Horizontal acquisition of nicotine catabolism gene cluster enhances Arthrobacter fitness within tobacco root microbiota - Microbiome

Background Plant 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. Results Nicotine 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 characterized the nicotine utilization ability of Arthrobacter and conducted adaptation assays under in planta conditions using genetically manipulated Arthrobacter strains and tobacco mutants impaired in nicotine catabolism and biosynthesis, respectively. Nicotine improves Arthrobacter colonization of tobacco roots through a catabolism-dependent mechanism. Bacterial community analysis using a synthetic community approach further demonstrated that this metabolic adaptation enhances Arthrobacter fitness within tobacco root microbiota. Conclusions Our 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 root microbiota community. Video Abstract

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