Vertical and seasonal dynamics of fungal communities in boreal Scots pine forest soil

FEMS Microbiology Ecology, 92, 2016, fiw170 doi: 10.1093/femsec/fiw170 Advance Access Publication Date: 10 August 2016 Research Article RESEARCH ARTICLE Minna Santalahti1 , Hui Sun1,2 , Ari Jumpponen3 , Taina Pennanen4 and Jussi Heinonsalo1,∗ 1 Department of Food and Environmental Sciences, University of Helsinki, PO Box 56, FI-00014 Helsinki, Finland, 2 Collaborative Innovation Center of Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing 210037, China, 3 Division of Biology, Kansas State University, 433 Ackert Hall, Manhattan, KS 66506, USA and 4 Natural Resources Institute Finland, PO Box 18, FI-01301 Vantaa, Finland ∗ Corresponding author: Department of Food and Environmental Sciences, University of Helsinki, PO Box 56 (Viikinkaari 9), FI-00014 Helsinki, Finland. Tel: +358-2941-59317; E-mail: One sentence summary: Fungal communities were diverse also in deeper soil horizons, and they varied significantly both vertically and seasonally; community structure in winter was the most different compared to the growing season. Editor: Petr Baldrian ABSTRACT Fungal communities are important for carbon (C) transformations in boreal forests that are one of the largest C pools in terrestrial ecosystems, warranting thus further investigation of fungal community dynamics in time and space. We investigated fungal diversity and community composition seasonally and across defined soil horizons in boreal Scots pine forest in Finland using 454 pyrosequencing. We collected a total of 120 samples from five vertical soil horizons monthly from March to October; in March, under snow. Boreal forest soil generally harbored diverse fungal communities across soil horizons. The communities shifted drastically and rapidly over time. In late winter, saprotrophs dominated the community and were replaced by ectomycorrhizal fungi during the growing season. Our studies are among the first to dissect the spatial and temporal dynamics in boreal forest ecosystems and highlights the ecological importance of vertically distinct communities and their rapid seasonal dynamics. As climate change is predicted to result in warmer and longer snow-free winter seasons, as well as increase the rooting depth of trees in boreal forest, the seasonal and vertical distribution of fungal communities may change. These changes are likely to affect the organic matter decomposition by the soil-inhabiting fungi and thus alter organic C pools. Keywords: boreal forest; fungal diversity; mycorrhiza; saprotroph; seasonal dynamics; vertical dynamics INTRODUCTION Boreal forest soils are important in global nutrient and carbon (C) cycling and a net sink for carbon (Goodale et al. 2002; Magnani et al. 2007). The large C pools in boreal soils consist of C stored in soil organic matter (SOM) as plant litter and humic materials (Berg et al. 2009). Fungi are an important component of microbiota and the predominant decomposers in boreal forests. With their various extracellular enzymes, fungi have unique access to e.g. growth-limiting nitrogen that is bound to recalcitrant SOM (De Boer et al. 2005; Bödeker et al. 2014; Rytioja et al. 2014; Kohler et al. 2015). Saprotrophic (SAP) and wood or litter-decomposing fungi break down a variety of organic compounds and contribute to soil nutrient cycling (Lindahl, Taylor and Finlay 2002). Ectomycorrhizal (ECM) and ericoid mycorrhizal (ERM) fungi form symbiotic relationships with forest trees and understory shrubs, thus Received: 15 April 2016; Accepted: 5 August 2016  C FEMS 2016. All rights reserved. For permissions, please e-mail: 1 Vertical and seasonal dynamics of fungal communities in boreal Scots pine forest soil 2 FEMS Microbiology Ecology, 2016, Vol. 92, No. 11 Second, by combining modeling and ecosystem flux data, Piao et al. (2008) concluded that a net loss of CO2 in northern terrestrial biomes is a response to autumn warming resulting from climate change. This net loss was primarily driven by the relatively greater increases in respiration compared to photosynthesis. More information is needed to understand how this late autumn warming and CO2 loss will affect soil C storage and the interaction between trees and soil fungi. Koorem et al. (2014) dissected fungal communities in a hemiboreal, herb-rich spruce forest. They observed that the abundance of arbuscular mycorrhizal fungi was higher in early than in mid-growing season and correlated positively with soil nitrogen and negatively with soil phosphorus content. In a study conducted in a temperate oak forest, seasonal dynamics were documented in the fungal communities, particularly in the litter horizon, where ECM fungi dominated in summer and SAP fungi were more abundant in autumn (Vořı́šková et al. 2014). These community changes likely have also fundamental functional consequences with corroborating alterations in nutrient cycling. The seasonal community shifts from early or late growing season saprotroph dominance to mid-growing season symbiont dominance seems a general pattern. For example, in Quercus spp. stands in midwestern USA, saprotrophic and putative rootassociated antagonists were more abundant in spring, whereas ECM fungi dominated the communities later in the summer (Jumpponen et al. 2010). Mundra et al. (2015) followed Bistorta vivipara -associated ECM communities in the high Arctic over 2 years. In that study, the ECM community composition and diversity were distinct between winter and growing season. Similarly, Zhang et al. (2014) observed a clear change in the microbial community composition and function between winter and summer in snow-covered temperate ecosystems. We aimed to investigate the vertical and seasonal dynamics of soil fungal communities in a southern boreal Scots pine forest using 454 pyrosequencing of the internal transcribed spacer 2 (ITS2) region. There are no previous, simultaneous studies on responsiveness of vertical community of soil fungi as a function of seasonal changes in boreal forests. To address this, we collected soil samples from three plots within a stand and divided them to five vertical horizons, i.e., raw litter (O/L), fermented litter (O/F), humus (O/H) and E- and B-mineral horizons to assess vertical heterogeneity of the fungal communities. We sampled these horizons monthly from March (late winter) to October (late fall) to also analyze seasonal changes of the communities. We hypothesized that the fungal community composition would differ between winter and the active growing season and that the ECM dominance in the fungal community would peak in the summer. We also hypothesized that the fungal diversity would decrease with increasing soil depth and that the O/L-horizon would have a fungal community most distinct from other soil horizons. MATERIALS AND METHODS Study site and sampling The study site is located in Hyytiälä, South-Eastern Finland (61◦ 51 N, 24◦ 17 E) in the vicinity of the Forestry field statio (...truncated)