Horizontal acquisition of nicotine catabolism gene cluster drives the assembly of tobacco root microbiota community

Abstract

BackgroundPlant roots are hotspots for interactions with soil microbes, where a characteristic bacterial community structure is formed. Plant specialized metabolites often play pivotal roles in this assembly process. However, the molecular basis underlying root microbiota responses to these bioactive compounds, and how such metabolic interactions shape the assembly of host-specific root microbiota, remain largely unknown. Nicotine is a toxic alkaloid predominantly produced by the genus Nicotiana, and the genus Arthrobacter is known as one of the nicotine-degrading bacteria in the tobacco root microbiota. In this study, we used the tobacco-Arthrobacter interaction system as a model and integrated comparative genomics and experimental genetic manipulation assays to uncover the role of bacterial catabolism capacity for host specialized metabolites in shaping host-specific root microbiota. ResultsNicotine catabolism genes are uniquely found in the Arthrobacter strains derived from nicotine-containing environments, and this restricted gene distribution is driven by a plasmid-mediated horizontal gene transfer. To assess the ecological consequences of this genomic adaptation in Arthrobacter fitness in tobacco roots, we conducted adaptation assays under both in vitro and in planta conditions using genetically manipulated Arthrobacter and tobacco mutants, which are impaired in nicotine catabolism and biosynthesis, respectively. Nicotine improves Arthrobacter colonization to the tobacco roots through both catabolism-dependent and catabolism-independent mechanisms. Bacterial community analysis using a synthetic community approach further demonstrated that these metabolic interactions, mediated by tobacco nicotine biosynthesis and its catabolism by Arthrobacter, jointly affect root microbiota composition. ConclusionsOur findings illustrated that bacterial catabolic capacity toward host-derived plant specialized metabolites is key for successful root colonization. This metabolic adaptation is driven by plasmid-mediated horizontal gene transfer and ultimately shapes the structure of the overall root microbiota community.