Predictors of soil fungal biomass and community composition in temperate mountainous forests in Central Europe
Graphical abstract
Introduction
Fungi comprise a highly diverse group of soil organisms with diverse ecologies and important involvement in multiple ecosystem functions (Peay et al., 2016; Taylor et al., 2014). Biotrophic fungal groups like mycorrhizal root symbionts increase ecosystem productivity by providing nutrients to their host plants, while pathogens negatively affect their hosts in both natural and agricultural ecosystems. Due to the unique ability to decompose biopolymers, saprotrophic fungi are the most important decomposers of soil organic compounds (Baldrian, 2008; De Boer et al., 2005).
The role of fungi is specifically pronounced in temperate and boreal forest soils where high production of recalcitrant plant biomass contributes to C accumulation in the upper horizons of soil as well as on the soil in the form of plant litter. Fungi, as proficient decomposers and recyclers of this pool of organic matter, are especially fit for this environment and represent substantial fraction of the microbiome and its activity (Baldrian, 2017). Fungal communities in forest topsoil are vertically stratified, with litter exhibiting the highest biomass of fungi and a high share of saprotrophic taxa, while fungal biomass decreases and the share of mycorrhizal fungi increases with depth (Baldrian et al., 2012; Lindahl et al., 2007; O'Brien et al., 2005). This is a reflection of the high content of organic compounds in litter (Šnajdr et al., 2008) and its decreasing content and increasing recalcitrance with soil depth (Lindahl et al., 2007; Šnajdr et al., 2010; Sterkenburg et al., 2015). Plant roots and the rhizosphere represent unique environments, rich in plant-derived, easily accessible C, but depleted in other nutrients due to plant activity (Hinsinger et al., 2005). Plant symbiotic mycorrhizal fungi dominate these habitats (Buée et al., 2009), forming unique symbiotic structures such as the ectomycorrhizas on tree roots (van der Heijden et al., 2015).
Given the importance of fungi in forest ecosystems, the understanding of factors affecting their distribution is needed for the understanding of litter and soil ecology. In this line, microbial biogeography is receiving increased attention in recent years (Martiny et al., 2006) and global studies have shown that large-scale distributional patterns of fungi are primarily influenced by climate (Bahram et al., 2018; Tedersoo et al., 2014; Větrovský et al., 2019). Studies focusing on landscape and regional scales, less affected by climatic and historical dispersal limitation, are also starting to accumulate (Lindahl et al., 2007; Sterkenburg et al., 2015; Tedersoo et al., 2020); these studies show that both abiotic factors (i.e. soil chemistry) and biotic factors (i.e. plant composition and the characteristics of produced litter) play prominent roles in determining fungal species distributions (Bahnmann et al., 2018; Tedersoo et al., 2020; Urbanová et al., 2015).
Soil pH is a widely reported abiotic driver of fungal community composition (Bahnmann et al., 2018; Tedersoo et al., 2020; van der Linde et al., 2018) acting either directly or affecting the availability of soil nutrients (van der Linde et al., 2018). Soil N and P content also affects fungal communities, particularly when they are limiting (Almeida et al., 2019; Čapek et al., 2016; Lindahl et al., 2007; Sterkenburg et al., 2015; van der Linde et al., 2018). Dominant vegetation strongly affects fungal communities (Bahnmann et al., 2018; Odriozola et al., 2020; Peay et al., 2013; Tedersoo et al., 2020) through several routes including the production of leaf and root litter of specific chemical composition (Urbanová et al., 2015), and through association with tree-specific root symbionts (Prescott and Grayston, 2013), through the modification of soil chemistry (Šnajdr et al., 2013; Tedersoo et al., 2016) or microclimate alteration (Castaño et al., 2018). Due to direct effects, previous research has reported stronger effects of dominant vegetation on biotrophic fungal groups as compared to saprotrophs (Odriozola et al., 2020; Tedersoo et al., 2020).
The spatial distribution of microbial taxa is a function of the dispersal abilities and availability of suitable niche for establishment (Talbot et al., 2014). Fungal taxa widely differ with respect to both of these factors. The distributions of fungi forming large mycelial networks resembles that of plants and their dispersal also proceeds at comparable rates (Peay et al., 2010; Wolfe et al., 2010). However, the large phenotypic diversity of fungi is likely to be reflected in the drivers of their spatial distributions. For instance, the ecology and distribution of soil yeast-like fungi, mycorrhizal fungi depending on plant hosts and saprotrophs usually differs (Maksimova and Chernov, 2004; Odriozola et al., 2020; Tedersoo et al., 2020; Urbanová et al., 2015).
