Biosynthesis of 1α-hydroxycorticosterone in the winter skate Leucoraja ocellata: evidence to suggest a novel steroidogenic route

J Fish Biol. 2017 Jul;91(1):260-277. doi: 10.1111/jfb.13345. Epub 2017 Jun 7.

Abstract

The present study explores the ability of intracellular bacteria within the renal-inter-renal tissue of the winter skate Leucoraja ocellata to metabolize steroids and contribute to the synthesis of the novel elasmobranch corticosteroid, 1α-hydroxycorticosterone (1α-OH-B). Despite the rarity of C1 hydroxylation noted in the original identification of 1α-OH-B, literature provides evidence for steroid C1 hydroxylation by micro-organisms. Eight ureolytic bacterial isolates were identified in the renal-inter-renal tissue of L. ocellata, the latter being the site of 1α-OH-B synthesis. From incubations of bacterial isolates with known amounts of potential 1α-OH-B precursors, one isolate UM008 of the genus Rhodococcus was seen to metabolize corticosteroids and produce novel products via HPLC analysis. Cations Zn2+ and Fe3+ altered metabolism of certain steroid precursors, suggesting inhibition of Rhodococcus steroid catabolism. Genome sequencing of UM008 identified strong sequence and structural homology to that of Rhodococcus erythropolis PR4. A complete enzymatic pathway for steroid-ring oxidation as documented within other Actinobacteria was identified within the UM008 genome. This study highlights the potential role of Rhodococcus bacteria in steroid metabolism and proposes a novel alternative pathway for 1α-OH-B synthesis, suggesting a unique form of mutualism between intracellular bacteria and their elasmobranch host.

Keywords: Rhodococcus sp; corticosteroid; elasmobranch; steroid metabolism.

MeSH terms

  • Animals
  • Chromatography, High Pressure Liquid
  • Corticosterone / analogs & derivatives*
  • Corticosterone / biosynthesis*
  • DNA, Bacterial / isolation & purification
  • Female
  • Genome, Bacterial
  • Kidney / metabolism
  • Kidney / microbiology
  • Kidney / ultrastructure
  • Liver / microbiology
  • Male
  • Microscopy, Electron, Transmission
  • Rhodococcus / genetics
  • Rhodococcus / metabolism*
  • Rhodococcus / ultrastructure
  • Skates, Fish / genetics
  • Skates, Fish / metabolism*
  • Skates, Fish / microbiology
  • Steroid Hydroxylases / metabolism
  • Steroids / metabolism
  • Urea / metabolism

Substances

  • DNA, Bacterial
  • Steroids
  • 1 alpha-hydroxycorticosterone
  • Urea
  • Steroid Hydroxylases
  • Corticosterone