Rodrigo Alegria Terrazas
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Senga Robertson-Albertyn
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Aileen Mary Corral
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Carmen Escudero-Martinez
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Katharin Balbirnie-Cumming
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AbstractBackgroundSince the dawn of agriculture, human selection on plants has progressively differentiated input-demanding productive crops from their wild progenitors thriving in marginal areas. Barley (Hordeum vulgare), the fourth most cultivated cereal globally, is a prime example of this process. We previously demonstrated that wild and domesticated barley genotypes host distinct microbial communities in their rhizosphere. Here, we tested the hypothesis that microbiota diversification is modulated by, and responds to, nitrogen (N) application in soil and assessed the impact of microbiota taxonomic and functional compositions on plant growth.MethodsWe grew two wild (H. vulgare ssp. spontaneum) and an ‘Elite’ domesticated (H. vulgare ssp. vulgare) barley genotypes in an agricultural soil treated with and without N inputs. By using a two-pronged 16S rRNA gene amplicon sequencing and comparative metagenomics approach, we determined the impact of N application on taxonomic composition and metabolic potential of the microbial communities exposed to limiting and replete N supplies. We then implemented a plant-soil feedback experiment to assess microbiotas’ recruitment cues and contribution to plant growth.ResultsN availability emerged as a modulator of the recruitment cues of the barley bacterial microbiota as evidenced by the increased number of bacterial genera differentially recruited between unplanted soil and rhizosphere communities under N-limiting conditions. This recruitment pattern mirrored the impact of the host genotype on rhizosphere bacteria. The characterisation of the assembled metagenomes of plants exposed to N-limiting conditions revealed a metabolic specialisation of the rhizosphere microbiota compared to unplanted soil controls. This specialisation is underpinned predominantly by bacteria and is manifested by the enrichment of a core set of biological processes sustaining the adaptation of polymicrobial communities such as N utilisation, quorum sensing and motility across genotypes. The quantitative variation in a group of these biological processes defined host signatures in the barley rhizosphere metagenome. Finally, a plant-soil feedback experiment revealed that the host-mediated taxonomic diversification of the bacterial microbiota is associated with barley growth under sub-optimal N supplies.ConclusionsOur results suggest that under N limiting conditions, a substrate-driven selection process underpins the assembly of barley rhizosphere microbiota. Host-microbe and microbe-microbe interactions fine-tune this process at the taxonomic and functional level across kingdoms. The disruption of these recruitment cues negatively impacts plant growth.
An Affinity–Effect Relationship for Microbial Communities in Plant–Soil Feedback Loops
