Decoding contact-dependent communication and coordination in bacteria

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The long-held notion of bacteria as “bags of enzymes” has undergone a paradigm shift in the past several years, with many eukaryotic traits now also identified in bacteria. One such trait is multicellularity (through differentiated cell fates), as exemplified by the Gram-negative social bacterium Myxococcus xanthus; upon starvation, swarms induce formation of spore-filled fruiting bodies by certain cells, exploration of the local environment by others, and programmed cell death by yet a third subpopulation to provide nutrients for cannibalistic feeding, all without conventional quorum sensing systems. Individual M. xanthus cells moving on hard surfaces leave behind slime polysaccharide trails, which can be followed by subsequent cells and swarms. Slime trails also contain outer-membrane vesicles/tubes left behind by previously-transited cells. However, the role of cell-surface factors in the discrimination of material from “self” vs. “non-self” sources has also never been characterized. As such, numerous questions remain as to how bacteria can communicate and coordinate their actions across an entire population simply through contact with self-generated signals and each other to effect multicellular behaviour. This research program aims to determine the mechanisms and roles of bacterial surface dynamics in the coordination of bacterial population behaviour. Specifically, we will examine the basis by which subsequent “chase” cells preferentially follow previously-deposited slime trails from “seed” cells, and whether or not the uptake of outer-membrane debris from kin cells in these trails affects this outcome. Complementarily, we will elucidate the process by which slime is produced as well as the chemical properties of the polysaccharide that contribute to its adhesiveness. As outer-membrane debris is prevalent in slime trails, we will also characterize the events responsible for this dynamic deposition of surface material, including the structural factors of the membrane itself that may predispose it to such phenomena. Finally, we will identify the surface-associated bacterial factors responsible for distinguishing kin cells from those that are not related. We will address these questions through the use of multidisciplinary and cutting-edge microfluidics, click chemistry, structural biology, and high-throughput screening techniques, yielding unprecedented insights into the mechanisms and roles of outer-membrane dynamics in bacteria. The long-term vision for this research program is to develop a comprehensive understanding of the interplay between bacterial components that are crucial for contact-mediated communication and fundamental behavioral coordination; this will revolutionize our understanding of bacterial survival and persistence in niches as diverse as soils and rivers, to the gastrointestinal tract and its associated microbiota.