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

Abstract

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.

Catabolism of the Last Two Steroid Rings in Mycobacterium tuberculosis and Other Bacteria

“…The HIP catabolic genes are conserved in steroid-degrading bacteria for which genome sequence data are available, suggesting that the pathway is employed not only in the degradation of steroids other than cholesterol (2, 3, 9), but also in the anaerobic degradation of steroids (4). Indeed, differences in the HIP catabolic gene cluster in diverse bacteria appear to reflect the different steroid-catabolizing capabilities of the strains.…”

“…A homolog of EchA20, EchA13 is proposed to remove the hydroxyl of 7β-OH HIP, generated from cholate degradation (10, 20), and is not present in M. tuberculosis , which does not degrade cholate. Similarly, the HIP catabolic gene cluster of S. denitrificans DSM 18526, which is upregulated during the aerobic and anaerobic catabolism of testosterone (4), lacks a homolog of fadD3 / stdA3 (Fig. 1).…”

“…Actinobacteria that contain multiple steroid catabolic pathways appear to complete this catabolism using a single HIP catabolic pathway (9). Interestingly, recent bioinformatic and transcriptomic studies indicate that the aerobic and anaerobic steroid degradation pathways of Steroidobacter denitrificans also converge at HIP (4) (Fig. 1B).…”

“…However, the only known organisms that can catabolize steroids and utilize them as growth substrates are bacteria (1). Bacterial steroid catabolism can be either aerobic, as occurs in most mycolic acid-containing actinobacteria and some proteobacteria (1–3), or anaerobic, as in some proteobacteria (4). Aerobic catabolism has been studied for many decades, due in part to its potential to transform low-value steroids into high-value ones (5).…”

A Community Multi-Omics Approach towards the Assessment of Surface Water Quality in an Urban River System

“…To date, such studies have focused on specific pollution events (e.g., the Deepwater Horizon oil spill [20]), the assessment of biotechnology/bioremdiation (e.g., bioremdiation of steriods in the enviornment [21]) or used to characterize well-controlled engineered systems (e.g., anerobic bioreactors [22,23]). To the best of our knowledge, such an approach has not been used to characterize a system as part of a water quality monitoring survey.…”