Rhizosphere fungal community assembly varied across functional guilds in a temperate forest

Abstract

Background Rhizosphere fungi play an important role in plant community dynamics and biogeochemical cycling. While the drivers of fungal community assembly have been studied in varied ecosystems, it is still unclear how these processes function for rhizosphere soil fungi in temperate forests. Furthermore, it is unknown whether the relative contributions of important determinants remain consistent or vary across fungal ecological guilds. This study used high-throughput next-generation sequencing to characterize the fungal communities of 247 rhizosphere soil samples from 19 tree species in a temperate forest within Northeast China. We aimed to investigate how three important determinants in temperate forests (host tree species, neighbouring plant communities, and edaphic properties) influence the community assembly of fungal functional guilds in the rhizosphere soil of trees. Results We found that host tree species contributed more to plant pathogens’ community composition than ectomycorrhizal fungi, and plant pathogens consistently showed higher host specialization than ectomycorrhizal fungi. Saprotrophs also showed high host specialization, which was mediated by the tree species’ effect on rhizosphere soil pH. Although neighboring plant communities contributed remarkably to richness of all fungal guilds, this effect on fungal composition varied across functional guilds, with stronger effect for biotrophic guilds (plant pathogens and ectomycorrhizal fungi) than for non-biotrophic guild (saprotrophs). Neighboring plant communities shaped the ectomycorrhizal community composition strongly in all samples regardless of host trees’ mycorrhizal type, whereas edaphic properties were the most important drivers for this guild in samples from only ectomycorrhizal-associated trees. Edaphic properties played an important role in shaping ectomycorrhizal and saprotrophic fungal compositions, indicating the importance of edaphic properties on the fungal functional guilds associated with the absorption and decomposition of nutrients. Conclusions These results demonstrated that rhizosphere soil fungal community assembly determinants varied across fungal guilds, reflecting their different ecological functions in temperate forest ecosystems.

The spatial patterns of community composition, their environmental drivers and their spatial scale dependence vary markedly between fungal ecological guilds

“…Namely, strong spatial structure captured at the shortest spatial distances was present in ECM fungi and saprotrophs but not in yeasts; therefore, it likely captured the mycelial growth of the large, filamentous fungal species, which have been demonstrated to grow up to several metres long (Cairney, 2005). The vegetation effect observed at intermediate scales in our study corresponds with the results of other studies conducted at similar scales, where vegetation has been shown to affect fungal communities (Bahram et al., 2013; Liang et al., 2023; Odriozola et al., 2020, 2021; Peay et al., 2013; Tedersoo et al., 2020; Urbanová et al., 2015). In contrast to our hypothesis, the distribution of ECM fungi did not show stronger coupling with vegetation than the distribution of saprotrophs and yeasts.…”

“…For instance, Liang et al. (2023) reported strong vegetation effects on ECM fungal composition when analysing samples dominated by host trees with mixed mycorrhizal types, but soil variables were the main predictors when analysing only the samples dominated by ECM‐associated trees. All samples in our study were dominated by ECM‐associated trees, which might have contributed to the weaker vegetation effects on ECM fungi.…”

“…In contrast, yeasts are unicellular organisms that share several ecological characteristics with bacteria (Mašínová et al., 2017). These physiological differences between guilds presumably lead to differences in their dispersal capacity and their responses to environmental conditions, which, in turn, lead to different spatial patterns and drivers of community composition (Liang et al., 2023; Odriozola et al., 2020, 2021; Peguero et al., 2021; Soininen et al., 2007; Zinger et al., 2019). Several studies have demonstrated that ECM fungi may show biogeographic patterns similar to those of macroorganisms (Bahram et al., 2012; Peay et al., 2007, 2012), and their geographic distributions can be limited by dispersal (Bahram et al., 2013; Talbot et al., 2014).…”

“…Correspondingly, a recent study has shown that the temporal turnover of ECM fungal communities in forest soil is highly stochastic and site‐specific, whereas the temporal turnover of yeasts over different sites has more systematic patterns, more similar to those of soil bacteria than of other fungal guilds (Martinović et al., 2021). Last, many studies have shown strong covariation between the spatial distribution of ECM fungi and plant community composition, which has been attributed to their plant‐associated lifestyle (Bahram et al., 2013; Liang et al., 2023; Odriozola et al., 2020; Peay et al., 2013; van der Linde et al., 2018). Yet, yeasts and saprotrophs sometimes also show associations with tree identity and plant community composition, even though they are free‐living organisms not directly dependent on the association with a host plant (Mašínová et al., 2017; Odriozola et al., 2021; Urbanová et al., 2015).…”

Responses of Soil Fungi to Long‐Term Nitrogen‐Water Interactions Depend on Fungal Guilds in a Mixed Pinus koraiensis Forest

“…Furthermore, we found that fine‐root diameter, fine‐root nitrogen and phosphorus concentration, and RTD variously regulated the community structure of soil patho‐, sapro‐ and symbiotrophic fungi, supporting our third hypothesis. Generally, soil patho‐ and symbiotrophic fungi are part of the biotrophic guilds that depend on living plants to survive, while soil saprotrophicic fungi are non‐biotrophic, meaning they acquire all their nutrients from non‐living plant material or surrounding soil organic matter (Liang et al., 2023). Due to their ecological and functional dissimilarities, these fungal guild communities of biotrophic and non‐biotrophic guilds might be shaped by different determinants associating soil and plant traits (Nguyen, Williams, et al., 2016; T. Yang et al., 2019).…”