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

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. 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. 1-Octen-3-ol is a volatile compound with an earthy and mushroom-like organoleptic property that commonly occurs in nature, such as in mushrooms, molds, and moist air in a laurel forest. It is also found in human breath and sweat. It attracts biting insects, such as mosquitoes (1Potter C.J.H. Stop the biting: targeting a mosquito’s sense of smell.Cell. 2014; 156: 878-881Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar). An olfactory receptor specific to 1-octen-3-ol has been isolated from malaria-causing mosquitoes (2Takke W. Knols B.G.J. Odor-mediated behavior of afrotropical malaria mosquitoes.Annu. Rev. Entomol. 1999; 44: 131-157Crossref PubMed Scopus (497) Google Scholar). Despite its familiarity, the details of the biosynthesis of 1-octen-3-ol, as well as its ecological and physiological significance, are not fully understood. The biosynthetic pathway for 1-octen-3-ol formation in common mushrooms (Agaricus bisporus) has been elucidated by Wurzenberger and Grosch (3Wurzenberger M. Grosch W. The enzymic oxidative breakdown of linoleic acid in mushrooms (Psalliota bispora).Z. Lebensm. Unters. Forsch. 1982; 175: 168-190Crossref Scopus (88) Google Scholar, 4Wurzenberger M. Grosch W. The formation of 1-octen-3-ol from the 10-hydroperoxide isomer of linoleic acid by a hydroperoxide lyase in mushrooms (Psalliota bispora).Biochim. Biophys. Acta. 1984; 794: 25-30Crossref Scopus (113) Google Scholar, 5Wurzenberger M. Grosch W. Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (Psolliota bispora).Biochim. Biophys. Acta. 1984; 795: 163-165Crossref Scopus (72) Google Scholar). Linoleic acid is the substrate, and its stereospecific oxygenation yields the 10(S)-hydroperoxide of linoleic acid (10(S)HPODE) and subsequent cleavage yields (R)-(-)-1-octen-3-ol and 10-oxo-(E)-9-decenoic acid (Fig. 1). The involvement of the 10(S)-isomer as an intermediate to form 1-octen-3-ol from linoleic acid was also confirmed in Lentinula edodes (Shiitake and acid and 1-octen-3-ol in Lentinula edodes and PubMed Scopus Google Scholar, of and and from acid by hydroperoxide PubMed Scopus Google Scholar). the of the enzymes involved in biosynthetic pathway not been for 40 an of oxylipin as are responsible for the biosynthesis of oxylipin biosynthetic genes and in PubMed Scopus Google Scholar, as and communication Full Text Full Text PDF PubMed Scopus Google Scholar, in PubMed Scopus Google Scholar, acid enzymes of PubMed Scopus Google Scholar). is a of a domain its and cytochrome domain the The domain a dioxygenase with such as linoleic acid and and the domain a with the acid hydroperoxide by the domain in PubMed Scopus Google Scholar, acid enzymes of PubMed Scopus Google Scholar). The of such as or show in the of oxygenation on acid by the domain and the of the of is by the domain in PubMed Scopus Google Scholar, acid enzymes of PubMed Scopus Google Scholar). also converts linoleic acid to its to form or linoleic acid M. linoleic acid and hydroperoxide of the fungus Full Text PDF PubMed Google Scholar). from also of an N-terminal domain and C-terminal domain. The domain for the formation of the 10-hydroperoxide of linoleic acid the domain not forms the 10-hydroperoxide of linoleic acid from is a with PubMed Scopus Google Scholar). of the of the hydroperoxide in linoleic enzymes are to be involved in the of 1-octen-3-ol in Ascomycota. of genes in and to 1-octen-3-ol and are by the fungus to Biophys. Acta. Scopus Google Scholar, acid in for 1-octen-3-ol biosynthesis in PubMed Scopus Google Scholar). has not been confirmed the genes of and are involved in the formation of 1-octen-3-ol the of gene not been the of the from to was of and and from acid by hydroperoxide PubMed Scopus Google was not to form 1-octen-3-ol by the from common mushrooms M. Grosch W. Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (Psolliota bispora).Biochim. Biophys. Acta. 1984; 795: 163-165Crossref Scopus (72) Google Scholar). genes with with been in such as and gene that a with to is in of PubMed Scopus (38) Google Scholar, of by with and PubMed Scopus Google the and of the enzymes by genes been we Ccdox1 and in the of the Coprinopsis with from commonly as the is a that its a 2 in the and in the Rev. PubMed Scopus Google Scholar). with and and is for the cinerea is to and a for gene has been of from the of the mushroom Coprinopsis cinerea PubMed Scopus Google Scholar). We characterized the of recombinant CcDOX1 and CcDOX2 in Ccdox1 gene was to its involvement in 1-octen-3-ol The of 1-octen-3-ol the of by mosquitoes and 1-Octen-3-ol has also been to and on and nematodes volatile than a Rev. PubMed Scopus Google its involvement in the is evidence the of 1-octen-3-ol to a cinerea strain in the to form 1-octen-3-ol was to the ecological physiological of 1-octen-3-ol. 1-Octen-3-ol was in the mycelia of cinerea on the formation of of 1-octen-3-ol with and was of the mycelia with (Fig. The formation of 1-octen-3-ol was suppressed in the of (Fig. biosynthesis of 1-octen-3-ol from linoleic formation of 1-octen-3-ol was also the mycelia with a and the formation was suppressed by the of such as or (Fig. a also suppressed 1-octen-3-ol was with the and acid (Fig. and been in as enzymes the dioxygenation of to the hydroperoxide in PubMed Scopus Google we that an enzyme similar to or in the first acid oxygenation step in the biosynthetic pathway to form 1-octen-3-ol. in the of the gene with the gene PubMed Scopus Google was as a for with the cinerea cinerea in for 2014; PubMed Scopus Google with a was the was with as the with and and with than CcDOX1 and CcDOX1 and CcDOX2 are and and and showed that a a with CcDOX1 that of an N-terminal domain to the heme peroxidase and a C-terminal domain that was as a to the cytochrome although the was not as a of in (Fig. was the with a of its C-terminal domain was as a of the cytochrome (Fig. The and in CcDOX1 and and and and in CcDOX1 and for heme are as found with acid oxygenation by and 1999; Full Text Full Text PDF PubMed Scopus Google (Fig. are the in the in the N-terminal of The for acid in was not and is the of in acid oxygenation by and 1999; Full Text Full Text PDF PubMed Scopus Google was with in (Fig. The of the C-terminal domain of is not The of from as a of a acid heme and a cytochrome Full Text Full Text PDF PubMed Scopus Google is of the in the of is in the heme of from as a of a acid heme and a cytochrome Full Text Full Text PDF PubMed Scopus Google is in the has been to be for hydroperoxide in of from as a of a acid heme and a cytochrome Full Text Full Text PDF PubMed Scopus Google and the Cys for as the heme ligand the and of cytochrome Rev. 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The from linoleic acid by recombinant was confirmed to be (Fig. such as and The in of the was and the with acid or to of PubMed Scopus Google the of by of linoleic acid (Fig. The by recombinant CcDOX1 from linoleic acid showed with the as that of with recombinant dioxygenase An of in is a that in with a with specific lyase 2014; Full Text Full Text PDF PubMed Scopus Google (Fig. on the acid of CcDOX1 and the of CcDOX1 by M. with PubMed Scopus Google the the N-terminal domain and the C-terminal domain of CcDOX1 was to be and (Fig. the N-terminal domain to of the C-terminal P450-related was to and in for the formation of from linoleic acid was (Fig. the enzyme was on CcDOX1 showed the with linoleic with a still with acid and acid and to linoleic The with linoleic acid was to the with the of and of (Fig. The of Ccdox1 was via of a gene in the of the Coprinopsis cinerea Scopus Google in the cinerea strain. KO of the Ccdox1 gene (Fig. showed that the to form 1-octen-3-ol was suppressed in KO (Fig. was for WT cinerea was in 1-octen-3-ol slightly in the mycelia on of and by (Fig. mycelia from of 1-octen-3-ol (Fig. the ΔCcdox1 the formation of 1-octen-3-ol of mycelia and the formation in mycelia suppressed (Fig. The of ΔCcdox1 mycelia was slightly than that of the (Fig. with in and (Fig. CcDOX1 lacks the Cys for cytochrome the that CcDOX1 the on to form 1-octen-3-ol be fully is a acid similar domain that for the with acid hydroperoxide form the Full Text Full Text PDF PubMed Scopus Google Scholar, The of from PubMed Scopus Google Scholar, is for of in 2014; PubMed Scopus Google Scholar, 2 is for formation of and PubMed Scopus Google Scholar). recombinant CcDOX1 was with formation of 1-octen-3-ol was the while was 1-octen-3-ol with the from mycelia of WT cinerea (Fig. the with was with the from the WT strain or the ΔCcdox1 difference was in to form 1-octen-3-ol from (Fig. show mushroom 1-octen-3-ol of the and its PubMed Scopus Google Scholar). We the olfactory of the mycelia of cinerea and ΔCcdox1 (Fig. The showed a for mycelia to to a of fungus gnats in the and to mushroom in M. of fungus gnats to with of from and 2014; PubMed Scopus Google Scholar). the on the of the mycelia of or on the mycelia of in the (Fig. and and are fungivorous nematodes of the feeding to and the with Scopus Google Scholar, and of Scopus Google Scholar). We the of nematodes in the WT and ΔCcdox1 and showed in the cinerea (Fig. the of was with ΔCcdox1 than with The biosynthetic pathway to form 1-octen-3-ol from linoleic acid was in in the common mushroom bisporus) (3Wurzenberger M. Grosch W. The enzymic oxidative breakdown of linoleic acid in mushrooms (Psalliota bispora).Z. Lebensm. Unters. Forsch. 