While the most important drivers of fungal community composition appear to be known, it is less clear how their relative importance differs ecological guilds of fungi (saprotrophs, mycorrhizal fungi, root endophytes etc.) and principal forest topsoil microhabitats (plant roots, soil and litter) that differ in nutrient content, organic matter quality and spatial heterogeneity (Baldrian, 2017). In fact, the available information is largely constrained to soil (Tedersoo et al, 2014, 2020) and mostly comes from experimental forests and monoculture stands that hardly reflect the natural variation of forest complexity. Last, but not least, the predictors of fungal standing biomass are much less known than those of the community composition. To fill these important gaps of knowledge, we have collected and analyzed a comprehensive dataset from a Central European temperate forests, covering a broad range of elevations and vegetation types, and spanning from managed forests to protected forests with minimal human intervention. In addition to variables related to site characteristics, soil and litter chemistry, we have performed detailed botanical surveys and belowground vegetation analysis using high throughput sequencing of molecular markers of plant roots. This study had the following specific objectives: i) to determine if there are significant differences between soil habitats, soil, roots and litter, in terms of fungal biomass, fungal species composition and ecological guild composition, i.e., relative abundance of saprotrophs, molds, yeasts, ECM, plant pathogens and endophytes; ii) to identify environmental predictors that explain variation in fungal biomass, fungal species composition and ecological guild composition within each habitat; iii) to assess the relative importance of different abiotic (soil variables, site characteristics) and biotic (vegetation and litter characteristics) predictors in explaining variance in fungal community composition within different habitats for whole fungal communities, as well as within fungal ecological guilds.
Similar to previous works we expected to find higher contents of nutrients (N, P) in litter compared to soil and, consequently, higher fungal biomass and abundance of saprotrophs, which depend on the availability of C within plant biopolymers. Accordingly, we expected to find lower fungal biomass and higher share of root-associated fungi in deeper soil. Previous research on boreal forests has shown that N is the main limiting factor affecting fungal biomass and community composition (Lindahl et al., 2007; Sterkenburg et al., 2015). Nevertheless, after decades of heavy atmospheric deposition (Kopáček et al., 1998), N is unlikely to be limiting in Central European forests. Thus, we hypothesized that N-limitation may have shifted to P-limitation in our study system and we expect P to be the main nutrient explaining variation in both fungal biomass and community composition. Lastly, we hypothesized that vegetation has stronger effects on mycorrhizal fungi and plant pathogens, whereas the effects of vegetation on saprotrophs are weaker and mainly mediated by litter chemistry. Consequently, the relative effect of vegetation was expected to be higher in roots and litter through direct interaction and specific chemistry features compared to soil where the nutrient content and site characteristics should play a major role. Since we surveyed ground vegetation with a so far unprecedented detail, we also expected to observe larger effects of vegetation on saprotrophs than previously reported when ground vegetation composition was not considered (Tedersoo et al., 2020). This is because ground vegetation substantially contributes to overall litter production and its litter often has specific chemical features (Štursová et al., 2020; Svoboda et al., 2006).
Section snippets
Sampling design
The study took place in the Bohemian Forest National Park in the Czech Republic, Central Europe (49°N, 13°E). The National Park protects the largest area of temperate mountainous forests in Central Europe ranging from managed to natural forests and covering wide gradients of altitude 690–1300 m a.s.l. and vegetation diversity (Table S1). The area has mean annual temperature between 3 °C and 5 °C and annual precipitation of 700–1600 mm depending on altitude. Picea abies (L.) H.Karst. is the most
Environmental properties
The sampling sites covered the whole area of the Bohemian Forest National Park and showed high diversity of environmental conditions, vegetation composition and management (Table S1). Out of the 58 sites, 35 were managed with removal of harvested wood, 9 were managed where harvested wood was left and 14 were unmanaged. Soil pH was generally acidic (3.48–5.16) as well as litter pH (3.60–5.28) and soil organic matter and C content were relatively high (14–97% and 5–47%, respectively). The content
Discussion
In our study, for the first time we explored the role of various environmental factors, such as substrate chemical characteristics, vegetation, space and topography, on fungal biomass and community composition of different fungal ecological guilds in three different topsoil habitats in a temperate forest, thus significantly contributing to the overall understanding of the complex mechanisms that determine forest mycobiome productivity and composition in the regional spatial scale.
Conclusions
The expected vertical stratification of fungal biomass and community composition was clearly observable in our study. Litter contained higher amounts of fungal biomass and was dominated by saprotrophic fungi, while soil contained less fungal biomass, was dominated by ECM fungi and was relatively depleted of free-living saprotrophs. Additionally, we show that vegetation is a key predictor of fungal community composition across ecological guilds and habitats, which may affect fungal groups
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by the Czech Science Foundation (18-26191S and 21-17749S) and by the Ministry of Education, Youth and Sports of the Czech Republic (LTC20073). The Šumava National Park Administration is acknowledged for the research permit. We acknowledge all members of the Laboratory of Environmental Microbiology who helped with fieldwork.
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these authors contributed equally.