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Biodegradation

A Novel Steroid-Coenzyme A Ligase from Novosphingobium sp. Strain Chol11 Is Essential for an Alternative Degradation Pathway for Bile Salts

Onur Yücel, Johannes Holert, Kevin Christopher Ludwig, Sven Thierbach, Bodo Philipp
Maia Kivisaar, Editor
Onur Yücel
aWestfälische Wilhelms-Universität Münster, Institut für Molekulare Mikrobiologie und Biotechnologie, Münster, Germany
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Johannes Holert
bUniversity of British Columbia, Department of Microbiology and Immunology, Life Sciences Institute, Vancouver, British Columbia, Canada
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Kevin Christopher Ludwig
aWestfälische Wilhelms-Universität Münster, Institut für Molekulare Mikrobiologie und Biotechnologie, Münster, Germany
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Sven Thierbach
aWestfälische Wilhelms-Universität Münster, Institut für Molekulare Mikrobiologie und Biotechnologie, Münster, Germany
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Bodo Philipp
aWestfälische Wilhelms-Universität Münster, Institut für Molekulare Mikrobiologie und Biotechnologie, Münster, Germany
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Maia Kivisaar
University of Tartu
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DOI: 10.1128/AEM.01492-17
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ABSTRACT

Bile salts such as cholate are steroid compounds with a C5 carboxylic side chain and occur ubiquitously in vertebrates. Upon their excretion into soils and waters, bile salts can serve as growth substrates for diverse bacteria. Novosphingobium sp. strain Chol11 degrades 7-hydroxy bile salts via 3-keto-7-deoxy-Δ4,6 metabolites by the dehydration of the 7-hydroxyl group catalyzed by the 7α-hydroxysteroid dehydratase Hsh2. This reaction has not been observed in the well-studied 9-10-seco degradation pathway used by other steroid-degrading bacteria indicating that strain Chol11 uses an alternative pathway. A reciprocal BLASTp analysis showed that known side chain degradation genes from other cholate-degrading bacteria (Pseudomonas stutzeri Chol1, Comamonas testosteroni CNB-2, and Rhodococcus jostii RHA1) were not found in the genome of strain Chol11. The characterization of a transposon mutant of strain Chol11 showing altered growth with cholate identified a novel steroid-24-oyl–coenzyme A ligase named SclA. The unmarked deletion of sclA resulted in a strong growth rate decrease with cholate, while growth with steroids with C3 side chains or without side chains was not affected. Intermediates with a 7-deoxy-3-keto-Δ4,6 structure, such as 3,12-dioxo-4,6-choldienoic acid (DOCDA), were shown to be likely physiological substrates of SclA. Furthermore, a novel coenzyme A (CoA)-dependent DOCDA degradation metabolite with an additional double bond in the side chain was identified. These results support the hypothesis that Novosphingobium sp. strain Chol11 harbors an alternative pathway for cholate degradation, in which side chain degradation is initiated by the CoA ligase SclA and proceeds via reaction steps catalyzed by so-far-unknown enzymes different from those of other steroid-degrading bacteria.

IMPORTANCE This study provides further evidence of the diversity of metabolic pathways for the degradation of steroid compounds in environmental bacteria. The knowledge about these pathways contributes to the understanding of the CO2-releasing part of the global C cycle. Furthermore, it is useful for investigating the fate of pharmaceutical steroids in the environment, some of which may act as endocrine disruptors.

FOOTNOTES

    • Received 7 July 2017.
    • Accepted 6 October 2017.
    • Accepted manuscript posted online 20 October 2017.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.01492-17.

  • Copyright © 2017 American Society for Microbiology.

All Rights Reserved.

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A Novel Steroid-Coenzyme A Ligase from Novosphingobium sp. Strain Chol11 Is Essential for an Alternative Degradation Pathway for Bile Salts
Onur Yücel, Johannes Holert, Kevin Christopher Ludwig, Sven Thierbach, Bodo Philipp
Applied and Environmental Microbiology Dec 2017, 84 (1) e01492-17; DOI: 10.1128/AEM.01492-17

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A Novel Steroid-Coenzyme A Ligase from Novosphingobium sp. Strain Chol11 Is Essential for an Alternative Degradation Pathway for Bile Salts
Onur Yücel, Johannes Holert, Kevin Christopher Ludwig, Sven Thierbach, Bodo Philipp
Applied and Environmental Microbiology Dec 2017, 84 (1) e01492-17; DOI: 10.1128/AEM.01492-17
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KEYWORDS

CoA ligase
Novosphingobium
bile salts
steroid degradation

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