Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches

Soil bacteria and fungi are known to form niche-specific communities that differ between actively growing and decaying roots. Yet almost nothing is known about the cross-kingdom interactions that frame these communities and the environmental filtering that defines these potentially friendly or competing neighbors. We explored the temporal and spatial patterns of soil fungal (mycorrhizal and nonmycorrhizal) and bacterial cooccurrence near roots of wild oat grass, Avena fatua, growing in its naturalized soil in a greenhouse experiment. Amplicon sequences of the fungal internal transcribed spacer (ITS) and bacterial 16S rRNA genes from rhizosphere and bulk soils collected at multiple plant growth stages were used to construct covariation-based networks as a step toward identifying fungal-bacterial associations. Corresponding stable-isotope-enabled metagenome-assembled genomes (MAGs) of bacteria identified in cooccurrence networks were used to inform potential mechanisms underlying the observed links. Bacterial-fungal networks were significantly different in rhizosphere versus bulk soils and between arbuscular mycorrhizal fungi (AMF) and nonmycorrhizal fungi. Over 12 weeks of plant growth, nonmycorrhizal fungi formed increasingly complex networks with bacteria in rhizosphere soils, while AMF more frequently formed networks with bacteria in bulk soils. Analysis of network-associated bacterial MAGs suggests that some of the fungal-bacterial links that we identified are potential indicators of bacterial breakdown and consumption of fungal biomass, while others intimate shared ecological niches. IMPORTANCE Soils near living and decomposing roots form distinct niches that promote microorganisms with distinctive environmental preferences and interactions. Yet few studies have assessed the community-level cooccurrence of bacteria and fungi in these soil niches as plant roots grow and senesce. With plant growth, we observed increasingly complex cooccurrence networks between nonmycorrhizal fungi and bacteria in the rhizosphere, while mycorrhizal fungal (AMF) and bacterial cooccurrence was more pronounced in soil further from roots, in the presence of decaying root litter. This rarely documented phenomenon suggests niche sharing of nonmycorrhizal fungi and bacteria, versus niche partitioning between AMF and bacteria; both patterns are likely driven by C substrate availability and quality. Although the implications of species cooccurrence are fiercely debated, MAGs matching the bacterial nodes in our networks possess the functional potential to interact with the fungi that they are linked to, suggesting an ecological significance of fungal-bacterial cooccurrence patterns.

Automated summary

Soil bacteria and fungi form niche-specific communities near roots, with nonmycorrhizal fungi showing increasingly complex networks with bacteria in rhizosphere soils, while arbuscular mycorrhizal fungi (AMF) more often form networks with bacteria in bulk soils. This suggests niche sharing between nonmycorrhizal fungi and bacteria, versus niche partitioning between AMF and bacteria, likely driven by C substrate availability and quality. MAGs matching the bacterial nodes possess functional potential to interact with linked fungi, suggesting ecological significance of fungal-bacterial cooccurrence.