems, is extremely limited. We previously reported that Steroidobacter denitrificans anaerobically degrades androgens through the 2,3-seco pathway. In this study, the genome of Sdo. denitrificans was completely sequenced. Transcriptomic data revealed gene clusters that were distinctly expressed during anaerobic growth on testosterone. We isolated and characterized the bifunctional 1-testosterone hydratase/dehydrogenase, which is essential for anaerobic degradation of steroid A-ring. Because of apparent substrate preference of this molybdoenzyme, corresponding genes, along with the signature metabolites of the 2,3-seco pathway, were used as biomarkers to investigate androgen biodegradation in the largest sewage treatment plant in Taipei, Taiwan. Androgen metabolite analysis indicated that denitrifying bacteria in anoxic sewage use the 2,3-seco pathway to degrade androgens. Metagenomic analysis and PCR-based functional assays showed androgen degradation in anoxic sewage by Thauera spp. through the action of 1-testosterone hydratase/dehydrogenase. Our integrative 'omics' approach can be used for culture-independent investigations of the microbial degradation of structurally complex compounds where isotopelabeled substrates are not easily available.

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Anoxic Androgen Degradation by the Denitrifying Bacterium Sterolibacterium denitrificans via the 2,3-seco Pathway

Cited by 41 publications

References 63 publications

A patchwork pathway for oxygenase‐independent degradation of side chain containing steroids

A patchwork pathway for oxygenase‐independent degradation of side chain containing steroids

The 7α‐hydroxysteroid dehydratase Hsh2 is essential for anaerobic degradation of the steroid skeleton of 7α‐hydroxyl bile salts in the novel denitrifying bacterium Azoarcus sp. strain Aa7

Integrated multi-omics analyses reveal the biochemical mechanisms and phylogenetic relevance of anaerobic androgen biodegradation in the environment

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