Interactions between soil- and dead wood-inhabiting fungal communities during the decay of Norway spruce logs

OPEN The ISME Journal (2017) 11, 1964–1974 www.nature.com/ismej ORIGINAL ARTICLE Interactions between soil- and dead wood-inhabiting fungal communities during the decay of Norway spruce logs Raisa Mäkipää1, Tiina Rajala1,4, Dmitry Schigel2, Katja T Rinne1, Taina Pennanen1, Nerea Abrego3 and Otso Ovaskainen2,3 1 Natural Resources Institute Finland (Luke), Helsinki, Finland; 2Department of Biosciences, University of Helsinki, Helsinki, Finland and 3Department of Biology, Centre for Biodiversity Dynamics, Norwegian University of Science and Technology, Trondheim, Norway We investigated the interaction between fungal communities of soil and dead wood substrates. For this, we applied molecular species identification and stable isotope tracking to both soil and decaying wood in an unmanaged boreal Norway spruce-dominated stand. Altogether, we recorded 1990 operational taxonomic units, out of which more than 600 were shared by both substrates and 589 were found to exclusively inhabit wood. On average the soil was more species-rich than the decaying wood, but the species richness in dead wood increased monotonically along the decay gradient, reaching the same species richness and community composition as soil in the late stages. Decaying logs at all decay stages locally influenced the fungal communities from soil, some fungal species occurring in soil only under decaying wood. Stable isotope analyses suggest that mycorrhizal species colonising dead wood in the late decay stages actively transfer nitrogen and carbon between soil and host plants. Most importantly, Piloderma sphaerosporum and Tylospora sp. mycorrhizal species were highly abundant in decayed wood. Soil- and wood-inhabiting fungal communities interact at all decay phases of wood that has important implications in fungal community dynamics and thus nutrient transportation. The ISME Journal (2017) 11, 1964–1974; doi:10.1038/ismej.2017.57; published online 21 April 2017 Introduction Fungi have essential roles in forest ecosystem functioning. Saprotrophic fungi are key regulators of nutrient recycling and the main agents decomposing organic matter (Boddy et al., 2008), and mycorrhizal fungi are of crucial importance in facilitating nutrient uptake for plants (Smith and Read, 2008). Therefore, fungal communities affect the rate of decomposition, nutrient cycling and resiliency of the ecosystem functioning (Hättenschwiler et al., 2005; Gessner et al., 2010; Valentín et al., 2014). Mycorrhizal fungi are mainly found in soil where their mycelia is associated to plant roots, and saprotrophic fungi inhabit both soil and dead wood, where decomposable organic resources are available. Saprotrophic fungal communities from soil and woody substrates are qualitatively different, as fungi utilising wood and fungi decomposing the organic matter in soil employ Correspondence: R Mäkipää, Natural Resources Institute Finland (Luke), Latokartanonkaari 9, FI-00790 Helsinki, Finland. E-mail: 4 Deceased. Received 20 December 2016; revised 18 February 2017; accepted 3 March 2017; published online 21 April 2017 different ecophysiological strategies adapted to the characteristics of each substrate (Watkinson et al., 2006). As a result of the fungal decomposition process, dead wood resources eventually become soil, and soil- and wood-inhabiting fungal communities converge. Soil- and wood-inhabiting fungal communities are more similar in the advanced decay stages of dead wood (for example, Renvall, 1995; Rajala et al., 2012; Ottosson et al., 2014), yet the timing of the species exchange and its consequences in nutrient cycling and fungal community dynamics remain poorly understood. Fungal communities in soil and wood have typically been studied separately (Buée et al., 2009; Kubartová et al., 2012; Ovaskainen et al., 2013), but several studies have noted the presence of wooddecaying fungi in soil (for example, Lindahl et al., 2007) and conversely the presence of mycorrhizal fungi in wood (Tedersoo et al., 2003; Rajala et al., 2012, 2015). Indeed, many mycorrhizal fungi are also able to colonise woody substrates that are heavily decayed and in contact with the soil surface (Tedersoo et al., 2003), whereas many soil saprotrophs are able to colonise wood (Rayner and Boddy, 1988). Some mycorrhizal species even tend to produce fruiting bodies more often in wood than Interaction between soil- and wood-inhabiting fungi R Mäkipää et al they do in soil (for example, Piloderma, Tomentella and Tylospora species) (Stokland et al., 2012). The mycorrhizal species which are able to colonise wood have the ability to obtain mineral nutrients through decomposition, in addition to their primary strategy of translocating nutrients to plant roots (Lindahl and Tunlid, 2015). Conversely, some wood-decaying fungi (in particular cord-forming basidiomycetes) are able to grow out of the wood and forage for new resources in soil (for example, Armillaria, Hypholoma and Phanerochaete species; Boddy, 1993, 1999). Even if most occurrences of mycorrhizal fungi in dead wood have been reported for the last decay phases of dead wood (Renvall, 1995; Rajala et al., 2012, 2015; Ottosson et al., 2014), the colonisation of dead wood by mycorrhizal fungi might happen in earlier phases of wood decay. For instance, some Tomentella species have been found to occur more often in dead wood in intermediate decay phases than in late decay phases (cf. Edman and Jonsson, 2001; Abrego and Salcedo, 2013). As another example of species exchange between soil and wood in early phases of decay, the cord-forming Armillaria species extend their mycelia from dead wood through soil and colonise living trees (Ferguson et al., 2003). The exchange of fungal species between wood and soil has important implications in forest nutrient cycling. As shown by Mahmood et al. (2003), the mycorrhizal activity of some fungal species is stimulated when they colonise woody substrates that ultimately improves plant growth. The nutrients accumulated in wood resources are reallocated in soil by wood-decaying saprotrophs, which can extend their mycelial networks many metres from where the wood pieces are located (Boddy and Watkinson, 1995). Conversely, wood-decaying fungi with rhizomorphs can translocate 15N-enriched nitrogen from the forest floor to decaying logs, and thus fungi-mediated nitrogen transport from the soil can be a source of external nitrogen in decaying logs (Philpott et al., 2014). This additional nutritional income in dead wood might have important implications in the decomposition process, as the activity of saprotrophic fungi is stimulated when the nitrogen availability is enhanced (Bebber et al., 2011). As fungal species colonise new habitats, they are exposed not only to a new abiotic environment, but also to a new biotic environment where other fungal species are utilising the same resources. Interspecific combative interactions occur commonly between fungi that share a given habitat and hav (...truncated)