Top‐down control of soil fungal community composition by a globally distributed keystone consumer

Abstract

The relative contribution of top-down and bottom-up processes regulating primary decomposers can influence the strength of the link between the soil animal community and ecosystem functioning. Although soil bacterial communities are regulated by bottom-up and top-down processes, the latter are considered to be less important in structuring the diversity and functioning of fungal-dominated ecosystems. Despite the huge diversity of mycophagous (fungal-feeding) soil fauna, and their potential to reverse the outcomes of competitive fungal interactions, top-down grazing effects have never been found to translate to community-level changes. We constructed soil mesocosms to investigate the potential of isopods grazing on cord-forming basidiomycete fungi to influence the community composition and functioning of a complex woodland soil microbial community. Using metagenomic sequencing we provide conclusive evidence of direct top-down control at the community scale in fungal-dominated woodland soil. By suppressing the dominant cord-forming basidiomycete fungi, isopods prevented the competitive exclusion of surrounding litter fungi, increasing diversity in a community containing several hundred fungal species. This isopod-induced modification of community composition drove a shift in the soil enzyme profile, and led to a restructuring of the wider mycophagous invertebrate community. We highlight characteristics of different soil ecosystems that will give rise to such top-down control. Given the ubiquity of isopods and basidiomycete fungi in temperate and boreal woodland ecosystems, such top-down community control could be of widespread significance for global carbon and nutrient cycling.

Biotic interactions mediate soil microbial feedbacks to climate change

“…1 and 2). As observed in laboratory-based studies (20), the selective grazing of fungal cords also reduced total hydrolytic enzyme production (F 1,48 = 4.28, P = 0.04) and fungal-mediated wood decomposition rates (F 1,16 = 5.21, P = 0.036) (Fig. 3).…”

“…Given the regulatory effects of isopods observed under simplified laboratory conditions (20,27), we expected the top-down process to limit fungal biomass across all abiotic scenarios. However, the present study highlights that regulatory effects of grazers are apparent only above the ambient range of soil inorganic nitrogen concentrations (0-20 μg/g soil).…”

“…Increasing availability of fungi, with relatively low carbon:nitrogen ratios, is likely to drive a switch in isopod feeding, from leaf litter to fungal cords. A switch in feeding is likely to have direct functional consequences for the turnover rates of organic material in soil: The grazing and shredding of leaf litter increases microbial activity and decomposition rates (28,31,32), whereas the direct grazing of fungal cords generally limits enzyme activity and decomposition in forest soil (7,20,27). Such a functional switch would reinforce the capacity of soil invertebrates to limit microbial responses to global change as nitrogen enrichment converts their feeding habits from litter consumption (stimulating decomposition) into fungal grazing (limiting decomposition).…”

“…Indeed, the exclusion of other common macroinvertebrates, such as diplopods, from experimental chambers means that the invertebrate treatments plots are likely to underrepresent the potential for grazers to regulate the fungal community response to global change (34). However, the unique capacity of isopods to sever and ingest thick fungal cords makes this interaction a particularly strong one within forest soil (20). The selective removal of fungal cords by isopods has the capacity to govern the outcomes of fungal interactions (33) and prevent the competitive exclusion of microscopic fungi (including Ascomycota and Zycomycota), thus maintaining microbial diversity as well as biomass in European forest soils (20).…”

“…In belowground systems, the grazing of fungal mycelia by soil invertebrates is an analogous trophic interaction, but the functional consequences of this process are poorly understood. Contemporary food web theory asserts that the complexity of the detrital food web will dampen the effects of any top-down interactions in soil, relative to aboveground systems (19), but laboratory-based studies suggest that the selective removal of dominant microbial groups by large invertebrates (isopods in particular) can be an important regulatory force (20). Indeed, simplified (two-species) model systems highlight the potential for interactive effects of warming and invertebrate grazing on fungal cord growth (7,9), but it remains unclear whether these effects are relevant within natural, complex soil food webs.…”