Metabolism of hemicelluloses by root-associated Bacteroidota species

Abstract

Bacteroidota species are enriched in the plant microbiome and provide several beneficial functions for their host, including disease suppression. Determining the mechanisms that enable bacteroidota to colonise plant roots may therefore provide opportunities for enhancing crop production through microbiome engineering. By focusing on nutrient acquisition mechanisms, we discovered Bacteroidota species lack high affinity ATP-binding cassette transporters common in other plant bacteria for capturing simple carbon exudates. Instead, bacteroidota possess TonB-dependent transporters predicted to import glycans produced by plant polysaccharide breakdown. Metatranscriptomics (oat rhizosphere) identified several TonB-dependent transporters genes that were highly expressed in Flavobacterium (phylum Bacteroidota). Using Flavobacterium johnsoniae as the model, we experimentally validated the function of one highly expressed TonB-dependent transporters, identifying a conserved Xyloglucan Utilisation Loci conferring an ability to import xyloglucan, the major hemicellulose secreted from plant roots. Xyloglucan utilisation loci harbour an endoxyloglucanase related to family 5 subfamily 4 subclade 2D glycoside hydrolases carrying a mutation that we demonstrate is required for full activity towards xyloglucan. Based on analysing 700 soil metagenomes, subclade 2D glycoside hydrolases have radiated in soil and are prevalent among plant-associated bacteroidota and certain taxa affiliated with Gammaproteobacteria. In bacteroidota, particularly Flavobacterium species, xyloglucan utilisation loci organisation was highly conserved, which may increase their competitive ability to utilise xyloglucan. Given bacteroidota lack high-affinity nutrient transporters for simple carbon, instead possessing xyloglucan utilisation loci and similar gene clusters, our data suggests hemicellulose exudates provide them with an important carbon source in the rhizosphere.