1982; 175: 168-190Crossref Scopus (88) Google Scholar, 4Wurzenberger M. Grosch W. The formation of 1-octen-3-ol from the 10-hydroperoxide isomer of linoleic acid by a hydroperoxide lyase in mushrooms (Psalliota bispora).Biochim. Biophys. Acta. 1984; 794: 25-30Crossref Scopus (113) Google Scholar, 5Wurzenberger M. Grosch W. Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (Psolliota bispora).Biochim. Biophys. Acta. 1984; 795: 163-165Crossref Scopus (72) Google the enzymes involved in biosynthesis been identified. an enzyme similar to or as a enzyme that linoleic acid to form its hydroperoxide a of the of the Coprinopsis cinerea Ccdox1 and showed with with to on we of evidence that CcDOX1 in the cinerea is for the first step in 1-octen-3-ol linoleic acid The first of evidence was the recombinant CcDOX1 CcDOX1 is a acid dioxygenase that linoleic acid as the to acid or acid and forms with The recombinant CcDOX2 was also a acid dioxygenase from linoleic the involvement of CcDOX2 in 1-octen-3-ol formation in cinerea was The of recombinant CcDOX2 from linoleic acid was as that was from is as an by a M. and of PubMed Scopus Google Scholar). The of Ccdox1 and genes the of cinerea and the of the in the to form 1-octen-3-ol also the involvement of CcDOX1 in the biosynthesis of 1-octen-3-ol. the of by CcDOX1 is with that of to as an intermediate for 1-octen-3-ol formation in edodes and M. Grosch W. Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (Psolliota bispora).Biochim. Biophys. Acta. 1984; 795: 163-165Crossref Scopus (72) Google Scholar, acid and 1-octen-3-ol in Lentinula edodes and PubMed Scopus Google Scholar, of and and from acid by hydroperoxide PubMed Scopus Google Scholar). The second of evidence was by the Ccdox1 gene in of Ccdox1 in of the of cinerea mycelia to form 1-octen-3-ol. The of a enzyme from mycelia of the WT or ΔCcdox1 in of the hydroperoxide 1-octen-3-ol a similar of indicates that is an intermediate in the biosynthesis of 1-octen-3-ol from linoleic acid in cinerea and that the Ccdox1 gene is for the of linoleic acid to not for the of to form 1-octen-3-ol. The cleavage is to be by of the of the Ccdox1 The involvement of or in 1-octen-3-ol formation in has been the of from linoleic acid is from is a with PubMed Scopus Google Scholar). the of the gene in and 1-octen-3-ol and are by the fungus to Biophys. Acta. Scopus Google Scholar, acid in for 1-octen-3-ol biosynthesis in PubMed Scopus Google Scholar). the enzymes that from and that was not for 1-octen-3-ol with Basidiomycota M. Grosch W. Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (Psolliota bispora).Biochim. Biophys. Acta. 1984; 795: 163-165Crossref Scopus (72) Google Scholar, acid and 1-octen-3-ol in Lentinula edodes and PubMed Scopus Google Scholar, of and and from acid by hydroperoxide PubMed Scopus Google Scholar). the of 1-octen-3-ol in and Basidiomycota is the M. Grosch W. Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (Psolliota bispora).Biochim. Biophys. Acta. 1984; 795: 163-165Crossref Scopus (72) Google Scholar, in mushrooms and and Google to of the that Basidiomycota and form from with a an on the of the biosynthetic pathway of 1-octen-3-ol. the of the gene in and and the of the enzymes was in and is responsible for 1-octen-3-ol in and on the gene in the are to evidence to is to the of Ccdox1 in Basidiomycota to a of the 1-octen-3-ol formation in contain a of and in been acid enzymes of PubMed Scopus Google Scholar). for is a involved in the biosynthesis of that the and and in The and in Full Text Full Text PDF PubMed Scopus Google Scholar). in Basidiomycota not been gene from and genes from to been gene that a with to is in of PubMed Scopus (38) Google Scholar, of by with and PubMed Scopus Google the and of the enzymes by genes been CcDOX1 and CcDOX2 found in as the to also contain an N-terminal domain and a C-terminal P450-related C-terminal P450-related to be as of the with the C-terminal domain of not the Cys that is for the of enzymes as the heme ligand a and of cytochrome Rev. 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