Abstract
The application of thermophilic microorganisms opens new prospects in steroid biotechnology, but little is known to date on steroid catabolism by thermophilic strains. The thermophilic strain Saccharopolyspora hirsuta VKM Ac-666T has been shown to convert various steroids and to fully degrade cholesterol. Cholest-4-en-3-one, cholesta-1,4-dien-3-one, 26-hydroxycholest-4-en-3-one, 3-oxo-cholest-4-en-26-oic acid, 3-oxo-cholesta-1,4-dien-26-oic acid, 26-hydroxycholesterol, 3β-hydroxy-cholest-5-en-26-oic acid were identified as intermediates in cholesterol oxidation. The structures were confirmed by 1H and 13C-NMR analyses. Aliphatic side chain hydroxylation at C26 and the A-ring modification at C3, which are putatively catalyzed by cytochrome P450 monooxygenase CYP125 and cholesterol oxidase, respectively, occur simultaneously in the strain and are followed by cascade reactions of aliphatic sidechain degradation and steroid core destruction via the known 9(10)-seco-pathway. The genes putatively related to the sterol and bile acid degradation pathways form three major clusters in the S. hirsuta genome. The sets of the genes include the orthologs of those involved in steroid catabolism in Mycobacterium tuberculosis H37Rv and Rhodococcus jostii RHA1 and related actinobacteria. Bioinformatics analysis of 52 publicly available genomes of thermophilic bacteria revealed only seven candidate strains that possess the key genes related to the 9(10)-seco pathway of steroid degradation, thus demonstrating that the ability to degrade steroids is not widespread among thermophilic bacteria.
Highlights
Steroids are abundant biomolecules in various environments and growth substrates for diverse bacteria
The sterol degradation pathway is known to begin with the modification of 3β-hydroxy-5-ene into the 3-keto-4-ene structure by cholesterol oxidases (ChOs) or 3β-hydroxysteroid dehydrogenases (3β-HSDs) [48,49], while cytochrome P450mediated hydroxylation at C26(27) has been reported to be the initial reaction of sterol degradation in Rhodococcus strains [50,51]
The thermophilic strain Saccharopolyspora hirsuta VKM Ac-666T is capable of transforming various steroids [23,24]
Summary
Steroids are abundant biomolecules in various environments and growth substrates for diverse bacteria. Bile acids differ from sterols by cis-A/B-ring juncture, α-orientation of hydroxyl at C3, a saturated steroid core, and a C5 acyl side chain. Modern bioinformatics studies of publicly available genomes/metagenomes have highlighted the global distribution of actinobacteria capable of sterol and cholate degradation from various ecological niches (soil, aquatic environments, waste, etc.) [1,2]. The so-called 9(10)-seco-steroid pathway is the only one known for sterol and cholate aerobic degradation by actinobacteria [3,4,5,6]. This pathway has been intensively studied in the Microorganisms 2021, 9, 2554.
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