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Abstract

Many bacteria can communicate with each other, coordinating and synchronizing their behaviour by means of production and sensing of extracellular signal molecules called autoinducers. Most autoinducers modulate intraspecies communication, but autoinducer 2 (AI-2) functions as a universal quorum sensing signal that enables interspecies communication. In this work, we show novel roles of AI-2 in intra- and interspecies interactions of E. coli. We demonstrate that motility and chemotaxis play a crucial role in the collective behaviour – autoaggregation – of E. coli. This provides the first physiologically relevant example of collective behaviour in bacteria being driven by chemotaxis to a self-produced attractant. Equally important is our finding that this self-attraction is mediated by the quorum-sensing signal AI-2. AI-2 is produced by a large number of bacteria including E. coli, but significance of AI-2-mediated signalling remains poorly understood. Using comprehensive whole-population and single-cell analysis, we have conclusively shown that AI-2 import and metabolism represent the only AI-2 uptake-dependent phenotype in E. coli. Nevertheless, our work shows that, by promoting aggregative behaviour via chemotaxis, AI-2 plays a true signalling function in E. coli. Such AI-2-mediated autoaggregation promotes not only bacterial stress resistance but also formation of surface-attached biofilms. Our work thus establishes direct connection between these two forms of bacterial collective behaviour that are normally treated separately. We also demonstrate that autoaggregation behaviour and biofilm formation by E. coli are enhanced in presence of Enterococcus faecalis that naturally co-occurs with E. coli in mammalian gut. We further show that this enhancement is due to the interspecies signalling that is mediated by AI-2, which enables E. coli to maintain activity of its quorum sensing system and promotes its chemotaxis-dependent aggregation at lower cell densities. Formation of such mixed dual-species biofilms increases stress resistance of both E. coli and E. faecalis.