Biotransformation of [U-13C]linoleic acid suggests two independent ketonic- and aldehydic cycles within C8-oxylipin biosynthesis in Cyclocybe aegerita (V. Brig.) Vizzini

Dominik Karrer,Nikolas Hoberg,Martin Rühl,Vanessa Weigel,Alexander Atamasov

doi:10.1007/s11557-021-01719-3

Dominik Karrer, Nikolas Hoberg + Show 3 more

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https://doi.org/10.1007/s11557-021-01719-3

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Abstract

Although the typical aroma contributing compounds in fungi of the phylum Basidiomycota are known for decades, their biosynthetic pathways are still unclear. Amongst these volatiles, C8-compounds are probably the most important ones as they function, in addition to their specific perception of fungal odour, as oxylipins. Previous studies focused on C8-oxylipin production either in fruiting bodies or mycelia. However, comparisons of the C8-oxylipin biosynthesis at different developmental stages are scarce, and the biosynthesis in basidiospores was completely neglected. In this study, we addressed this gap and were able to show that the biosynthesis of C8-oxylipins differs strongly between different developmental stages. The comparison of mycelium, primordia, young fruiting bodies, mature fruiting bodies, post sporulation fruiting bodies and basidiospores revealed that the occurance of the two main C8-oxylipins octan-3-one and oct-1-en-3-ol distinguished in different stages. Whereas oct-1-en-3-ol levels peaked in the mycelium and decreased with ongoing maturation, octan-3-one levels increased during maturation. Furthermore, oct-2-en-1-ol, octan-1-ol, oct-2-enal, octan-3-ol, oct-1-en-3-one and octanal contributed to the C8-oxylipins but with drastically lower levels. Biotransformations with [U-13C]linoleic acid revealed that early developmental stages produced various [U-13C]oxylipins, whereas maturated developmental stages like post sporulation fruiting bodies and basidiospores produced predominantly [U-13C]octan-3-one. Based on the distribution of certain C8-oxylipins and biotransformations with putative precursors at different developmental stages, two distinct biosynthetic cycles were deduced with oct-2-enal (aldehydic-cycle) and oct-1-en-3-one (ketonic-cycle) as precursors.

Highlights

Volatile compounds like oct-2-en-1-ol (1), octan-1-ol (2), oct-2-enal (3), octanal (4), octan-3-ol (5), oct-1-en-3-ol (6), oct-1-en-3-one (7) and octan-3-one (8) are known as the main C8-oxylipins from which octan-3-ol (5), oct-1en-3-ol (6), oct-1-en-3-one (7) and octan-3-one (8) are the predominant C8-oxylipins contributing to the characteristicSection editor: Marc Stadler.1 3 Vol.:(0123456789)Mycological Progress (2021) 20:929–940 and produces either 13-hydroperoxy-9,11-octadecadienoic acid (13-HPOD) or 9-hydroperoxy-10,12-octadecadienoic acid (9-HPOD), via radical rearrangements and the insertion of molecular oxygen
The composition of endogenous C8-oxylipins at different developmental stages were analysed by means of SPMEGC/MS peak areas
To verify which developmental stage produced the highest amount of a certain C8-oxylipin, the obtained peak areas were expressed as arbitrary units per gram of fresh weight tissue (AU/g ft) (Fig. 1)

Summary

Introduction

Volatile compounds like oct-2-en-1-ol (1), octan-1-ol (2), oct-2-enal (3), octanal (4), octan-3-ol (5), oct-1-en-3-ol (6), oct-1-en-3-one (7) and octan-3-one (8) are known as the main C8-oxylipins from which octan-3-ol (5), oct-1en-3-ol (6), oct-1-en-3-one (7) and octan-3-one (8) are the predominant C8-oxylipins contributing to the characteristicSection editor: Marc Stadler.1 3 Vol.:(0123456789)Mycological Progress (2021) 20:929–940 and produces either 13-hydroperoxy-9,11-octadecadienoic acid (13-HPOD) or 9-hydroperoxy-10,12-octadecadienoic acid (9-HPOD), via radical rearrangements and the insertion of molecular oxygen. LOX/DOX that oxygenate linoleic acid to 10-HPOD in Basidiomycota yet have to be found. Several studies showed that homogenates of fruiting bodies from Basidiomycota produce a variety of C8-oxylipins and are able to convert linoleic acid (Assaf et al, 1995; Husson et al, 2001; Wurzenberger & Grosch 1982). The most detected oxylipins in fruiting bodies include high amounts of compounds 5–8 (Cruz et al, 1997; Li et al, 2016; Mau et al, 1997). The C8-oxylipins 1–4 are represented more unregularly with notably lower amounts in fruiting bodies from which either oct-2-en-1-ol (1) and octan1-ol (2) or oct-2-enal (3) and octanal (4) are predominant (Cho et al 2006, Li et al, 2016; Matsui et al, 2003; Mau et al, 1997)

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