Social networks in the microbial world

Most natural environments harbour diverse communities of microbes. Within these complex communities, such as in the human gut microbiota, different species of bacteria can coexist. Thus, it is crucial that within bacterial populations the individuals communicate in order to regulate and coordinate their grouped behaviour. Amongst the different strategies, the most common is the use of quorum sensing. These systems provide bacteria with the capacity to 'talk' to each other. The predatory behaviour of bacteriophages, a type of virus that infects bacteria, also shapes bacterial communities. Bacteriophages are key regulators of bacterial populations, not only by their influence in population growth dynamics but also by their ability to transfer genetic material between bacteria, contributing to the diversification of the bacterial genomes. Until recently, phages were considered mere bystanders in microbial communication networks. However, this program will explore the idea that phages are in fact key participants. The discovery of a phage-encoded quorum sensing system that influences group decisions opens up a new research field that we intend to explore in this work: do phages communicate with their host or with other mobile genetic elements? How do these social interactions occur? How do these interactions affect population dynamics or bacterial virulence? This programme will make significant contributions to different scientific fields, from addressing the molecular basis of fundamental biological processes to understanding the evolution of virulence and the spread of antibiotic resistance in nature.

Communication is a key element in all successful organisations. Almost all living forms have developed systems to communicate and thereby coordinate their behaviours when living in complex ecological communities. Phages are not an exception and recently, intricate social interactions such as cooperation between phages to co-infect a host or altruism to overthrown bacterial defence mechanisms have been observed. The recent discovery of the arbitrium system, a quorum sensing communication system in phages infecting Bacillus highlights these entities as more social than previously thought. The system is widely distributed amongst phages in different Bacillus species, and it is composed of three main elements: a small signalling peptide (aimP) that binds to the transcriptional factor (aimR) regulating the expression of a small non-coding RNA (aimX), which in turn controls the decision between lytic or lysogenic pathways by an unknown mechanism. Notably, the arbitrium system is not exclusive to phages but it is also present in other MGEs including plasmids and ICEs, confirming the universality of this communication system. A close examination indicates that several of these elements encode for identical AimP signal peptides, opening the possibility of cross interactions between these MGEs. Since plasmids and ICEs do not engage in the phage lytic/lysogenic lifestyle, the presence of arbitrium in these elements is intriguing. What role is the system playing in these elements? It is possible that arbitrium possesses an alternative role, or it could be used to engage in social relationships (competition, cooperation). In this project we will unravel the molecular basis of these communication systems, not exclusively in phages but also in plasmids and ICEs. Moreover, we hypothesise that arbitrium systems are used by phages and other MGEs as communication systems to engage in complex social interactions, which will change our understanding of how microbial communities work.