Could microbes be the architects of improved soil structure under Miscanthus x giganteus?
The perennial grass Miscanthus x giganteus (miscanthus) offers a sustainable alternative to traditional biomass feedstocks while improving key soil health parameters, including aggregation. Aggregate stability results from dynamic soil-plant-microbe interactions, yet the relative importance of each factor remains an active research question. Building on previous observations that miscanthus alters soil structure to improve water-holding capacity and aggregate stability, we characterized the communities of soil bacteria and arbuscular mycorrhizal fungi (AMF) across three sites in Iowa, USA, comparing miscanthus to annual maize (Zea mays L.) and non-cropped perennial turfgrass (Poa spp.). We examined whether microbiomes co-varied with soil aggregation and, if so, whether plant cover identity or life history categorization better explained the observed patterns. Bacterial and AMF communities varied across sites and plant types, with signals that life history and plant cover identity both mattered. Aggregate stability aligned with a perennial-annual divergence in microbial beta diversity, while finer-scale differences in community composition and network structure were plant-specific. Soils under perennial plants were enriched in microbial groups positively correlated with aggregate stability; we identified 61 bacterial and 8 AMF "architect" taxa for future study. Within- and cross-kingdom co-occurrence network analysis revealed greater complexity under perennial plants: 1.9-fold more network links in miscanthus bacteria-bacteria networks than in maize, and 1.7-fold more in turfgrass AMF-AMF networks. Miscanthus fundamentally shapes microbial interactions, particularly among bacteria, relating to improved soil physical structure. Understanding these soil-plant-microbe feedbacks advances the development of biomass feedstocks with a portfolio of soil health benefits for next-generation biofuels and bioproducts. IMPORTANCEPerennial bioenergy crops can provide the raw material for biofuels and bioproducts while simultaneously improving soil health. Miscanthus x giganteus (miscanthus) efficiently stabilizes soil aggregates, potentially leading to higher water retention and erosion resistance. Understanding the microbial contributions to these outcomes is key to building resilient, sustainable bioenergy systems. This study highlights the connections between communities of soil microbes--bacteria and arbuscular mycorrhizal fungi--across three sites and three plant covers, including miscanthus, maize, and turfgrass. We identify a guild of potential "microbial architects" linked to soil aggregation and show more interconnected microbial networks under the perennial plant covers compared to annual maize. These insights shed light on the interactions between soil biological communities and soil physical and chemical properties. More broadly, the results may inform efforts to harness plant-associated microbiomes for sustainable biomass production.