Abstract
Autoinducer-2 (AI-2) is unique among quorum-sensing signaling molecules, as it is produced and recognized by a wide variety of bacteria and thus facilitates interspecies communication. To date, two classes of AI-2 receptors have been identified: the LuxP-type, present in the Vibrionales, and the LsrB-type, found in a number of phylogenetically distinct bacterial families. Recently, AI-2 was shown to affect the colonization levels of a variety of bacteria in the microbiome of the mouse gut, including members of the genus Clostridium, but no AI-2 receptor had been identified in this genus. Here, we identify a noncanonical, functional LsrB-type receptor in Clostridium saccharobutylicum. This novel LsrB-like receptor is the first one reported with variations in the binding-site amino acid residues that interact with AI-2. The crystal structure of the C. saccharobutylicum receptor determined at 1.35 Å resolution revealed that it binds the same form of AI-2 as the other known LsrB-type receptors, and isothermal titration calorimetry (ITC) assays showed that binding of AI-2 occurs at a submicromolar concentration. Using phylogenetic analysis, we inferred that the newly identified noncanonical LsrB receptor shares a common ancestor with known LsrB receptors and that noncanonical receptors are present in bacteria from different phyla. This led us to identify putative AI-2 receptors in bacterial species in which no receptors were known, as in bacteria belonging to the Spirochaetes and Actinobacteria phyla. Thus, this work represents a significant step toward understanding how AI-2-mediated quorum sensing influences bacterial interactions in complex biological niches.
Highlights
Autoinducer-2 (AI-2) is unique among quorum-sensing signaling molecules, as it is produced and recognized by a wide variety of bacteria and facilitates interspecies communication
We proposed the following criteria to identify functional LsrB receptors: (i) more than 60% sequence identity with the LsrB from Salmonella serovar Typhimurium, (ii) conservation of all six binding-site amino acid residues that interact with AI-2, and (iii) co-occurrence with orthologs to the other key transport proteins encoded by the lsr operon
Proteins identified from C. saccharobutylicum and C. autoethanogenum shared a sequence identity with the LsrB from B. cereus of 39.2 and 37.9%, respectively (Table S2)
Summary
Autoinducer-2 (AI-2) is unique among quorum-sensing signaling molecules, as it is produced and recognized by a wide variety of bacteria and facilitates interspecies communication. We proposed the following criteria to identify functional LsrB receptors: (i) more than 60% sequence identity with the LsrB from Salmonella serovar Typhimurium, (ii) conservation of all six binding-site amino acid residues that interact with AI-2, and (iii) co-occurrence with orthologs to the other key transport proteins encoded by the lsr operon. The identification of AI-2 receptors in these species represents a key step in understanding the mechanisms by which AI-2 regulates the levels of Firmicutes in the mouse gut and, more broadly, how AI-2–mediated quorum sensing influences the behavior of this and other complex communities
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