Coprinopsis cinerea dioxygenase is an oxygenase forming 10(S)-hydroperoxide of linoleic acid, essential for mushroom alcohol, 1-octen-3-ol, synthesis

Takuya Teshima, Risa Funai, Takehito Nakazawa, Junya Ito, Toshihiko Utsumi, Pattana Kakumyan, Hiromi Mukai, Toyoshi Yoshiga, Ryutaro Murakami, Kiyotaka Nakagawa, Yoichi Honda, Kenji Matsui

Research output: Contribution to journalArticlepeer-review

5 Citations (Scopus)

Abstract

1-Octen-3-ol is a volatile oxylipin found ubiquitously in Basidiomycota and Ascomycota. The biosynthetic pathway forming 1-octen-3-ol from linoleic acid via the linoleic acid 10(S)-hydroperoxide was characterized 40 years ago in mushrooms, yet the enzymes involved are not identified. The dioxygenase 1 and 2 genes (Ccdox1 and Ccdox2) in the mushroom Coprinopsis cinerea contain an N-terminal cyclooxygenase-like heme peroxidase domain and a C-terminal cytochrome P450-related domain. Herein, we show that recombinant CcDOX1 is responsible for dioxygenation of linoleic acid to form the 10(S)-hydroperoxide, the first step in 1-octen-3-ol synthesis, whereas CcDOX2 conceivably forms linoleic acid 8-hydroperoxide. We demonstrate that KO of the Ccdox1 gene suppressed 1-octen-3-ol synthesis, although added linoleic acid 10(S)-hydroperoxide was still efficiently converted. The P450-related domain of CcDOX1 lacks the characteristic Cys heme ligand and the evidence indicates that a second uncharacterized enzyme converts the 10(S)-hydroperoxide to 1-octen-3-ol. Additionally, we determined the gene KO strain (ΔCcdox1) was less attractive to fruit fly larvae, while the feeding behavior of fungus gnats on ΔCcdox1 mycelia showed little difference from that on the mycelia of the WT strain. The proliferation of fungivorous nematodes on ΔCcdox1 mycelia was similar to or slightly worse than that on WT mycelia. Thus, 1-octen-3-ol seems to be an attractive compound involved in emitter–receiver ecological communication in mushrooms.

Original languageEnglish
Article number102507
JournalJournal of Biological Chemistry
Volume298
Issue number11
DOIs
Publication statusPublished - 2022 Nov

Keywords

  • 1-octen-3-ol
  • cytochrome P450
  • dioxygenase
  • fatty acid metabolism
  • fungi-fungivore interaction
  • mushroom
  • oxylipins

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