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ABSTRACTThe ecological impacts of long-term (press) disturbance on mechanisms regulating the relative abundance (i.e., commonness or rarity) and temporal dynamics of species within a community remain largely unknown. This is particularly true for the functionally important arbuscular mycorrhizal (AM) fungi; obligate plant-root endosymbionts that colonize more than two-thirds of terrestrial plant species. Here, we use high-resolution amplicon sequencing to examine how AM fungal communities in a specific extreme ecosystem—mofettes or natural CO2 springs caused by geological CO2 exhalations—are affected by long-term stress. We found that in mofettes, specific and temporally stable communities form as a subset of the local metacommunity. These communities are less diverse and dominated by adapted, “stress tolerant” taxa. Those taxa are rare in control locations and more benign environments worldwide, but show a stable temporal pattern in the extreme sites, consistently dominating the communities in grassland mofettes. This pattern of lower diversity and high dominance of specific taxa has been confirmed as relatively stable over several sampling years and is independently observed across multiple geographic locations (mofettes in different countries). This study implies that the response of soil microbial community composition to long-term stress is relatively predictable, which can also reflect the community response to other anthropogenic stressors (e.g., heavy metal pollution or land use change). Moreover, as AM fungi are functionally differentiated, with different taxa providing different benefits to host plants, changes in community structure in response to long-term environmental change have the potential to impact terrestrial plant communities and their productivity.IMPORTANCEArbuscular mycorrhizal (AM) fungi form symbiotic relationships with more than two-thirds of plant species. In return for using plant carbon as their sole energy source, AM fungi improve plant mineral supply, water balance, and protection against pathogens. This work demonstrates the importance of long-term experiments to understand the effects of long-term environmental change and long-term disturbance on terrestrial ecosystems. We demonstrated a consistent response of the AM fungal community to a long-term stress, with lower diversity and a less variable AM fungal community over time under stress conditions compared to the surrounding controls. We have also identified, for the first time, a suite of AM fungal taxa that are consistently observed across broad geographic scales in stressed and anthropogenically heavily influenced ecosystems. This is critical because global environmental change in terrestrial ecosystems requires an integrative approach that considers both above- and below-ground changes and examines patterns over a longer geographic and temporal scale, rather than just single sampling events.

ABSTRACT Fungi underpin almost all terrestrial ecosystem functions, yet our understanding of their community ecology lags far behind that of other organisms. Here, red paddy soils in subtropical China were collected across a soil depth profile, comprising 0-to-10-cm- (0-10cm-), 10-20cm-, and 20-40cm-deep layers. Using Illumina MiSeq amplicon sequencing of the internal transcribed spacer (ITS) region, distance-decay relationships (DDRs), and ecological models, fungal assemblages and their spatial patterns were investigated from each soil depth. We observed significant spatial variation in fungal communities and found that environmental heterogeneity decreased with soil depth, while spatial variation in fungal communities showed the opposite trend. DDRs occurred only in 0-10cm- and 10-20cm-deep soil layers, not in the 20-40cm layer. Our analyses revealed that the fungal community assembly in the 0-10cm layer was primarily governed by environmental filtering and a high dispersal rate, while in the deeper layer (20-40cm), it was primarily governed by dispersal limitation with minimal environmental filtering. Both environmental filtering and dispersal limitation controlled fungal community assembly in the 10-20cm layer, with dispersal limitation playing the major role. Results demonstrate the decreasing importance of environmental filtering and an increase in the importance of dispersal limitation in structuring fungal communities from shallower to deeper soils. Effectively, “everything is everywhere, but the environment selects,” although only in shallower soils that are easily accessible to dispersive fungal propagules. This work highlights that perceived drivers of fungal community assembly are dependent on sampling depth, suggesting that caution is required when interpreting diversity patterns from samples that integrate across depths. IMPORTANCE In this work, Illumina MiSeq amplicon sequencing of the ITS region was used to investigate the spatial variation and assembly mechanisms of fungal communities from different soil layers across paddy fields in subtropical China, and the results demonstrate the decreasing importance of environmental filtering and an increase in the importance of dispersal limitation in structuring fungal communities from shallower to deeper soils. Therefore, the results of this study highlight that perceived drivers of fungal community assembly are dependent on sampling depth and suggest that caution is required when interpreting diversity patterns from samples that integrate across depths. This is the first study focusing on assemblages of fungal communities in different soil layers on a relatively large scale, and we thus believe that this study is of great importance to researchers and readers in microbial ecology, especially in microbial biogeography, because the results can provide sampling guidance in future studies of microbial biogeography.