Extreme environments simplify reassembly of communities of arbuscular mycorrhizal fungi

Abstract

ABSTRACT The 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 CO 2 springs caused by geological CO 2 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. IMPORTANCE Arbuscular 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.