Mycenaspecies can be opportunist-generalist plant root invaders

Abstract

SummaryRecently, several saprotrophic genera have been found to invade/interact with plant roots in laboratory growth experiments, and this coincides with reports of abundant saprotrophic fungal sequences in plant roots. However, it is uncertain if this reflects field phenomena, and if reports on coincidentally amplified saprotrophs are simply coincidental.We investigated root invasion by presumed saprotrophic fungi by focusing on the large genus Mycena in 1) a systematic analysis of the occurrence of saprotrophic fungi in new and previously published ITS1/ITS2 datasets generated from roots of 10 mycorrhizal plant species, and 2) we analysed natural abundances of 13C/15N stable isotope signatures of fungal/plant communities from five comparable field locations to examine the trophic status of Mycena species.Mycena was the only saprotrophic genus consistently found in 9 of 10 plant host roots, with high within-host variation in Mycena sequence proportions (0-80%) recovered. Mycena carpophores displayed isotopic signatures consistent with published 13C/15N profiles of both saprotrophic or mutualistic lifestyles, with considerable intraspecific variation, resembling the patterns seen in growth experiments. These results indicate that multiple Mycena species opportunistically invade the roots of a range of plant species, possibly forming a spectrum of interactions. This potentially challenges our general understanding of fungal ecology.Originality significance statementThis is the first study to apply a dual approach of systematic metabarcoding of plant roots and stable isotope signatures on dried field material to the large and common saprotrophic fungal genus Mycena. This is significant as it shows that members of this genus, normally not expected to be found inside plant roots at all, are in fact associated eith multiple plant hosts. The study furthermore shows that species in this genus may occupy different ecological roles in the field besides being saprotrophic. That a large and common fungal genus known to be a quantitatively important litter decayer can be an opportunistic root invader and interact with host plants is of interest to all mycologists and ecologists working on plant-fungus/microb symbiosis.

Fungi in hair roots of Vaccinium spp. (Ericaceae) growing on decomposing wood: colonization patterns, identity, and in vitro symbiotic potential

“…However, both sets of samples yielded several basidiomycetous OTU that could be linked to genera traditionally reserved for saprobes, namely Coprinellus , Gymnopilus , Hypochnicium and Mycena , the last being the most prevalent. Mycena (Mycenaceae, Agaricales) contains more than 1900 species (mycobank.org, accessed 23/8/2022) and while these are typically saprobic, they also associate with plant roots (see Harder et al ( 2021 ) and references therein) and engage in the orchid mycorrhizal symbiosis (e.g., Ogura-Tsujita et al 2009 ; Zhang et al 2012 ; Lee et al 2015 ). Mycena are not uncommon in ericaceous roots (see Grelet et al ( 2017 ) and references therein) but the mode of their interactions needs to be clarified (also see below).…”

Metagenomic Analyses of the Soybean Root Mycobiome and Microbiome Reveal Signatures of the Healthy and Diseased Plants Affected by Taproot Decline

“…From the Basidiomycota, the Agaricales Mycena maurella and Hymenopellis dominated E-S2 [ 60 ] (48% and 15%, respectively). M. maurella belongs to the widespread saprotrophic genus Mycena ; although not expected to be found as a root endophyte, Mycena associates with multiple plant hosts and was suggested to be an opportunistic root pathogen [ 61 ]. Interestingly, Hymenopellis, growing mainly on dead or buried hardwoods, was found to be a rich resource of bioactive compounds with antimicrobial, antioxidative, anti-inflammatory activities [ 62 ].…”

Prosperity of the commons: Generalist mycorrhizal species dominate a mixed forest and may promote forest diversity by mediating resource sharing among trees

“…Some species of Mycena and Gymnopus are known as saprotrophic fungi that were recruited as mycorrhizal symbionts of certain mycoheterotrophic orchids(Selosse et al 2010). Mycena , root-associated saprotrophic fungi, were found to occupy tree roots and to be involved in carbon and phosphorous transfer between fungi and their host in a manner similar to that of mycorrhizal species (Thoen et al 2020, Harder et al 2021). Here, the two Mycena species and the single Gymnopus species were identified in FUNGuild as saprotrophic (Fig.…”