Steroids as Environmental Compounds Recalcitrant to Degradation: Genetic Mechanisms of Bacterial Biodegradation Pathways

Abstract

Steroids are perhydro-1,2-cyclopentanophenanthrene derivatives that are almost exclusively synthesised by eukaryotic organisms. Since the start of the Anthropocene, the presence of these molecules, as well as related synthetic compounds (ethinylestradiol, dexamethasone, and others), has increased in different habitats due to farm and municipal effluents and discharge from the pharmaceutical industry. In addition, the highly hydrophobic nature of these molecules, as well as the absence of functional groups, makes them highly resistant to biodegradation. However, some environmental bacteria are able to modify or mineralise these compounds. Although steroid-metabolising bacteria have been isolated since the beginning of the 20th century, the genetics and catabolic pathways used have only been characterised in model organisms in the last few decades. Here, the metabolic alternatives used by different bacteria to metabolise steroids (e.g., cholesterol, bile acids, testosterone, and other steroid hormones), as well as the organisation and conservation of the genes involved, are reviewed.

Genome-Wide Transcriptome Profiling Provides Insight on Cholesterol and Lithocholate Degradation Mechanisms in Nocardioides simplex VKM Ac-2033D

“…The so-called “9(10)- seco -steroid” pathway is the only known route of sterol and cholate degradation by many actinobacteria [ 2 , 3 , 4 , 5 ]. Most strains degrade sterols and cholates via 3-keto-1,4-diene structures that are formed due to consecutive oxidations of 3-hydroxy group and introduction of the corresponding double bond(s) into a steroid core ( Figure 1 ).…”

Anaerobic bacteria need their vitamin B 12 to digest estrogen

“…Because steroids are generally recalcitrant to degradation and can disrupt endocrine functions even at low concentrations in a variety of organisms including humans, the constant release of natural and synthetic steroids into the environment due to agriculture, industry, and sewage is of ever-increasing concern. Hence, bacteria capable of degrading steroids are valuable bioremediation agents (14,15). How bacteria deal with steroids is also important in the context of host-microbe metabolic interdependencies, including in pathogenesis (16).…”

“…Bacterial steroid degradation mechanisms, pathways, and intermediates are well characterized for androgens but less so for estrogens, and aerobic pathways are better charted than anaerobic ones, with most insights emerging from studies of some Actinobacteria and a few α-, β-, and γ-Proteobacteria (14,15). Thus, androgens are degraded aerobically via the 9,10-seco pathway (bond cleavage between ring B carbon atoms C9 and C10 to generate the corresponding secosteroid) or anaerobically in denitrifying bacteria via the 2,3-seco pathway (bond cleavage between ring A atoms C2 and C3) (14,15). Estrogens are more refractory to degradation due to their stable aromatic A-ring and are degraded in some aerobic bacteria by oxygenase-catalyzed cleavage of the bond between ring A atoms C4 and C5 (the 4,5-seco pathway) (14,15).…”

“…Thus, androgens are degraded aerobically via the 9,10-seco pathway (bond cleavage between ring B carbon atoms C9 and C10 to generate the corresponding secosteroid) or anaerobically in denitrifying bacteria via the 2,3-seco pathway (bond cleavage between ring A atoms C2 and C3) (14,15). Estrogens are more refractory to degradation due to their stable aromatic A-ring and are degraded in some aerobic bacteria by oxygenase-catalyzed cleavage of the bond between ring A atoms C4 and C5 (the 4,5-seco pathway) (14,15). Anaerobic estrogen degradation had been reported only in two bacterial species, and the genes and mechanisms involved have remained unknown.…”

Special Issue: Genetics of Biodegradation and Bioremediation

“…Although they are very recalcitrant due to their hydrophobic nature and the absence of functional groups, several steroid-metabolising bacteria have been isolated, and their biodegradation pathways characterised. The different strategies to metabolise steroids by different bacteria, including a comparative analysis of the genes responsible for these activities, are reviewed by Olivera and Luengo [4]. Steroid biodegradation is also the focus of an original research paper by Ibero et al [5], where the testosterone biodegradation pathway of a Novosphingobium strain is inferred from in silico genomic analysis and subsequently confirmed experimentally.…”