Trade or scavenge? Miscanthus-microbiome interactions depend upon soil fertility

Miscanthus x giganteus (Miscanthus) is a robust bioenergy crop, able to withstand the poor soil fertility found on marginal lands (e.g., anthropogenically disturbed lands). Mounting evidence suggests that this robustness is related to the ability of Miscanthus to partner with soil microorganisms to gain nutrients. Of particular interest is how Miscanthus may alter microbially-mediated nitrogen (N) cycling (e.g., N-fixation and mineralization) resulting in efficient N acquisition across a range of soil fertility levels. However, a mechanistic understanding of how Miscanthus responds to and influences soil nitrogen cycling under the variable soil properties that emerge from land disturbance is lacking. Further, it remains unclear whether these plant-growth promoting microbial functions can be bolstered by directly managing microbial community composition (i.e., biofertilization). To address these knowledge gaps, we performed a greenhouse experiment with Miscanthus grown in soil from two sites with different soil fertility levels (e.g., differences in soil texture, inorganic nitrogen, and C/N). We also tested the effect of two biofertilizers (commercially available biofertilizer or a soil transplant from a mature Miscanthus stand) on Miscanthus growth or plant-microbe interactions. We surveyed microbial community composition via community-based amplicon sequencing and quantified function by measuring the activity of prokaryotic N-fixers and nitrifiers. Initial soil fertility outweighed biofertilization in determining microbial community composition and function. Specifically, when Miscanthus was grown in low fertility soil from a highly disturbed site, rates of N fixation by free-living N-fixers increased. This increase was accompanied by increases in arbuscular mycorrhizal fungi (AMF) abundance suggesting a synergism between N fixation rates and AMF that facilitates plant nitrogen acquisition. These effects of Miscanthus on the soil microbiome composition and function were less pronounced in the high fertility soil with more nitrogen. This suggests a scenario where, under nitrogen limitation, Miscanthus trades with symbionts providing carbon to nitrogen fixing bacteria and AMF to acquire nitrogen. Alternatively, when nitrogen is more plentiful, Miscanthus may scavenge nutrients, obtaining nitrogen released from organic matter by saprotrophs. These observations aid in illuminating how Miscanthus can dynamically shape microbial functions occurring in its rhizosphere which more broadly increases our understanding of plant-microbe interactions and bioenergy agroecosystems.