Diverse Ecological Roles Within Fungal Communities in Decomposing Logs

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Diverse Ecological Roles Within Fungal Communities in Decomposing Logs FEMS Microbiology Ecology, 91, 2015, fiv012 doi: 10.1093/femsec/fiv012 Advance Access Publication Date: 6 February 2015 Research Article RESEARCH ARTICLE Diverse ecological roles within fungal communities Downloaded from https://academic.oup.com/femsec/article-abstract/91/3/fiv012/436629 by guest on 06 August 2020 in decomposing logs of Picea abies Elisabet Ottosson1, Ariana Kubartova´ 1, Mattias Edman2,MariJonsson¨ 3, Anders Lindhe4, Jan Stenlid1 and Anders Dahlberg1,∗ 1Department of Forest Mycology and Plant Pathology, BioCenter, Swedish University of Agricultural Sciences, Uppsala SE-750 07, Sweden, 2Department of Natural Sciences, Mid Sweden University, SE-851 70 Sundsvall, Sweden, 3Swedish Species Information Centre, Swedish University of Agricultural Sciences, Uppsala SE-750 07, Sweden and 4Armfeltsgatan 16, SE-115 34 Stockholm, Sweden ∗ Corresponding author: Department of Forest Mycology and Plant Pathology, BioCenter, Swedish University of Agricultural Sciences, Uppsala SE-750 07, Sweden. Tel: +46-70-3502745; E-mail: [email protected] One sentence summary: A Swedish DNA-barcoding study revealed 1910 fungal species in 38 logs of Norway spruce and not only wood decayers but also many mycorrhizal, parasitic other saprotrophic species. Editor: Ian C Anderson ABSTRACT Fungal communities in Norway spruce (Picea abies) logs in two forests in Sweden were investigated by 454-sequence analyses and by examining the ecological roles of the detected taxa. We also investigated the relationship between fruit bodies and mycelia in wood and whether community assembly was affected by how the dead wood was formed. Fungal communities were highly variable in terms of phylogenetic composition and ecological roles: 1910 fungal operational taxonomic units (OTUs) were detected; 21% were identified to species level. In total, 58% of the OTUs were ascomycetes and 31% basidiomycetes. Of the 231 337 reads, 38% were ascomycetes and 60% basidiomycetes. Ecological roles were assigned to 35% of the OTUs, accounting for 62% of the reads. Wood-decaying fungi were the most common group; however, other saprotrophic, mycorrhizal, lichenized, parasitic and endophytic fungi were also common. Fungal communities in logs formed by stem breakage were different to those in logs originating from butt breakage or uprooting. DNA of specific species was detected in logs many years after the last recorded fungal fruiting. Combining taxonomic identification with knowledge of ecological roles may provide valuable insights into properties of fungal communities; however, precise ecological information about many fungal species is still lacking. Key words: boreal forest; decaying wood; fungal diversity; fungal ecology; Norway spruce; pyrosequencing INTRODUCTION dia, our knowledge about the distribution and ecology of these fungi is based primarily on fruit body observations (Stokland, Dead wood is pivotal for species diversity and for certain ecosys- Siitonen and Jonsson 2012). However, for most of its life, a tem processes in forests (Stokland, Siitonen and Jonsson 2012). wood-inhabiting fungus is cryptic and difficult to study, and as In northern Europe, more than 7500 species, mainly fungi yet the diversity, spatio-temporal dynamics and factors regu- and insects, are dependent on wood (Siitonen 2001; Stokland, lating the presence of fungal species in wood are poorly un- Siitonen and Jonsson 2012). Although more than 2500 wood- derstood. However, novel high-throughput sequencing methods inhabiting fungal species have been reported in Fennoscan- and bioinformatics tools have enabled new insights into fungal Received: 14 December 2014; Accepted: 26 January 2015 C FEMS 2015. All rights reserved. For permissions, please e-mail: [email protected] 1 2 FEMS Microbiology Ecology, 2015, Vol. 91, No. 3 phylogenetics and community ecology (Hibbett et al., 2011;Lin- succession (spatiotemporal dynamics) of wood-inhabiting fungi. dahl et al., 2013; Bohmann et al., 2014). Wood-decaying fungi are typically unit restricted, and selection Studies using high-throughput sequencing methods have re- for combative long-lived mycelia has implications for species fit- ported a remarkably high and largely cryptic species richness of ness and the degree of species turnover during the decomposi- fungi in environmental samples from litter, soil and wood (e.g. tion of wood. Buee´ et al., 2009; Kubartova´ et al., 2012; Clemmensen et al., 2013; Early establishing fungi may significantly affect subsequent Meiser, Balint and Schmitt 2013; Vorˇ´ıskovˇ a´ and Baldrian 2013; fungal community development in wood by capturing space Tedersoo et al., 2014). The number of operational taxonomic and modifying the wood (Renvall 1995; Fukami et al., 2010; units (OTUs) that can be identified to species level or to a higher Ottosson et al., 2014). Field observations, field experiments and taxon level is steadily increasing as databases with reliable se- time-series analyses of fruit bodies suggest that primary species quenced fungal taxa continue to grow. Identified sequences can may cause priority effects and non-random co-occurrence pat- be used to characterize communities phylogenetically, and can terns of wood-inhabiting fungal communities (Renvall 1995; also be linked to species distributions and life strategies to gain Pouska et al., 2011;Lindneret al., 2011; Ottosson et al., 2014;see Downloaded from https://academic.oup.com/femsec/article-abstract/91/3/fiv012/436629 by guest on 06 August 2020 deeper insights into fungal ecology and fungal-mediated pro- also Stokland, Siitonen and Jonsson 2012). Coarse dead wood cesses, as recent studies of wood-inhabiting fungi have demon- in Norway spruce forests occurs as a result of different distur- strated (Kubartova´ et al., 2012; Rajala et al., 2012;Ovaskainen bance agents, such as strong winds and heart-rot fungi, which et al., 2013; van der Wal, Ottosson and de Boer 2015). is likely to affect the fungal communities that develop in the Molecular phylogenetics has been widely used to determine coarse wood (Johannesson and Stenlid 1999;Edman,Jonsson¨ whether the phylogenetic relatedness of interacting species may and Jonsson 2007; Kuuluvainen and Aakala 2011). However, as help to explain mechanisms behind the coexistence of species yet, few studies have related community composition to the ori- and the functional consequences of phylogenetic relatedness gin of the decaying wood. in communities (Webb et al., 2002; Vamosi et al., 2009;Pausas In an earlier study, we detected 1910 fungal OTUs in an eval- and Verdu 2010). Phylogenetically closely related species tend uation of the fine-scale distribution of fungal mycelia within to be ecologically more similar than distantly related species and among decaying Norway spruce logs (Kubartova´ et al., 2012). (McGuire et al., 2010). This could, in theory, result in strong com- We concluded that in addition to the wood decayers, fungi with petition among closely related lineages due to niche overlap. Al- other ecological roles also appeared to be significant in wood. ternatively, functional complementarities may evolve, resulting Here, we present an in-depth species level analysis of the in coexistence between distinct evolutionary lineages due to re- phylogenetic diversity and ecological roles, or nutritional strate- duced competition and enhanced ecosystem functioning (Ma- gies, of the wood-inhabiting fungal communities reported in our herali and Klironomos 2007;Rinconet al., 2014). However, evi- earlier study (Kubartova´ et al., 2012). To achieve this, we linked dence that these assumptions apply to fungal communities is the identities of fungal taxa detected in wood by 454 sequencing limited (but see Maherali and Klironomos 2007;Rinconet al., with their known ecological roles as compiled from the scientific 2014). literature. We also combined the molecular data with long-term The relationship between fruit bodies and mycelia in wood fruit-body inventories of the same sites to examine our expec- is not simple because many species are predominantly or only tation that mycelia may be present despite the absence of fruit present as mycelia (e.g. Allmer´ et al., 2006; Kubartova´ et al., 2012; bodies and that mycelia may still be present many years after Monard, Gantner and Stenlid 2013), which has also been found the production of fruit bodies has ceased. Finally, we used the to be the case in studies of soil fungal communities (e.g. Porter, data from one of the sites where the logs had been formed as a Skillman and Moncalvo 2008; Hibbett et al., 2011; Clemmensen result of different types of stem breakage to explore whether the et al., 2013). Indeed, the majority of fungal OTUs detected in cause of tree death may affect the resulting fungal community wood to date represent either taxa that cannot be named ow- composition. ing to a lack of reference sequences or taxa that are as yet un- described (e.g. Kubartova´ et al., 2012). However, typically, a small MATERIALS AND METHODS proportion of the OTUs, whose taxonomic identity and ecologi- cal role is generally known, form a significant proportion of the The work reported in the present study was a continuation of sequence reads, implying that these OTUs perform a relatively a study of the fine-scale distribution of fungal mycelia within large proportion of the fungal functions in wood. 38 logs at two forest sites reported by Kubartova´ et al. (2012). A Fruit-body analyses of wood-inhabiting fungal species can summary of the study sites and the methods are given
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