Defining composition and function of the rhizosphere microbiota of barley genotypes exposed to growth-limiting nitrogen supplies

Abstract

BackgroundSince 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 in response to, nitrogen (N) application in soil and we assessed the impact of microbiota composition on plant growth.MethodsWe grew two wild (H. vulgaressp.spontaneum) and a modern domesticated (H. vulgaressp.vulgare) barley genotypes in an agricultural soil amended with and without nitrogen (N) inputs. By using a two-pronged 16S rRNA gene survey and a shotgun metagenomics approach, we determined the impact of N application on the taxonomic composition of the barley microbiota as well as the functional diversification of microbial communities exposed to limiting nitrogen supplies. In parallel, we used metagenomics reads to reconstruct genomes of individual bacterial members of the microbiota. Finally, we implemented a plant-soil feedback experiment to assess the microbiota’s contribution to plant growth.ResultsRhizosphere profiles were distinct from unplanted soil controls and displayed a significant, plant-mediated, N application-dependent taxonomic diversification which is maximised under N-limiting conditions. Strikingly, this diversification mirrors a metabolic specialisation of the barley microbiota, with functions implicated in nitrogen and sulphur metabolism enriched in a wild genotype as opposed to the RNA and cell capsule metabolisms enriched in a modern genotype. We reconstruct 28 high-quality individual bacterial genomes with a bias for Bacteroidetes and Proteobacteria, which are among the taxa differentially recruited between wild and modern genotypes. A plant-soil feedback experiment revealed that modern plants exposed to heat-sterilised soils grew less compared to plants maintained in untreated soils, although this difference was significant only for plants exposed to the wild barley microbiota.ConclusionsOur results point at nitrogen availability as a modulator of the structural and functional configuration of the rhizosphere bacterial communities and suggest a limited, but significant, contribution of the wild barley microbiota to plant growth. This knowledge will contribute to devise strategies to enhance sustainable crop production.

Applications of the indole-alkaloid gramine modulate the assembly of individual members of the barley rhizosphere microbiota

“…Yet, a recent study conducted on maize demonstrated that Proteobacteria, specifically members of the family Oxalobacteraceae, promote lateral root density and shoot dry weight (proxies for plant growth) under nitrogen limiting conditions ( Yu et al, 2021 ). As the soil tested in our experiments is limited in the availability of nitrogen for barley growth ( Terrazas et al, 2019 ) and considering the enrichment of putative ammonia oxidizers archaea in the rhizosphere of treated plants (see above), it can be speculated that the differential Proteobacterial enrichment triggered by gramine application may be linked to nitrogen turnover in the rhizosphere. An additional observation derived from these experiments is that gramine application triggers a differential microbial recruitment in the two tested genotypes.…”

“…Sequencing reads were processed using a customized bioinformatics pipeline as described before ( Terrazas et al, 2019 ). Briefly, sequencing reads were subjected to quality assessment using FastQC ( Andrews, 2010 ).…”

Applications of the indole-alkaloid gramine modulate the assembly of individual members of the barley rhizosphere microbiota

“…An alternative, not mutually exclusive scenario, is a differential rate of gramine degradation in the rhizosphere (Ghini, Burton & Gros, 1991) of the two genotypes as this would alter the bioavailability of this compound to the resident members of the microbiota. Regardless of the scenario, it is interesting to note that gramine applications failed to trigger a sustained enrichment of members of the Actinobacteria, which can be considered as a hallmark of elite, gramine-free, barley genotypes grown in the same soil type (Alegria Terrazas et al, 2020) and in other modern/ancestral plant pairs (Pérez-Jaramillo et al, 2018).…”

“…Sequencing reads were processed using a customized bioinformatics pipeline as described before (Terrazas et al, 2019). Briefly, sequencing reads were subjected to quality assessment using FastQC (Andrews et al, 2015).…”

Nitrogen Fertilisers Shape the Composition and Predicted Functions of the Microbiota of Field-Grown Tomato Plants

“…For instance, experimental data indicate that abundance of phytoavailable nitrogen, i.e., the scenario of mineral fertiliser treatments, tend to repress the proliferation and activity of members of the microbiota (Ramirez et al, 2012; Terrazas et al, 2019), and this in turn may be reflected in the metabolism of secondary compounds (terpenoid and polyketide metabolism) and membrane transport (ABC transporters).…”