Fungi are the primary decomposers of dead plant material (i.e., litter) in terrestrial environments, controlling a major flux of carbon (C) between the biosphere and atmosphere. While decomposer fungi exhibit predictable community succession patterns as litter decay progresses, the nature of species interactions within and among these communities remains unclear, as does the role, if any, of microbial interactions on decay processes that drive C flux from soils. We hypothesized that interspecies fungal interactions are species-specific and range from mutualistic to antagonistic, while interdomain interactions of fungi with co-occurring bacteria are largely negative for the fungi, potentially due to bacterial cheating. Furthermore, we hypothesized that fungal interactions stimulate decomposition, both through mutualistic cross-feeding and antagonistic oxidative attack. To test these hypotheses, we created laboratory microcosms with pairwise interactions of 10 fungal and 4 bacterial species identified in field litter-degrading communities. Microcosms were supplemented with fresh Arabidopsis thaliana litter to simulate early stage decay. We assessed interaction response through growth rate and effect on decomposition through extracellular enzyme activity and litter mass loss.
In contrast to our predictions, our primary finding was that fungal-bacterial interdomain interactions, rather than fungal-fungal interspecies interactions, control early stage plant litter decay, and that interdomain interactions hindered rather than stimulated the decay process. Interspecies fungal interactions were antagonistic or parasitic, but growth responses were minor, with little change in extracellular enzyme activity or litter mass loss. No mutualistic interactions were observed. In contrast, bacteria significantly decreased fungal growth and litter mass loss by aggressively surrounding the fungi, driving a shift in fungal resource allocation from C breakdown (hydrolase activity) to combat (oxidase activity). Moreover, interdomain interactions exhibited spatio-temporal dynamics in which (a) abrupt depression of fungal growth rate coincided with complete bacterial encirclement; (b) aggressive combat between bacteria and fungi was temporary, as fungi were generally able to rebound after warding off bacterial competitors. Our data suggest that spatial structure on solid litter substrates may be an important mechanism for the survival of decomposer fungi in natural litter-degrading communities. Restricting costly interdomain combat to the community periphery could allow fungi to sustain C decomposition activity during early stage decay. It remains unclear how these community dynamics may change as litter becomes more recalcitrant during later decay stages.