Quorum sensing systems (QSSs) are genetic systems supporting cell-cell or bacteriophage-bacteriophage communication. By regulating behavioral switches as a function of the encoding population density, QSSs shape the social dynamics of microbial communities. However, their diversity is tremendously overlooked in bacteriophages, which implies that many density-dependent behaviors likely remains to be discovered in these viruses. Here, we developed a signature-based computational method to identify novel peptide-based RRNPP QSSs in gram-positive bacteria (e.g. Firmicutes) and their mobile genetic elements. The large-scale application of this method against available genomes of Firmicutes and bacteriophages revealed 2708 candidate RRNPP-type QSSs, including 382 found in (pro)phages. These 382 viral candidate QSSs are classified into 25 different groups of homologs, of which 22 were never described before in bacteriophages. Remarkably, genomic context analyses suggest that candidate viral QSSs from 6 different families dynamically manipulate the host biology. Specifically, many viral candidate QSSs are predicted to regulate, in a density-dependent manner, adjacent (pro)phage-encoded regulator genes whose bacterial homologs are key regulators of the sporulation initiation pathway (either Rap, Spo0E, or AbrB). Consistently, we found evidence from public data that certain of our candidate (pro)phage-encoded QSSs dynamically manipulate the timing of sporulation of the bacterial host. These findings challenge the current paradigm assuming that bacteria decide to sporulate in adverse situation. Indeed, our survey highlights that bacteriophages have evolved, multiple times, genetic systems that dynamically influence this decision to their advantage, making sporulation a survival mechanism of last resort for phage-host collectives.
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