Plant miRNAs influence soil bacterial growth and amino acid uptake, restructuring community composition

Plants and microbes use many strategies to acquire soil amino acids. Recent findings suggest that genes related to amino acid metabolism and transport are influenced by plant miRNAs. Here, we first show that Arabidopsis modifies its root miRNA content when fertilized with a mixture of 17 amino acids. The miRNAs that responded to amino acid fertilization and other rhizosphere-abundant miRNAs were applied to a simplified soil community, grown with diverse amino acid sources, to test if they interfered with microbial community growth, community composition, and amino acid consumption. Plant miRNAs affected the community's growth in over 70% of the amino acid sources. The impact of plant miRNAs also depended on the N source supplied to the microbial community, with the strongest effect observed with L-lysine. Specifically, ath-miR159a reduced the microbial consumption of L-lysine, further supporting that plant miRNAs can influence microbial amino acid uptake. Plant miRNAs also strongly affected the relative abundance of specific bacterial taxa, which we subsequently isolated. These community shifts were explained by the subtle but robust impact of plant miRNAs on isolates' growth and, for two out of three isolates, on amino acid consumption. Surprisingly, while plant miRNAs inhibited amino acid consumption at both the community and isolate levels, the effects of plant miRNAs were mostly positive. Our results suggest that rhizospheric plant miRNAs might have a role in modulating the amino acid consumption of soil bacteria which reshapes the community, but not necessarily in a competitive framework.