Prevalence and Specificity of Chemoreceptor Profiles in Plant-Associated Bacteria

Chemosensory pathways are among the most abundant prokaryotic signal transduction systems, allowing bacteria to sense and respond to environmental stimuli. Signaling is typically initiated by the binding of specific molecules to the ligand binding domain (LBD) of chemoreceptor proteins (CRs). Although CRs play a central role in plant-microbiome interactions such as colonization and infection, little is known about their phylogenetic and ecological specificity. Here, we analyzed 82,277 CR sequences from 11,806 representative microbial species covering the whole prokaryotic phylogeny, and we classified them according to their LBD type using a de novo homology clustering method. Through phylogenomic analysis, we identified hundreds of LBDs that are found predominantly in plant-associated bacteria, including several LBDs specific to phytopathogens and plant symbionts. Functional annotation of our catalogue showed that many of the LBD clusters identified might constitute unknown types of LBDs. Moreover, we found that the taxonomic distribution of most LBD types that are specific to plant-associated bacteria is only partially explained by phylogeny, suggesting that lifestyle and niche adaptation are important factors in their selection. Finally, our results show that the profile of LBD types in a given genome is related to the lifestyle specialization, with plant symbionts and phytopathogens showing the highest number of niche-specific LBDs. The LBD catalogue and information on how to profile novel genomes are available at https://github.com/compgenomicslab/CRs. IMPORTANCE Considering the enormous variety of LBDs at sensor proteins, an important question resides in establishing the forces that have driven their evolution and selection. We present here the first clear demonstration that environmental factors play an important role in the selection and evolution of LBDs. We were able to demonstrate the existence of LBD families that are highly enriched in plant-associated bacteria but show a wide phylogenetic spread. These findings offer a number of research opportunities in the field of single transduction, such as the exploration of similar relationships in chemoreceptors of bacteria with a different lifestyle, like those inhabiting or infecting the human intestine. Similarly, our results raise the question whether similar LBD types might be shared by members of different sensor protein families. Lastly, we provide a comprehensive catalogue of CRs classified by their LBD region that includes a large number of putative new LBD types.