Peptide-based quorum sensing systems in Paenibacillus polymyxa

Abstract

Paenibacillus polymyxa is an agriculturally important plant growth–promoting rhizobacterium. Many Paenibacillus species are known to be engaged in complex bacteria–bacteria and bacteria–host interactions, which in other species were shown to necessitate quorum sensing communication. However, to date, no quorum sensing systems have been described in Paenibacillus. Here, we show that the type strain P. polymyxa ATCC 842 encodes at least 16 peptide-based communication systems. Each of these systems is comprised of a pro-peptide that is secreted to the growth medium and processed to generate a mature short peptide. Each peptide has a cognate intracellular receptor of the RRNPP family, and we show that external addition of P. polymyxa communication peptides leads to reprogramming of the transcriptional response. We found that these quorum sensing systems are conserved across hundreds of species belonging to the Paenibacillaceae family, with some species encoding more than 25 different peptide-receptor pairs, representing a record number of quorum sensing systems encoded in a single genome.

RRNPP_detector: a tool to detect RRNPP quorum sensing systems in chromosomes, plasmids and phages of gram-positive bacteria

“…Of the 3529 conservative candidate RRNPP QSSs, we found that 2793 are chromosomal (on 941 different chromosomes), 222 are plasmidic (on 172 different plasmids), 505 are predicted to be prophage-encoded (on 219 predicted intact prophages, 102 questionable prophages and 176 incomplete prophages) and 9 are encoded by genomes isolated from free temperate bacteriophages (on 8 distinct bacteriophages) ( Table S2 ). Although the presence of multiple QSSs on single chromosomes is not rare (8,21) due to the selective pressure that may exist for the acquisition of additional subpopulation-specific QSSs (41,42), only 1 MGE (Bacillus phage phi3T) has been previously reported to encode two RRNPP QSSs (43). Here, we report the identification of 30 plasmids and 8 (pro)phages encoding multiple candidate RRNPP QSSs (up to 5 in the pBMB400 plasmid of Bacillus thuringiensis serovar kurstaki str.…”

“…even discovered that some temperate bacteriophages encode RRNPP QSSs, namely the “arbitrium” systems that guide the lysis-lyogeny decision upon Bacillus infection (18,19). Recently, two other chromosomal RRNPP QSSs have been experimentally validated: the QsrB-QspB system that delays sporulation and solvent formation in Clostridium acetobutylicum (20) and the AloR13-AloP13 sporulation-regulator in Paenibacillus polymyxa (21). As important the experimentally-validated RRNPP QSSs are in the regulation of the biology of their encoding microbial entity, they represent only the tip of the iceberg.…”

Large-scale identification of viral quorum sensing systems reveals density-dependent sporulation-hijacking mechanisms in bacteriophages

“…3A). These results especially make sense in light of a recently identified chromosomal RRNPPtype QSS, shown to regulate the expression of its adjacent spo0E gene in a density dependent manner (31). The functions of the other (pro)phage-encoded candidate QSSs were difficult to predict from their genomic contexts and would require further exciting functional studies to characterize which biological processes they might regulate in a (pro)phage-density dependent manner.…”

“…Second, it consists in retaining only the coding sequences of those putative receptors that are located directly adjacent to the coding sequence of a candidate communication pro-peptide, defined as a small protein of 15-65 aa predicted to be secreted via the SEC-translocon by the stringent SignalP software (Fig. 1 (31).…”

“…As this signature-based method does not rely on homology search of already known QSSs, it has the potential to detect novel candidate 4 RRNPP-type QSS families, and thus novel 'languages' of peptide-based biocommunication via quorum sensing. The same principle, albeit implemented differently, was recently applied by Voichek et al in the Paenibacillus genus, and proved its efficiency at detecting novel, functional QSSs (31).…”