Steroids originating from bacterial bile acid degradation affect Caenorhabditis elegans and indicate potential risks for the fauna of manured soils

Abstract

Bile acids are steroid compounds from the digestive tracts of vertebrates that enter agricultural environments in unusual high amounts with manure. Bacteria degrading bile acids can readily be isolated from soils and waters including agricultural areas. Under laboratory conditions, these bacteria transiently release steroid compounds as degradation intermediates into the environment. These compounds include androstadienediones (ADDs), which are C 19 -steroids with potential hormonal effects. Experiments with Caenorhabditis elegans showed that ADDs derived from bacterial bile acid degradation had effects on its tactile response, reproduction rate, and developmental speed. Additional experiments with a deletion mutant as well as transcriptomic analyses indicated that these effects might be conveyed by the putative testosterone receptor NHR-69. Soil microcosms showed that the natural microflora of agricultural soil is readily induced for bile acid degradation accompanied by the transient release of steroid intermediates. Establishment of a model system with a Pseudomonas strain and C . elegans in sand microcosms indicated transient release of ADDs during the course of bile acid degradation and negative effects on the reproduction rate of the nematode. This proof-of-principle study points at bacterial degradation of manure-derived bile acids as a potential and so-far overlooked risk for invertebrates in agricultural soils.

Proteome, bioinformatic and functional analyses reveal a distinct and conserved metabolic pathway for bile salt degradation in the Sphingomonadaceae

“…These could be involved in transport of bile salts as well as early degradation intermediates such as Δ 4 -3-ketocholate (II in Fig 1 ) or HOCDA (VII), that are found in strain Chol11 culture supernatants (10, 28). Such transient extracellular accumulation of intermediates ( 10) is a common for bile-salt degrading Proteobacteria and has been observed during bile-salt degradation in soil (34). Thus, the above transporters could alternatively be involved in intermediate efflux.…”

“…As the hydroxy group eliminated by Hsh2 must again be added at the stage of HIP intermediates, the benefit of the elimination remains unclear. It might be related to the fact that many intermediates of bile-salt degradation are excreted in significant amounts during growth of bile-salt degrading bacteria not only in laboratory cultures but also in soil samples (10,34). Other bile-salt degrading strains, such as P. stutzeri Chol1, that exclusively use the Δ 1,4 -degradation pathway are unable to utilize Δ 4,6 -compounds as growth substrates (10,27).…”

Microbial degradation of steroid sex hormones: implications for environmental and ecological studies

“…In addition, steroid hormones can be discharged into environments through agricultural applications of municipal sewage biosolids as fertilizers (Lorenzen et al, 2004;Hamid and Eskicioglu, 2012). Moreover, steroid hormones in the environment may partially be the result of microbial activities (Mendelski et al, 2019). For example, phytosterols in pulp and paper mill effluents can be transformed into androgens by microorganisms in river sediments (Jenkins et al, 2003;Orrego et al, 2009).…”

“…Interestingly, the strain Chol1 accumulated extracellular androgenic intermediates such as ADD during the degradation of bile acids (Holert et al , ). The unusual release of the androgens by the bile acid‐degrading bacteria into the environment may have hormonal effects on the coexisting fauna (Mendelski et al , ). In summary, the aerobic catabolic pathways of sterols, bile acid, androgens and progestogens proceed through the oxygen‐dependent 9,10‐ seco pathway, with 9,10‐secosteroids (e.g.…”

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

“…The roles of certain enzymes, mechanisms of their functioning, and interactions with substrates were investigated. Aerobic cholate degradation has been studied mainly for a few Rhodococcus strains such as Rhodococcus jostii RHA1 [ 14 ] and Pseudomonas strains such as Pseudomonas stutzeri Chol1 [ 15 , 16 ] and Pseudomonas putida DOC21 [ 17 ].…”