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Peptide-Based Quorum Sensing Systems in Paenibacillus Polymyxa

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Peptide-Based Quorum Sensing Systems in Paenibacillus Polymyxa bioRxiv preprint doi: https://doi.org/10.1101/767517; this version posted September 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Peptide-based quorum sensing systems in Paenibacillus polymyxa 2 3 Maya Voichek1, Sandra Maaß2, Tobias Kroniger2, Dörte Becher2, Rotem Sorek1,# 4 5 1 Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel 6 2 Institute of Microbiology, Department of Microbial Proteomics; Center for Functional 7 Genomics of Microbes, University of Greifswald, Germany. 8 # Correspondence: [email protected] bioRxiv preprint doi: https://doi.org/10.1101/767517; this version posted September 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 9 Abstract 10 Paenibacillus polymyxa is an agriculturally important plant growth-promoting 11 rhizobacterium. Many Paenibacillus species are known to be engaged in complex bacteria- 12 bacteria and bacteria-host interactions, which in other species were shown to necessitate 13 quorum sensing communication. However, to date no quorum sensing systems have been 14 described in Paenibacillus. Here we show that the type strain P. polymyxa ATCC 842 15 encodes at least 16 peptide-based communication systems. Each of these systems is 16 comprised of a pro-peptide that is secreted to the growth medium and processed to generate 17 a mature short peptide. Each peptide has a cognate intracellular receptor of the RRNPP 18 family, and we show that external addition of P. polymyxa communication peptides leads 19 to reprogramming of the transcriptional response. We found that these quorum sensing 20 systems are conserved across hundreds of species belonging to the Paenibacillaceae 21 family, with some species encoding more than 25 different peptide-receptor pairs, 22 representing a record number of quorum sensing systems encoded in a single genome. bioRxiv preprint doi: https://doi.org/10.1101/767517; this version posted September 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 23 Introduction 24 Paenibacillaceae is a diverse family of bacteria, many of which are important in 25 agricultural and clinical settings. These include Paenibacillus larvae, a pathogen causing 26 the lethal American Foulbrood disease in honeybees1, as well as P. dendritiformis and P. 27 vortex, which are used as models for complex colony pattern formation2,3. Arguably the 28 best studied member of Paenibacillaceae is P. polymyxa, known for its plant-growth 29 promoting traits4–6. P. polymyxa produces a plethora of beneficial compounds, including 30 the antibiotic polymyxin7 and the phytohormone indole-3-acetic acid (IAA)8, and was 31 shown to protect multiple plant species against pathogens (reviewed in 9). Due to its 32 beneficial traits, P. polymyxa is commercially used as a soil supplement to improve crop 33 growth10,11. 34 Many of the characteristic features associated with the above-mentioned behaviors – 35 production and secretion of antimicrobials, expression of virulence factors, and forming 36 complex colony structures – often require some form of inter-cellular communication such 37 as quorum sensing12. Bacteria use quorum sensing to coordinate gene expression patterns 38 on a population level. For example, the quorum sensing network of Pseudomonas 39 aeruginosa controls the production of secreted toxins as well as the production of 40 rhamnolipids, which are important for its biofilm architecture13,14. Quorum sensing 41 regulates the production of bacteriocin antimicrobials in Lactobacilli15 and 42 Streptococci16,17; and in Bacillus subtilis, quorum sensing systems play a major role in 43 sporulation, biofilm formation and genetic competence18. Although Paenibacillus bacteria 44 are engaged in similar behaviors, no quorum sensing was reported in any Paenibacillus 45 species to date. 46 Gram-positive bacteria frequently use short peptides, termed autoinducer peptides, as their 47 quorum sensing agents12. A widespread group of such peptide-based communication 48 systems involves intracellular peptide sensors (receptors) of the RRNPP family, together 49 with their cognate peptides19. Peptides of these quorum sensing systems are secreted from 50 the cell as pro-peptides and are further processed by extracellular proteases20 to produce a 51 mature short peptide, usually 5-10 amino acids (aa) long19,21. The mature peptides are re- 52 internalized into the cells via the oligopeptide permease (OPP) transporter22,23, and bind bioRxiv preprint doi: https://doi.org/10.1101/767517; this version posted September 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 53 their intracellular receptors24. These receptors act either as transcription factors or as 54 phosphatases, and peptide binding activates or represses their function eventually leading 55 to modulation of the bacterial transcriptional program. For example, in B. subtilis the Rap 56 receptors function as phosphatases that regulate the major transcription factor Spo0A; upon 57 binding to their cognate Phr peptides, the phosphatase activity of Rap receptors is inhibited, 58 leading to activation of Spo0A that alters the transcriptional program25,26. In B. 59 thuringiensis the PlcR receptor is a transcription factor that becomes activated when bound 60 to its cognate PapR peptide, leading to expression of virulence factors that facilitate 61 infection of its insect larval host27. Such peptide-based communication was recently shown 62 also to control the lysis-lysogeny decision of phages infecting many species of Bacillus28,29. 63 Here we report the identification of a large group of peptide-based quorum sensing systems 64 in P. polymyxa. We found that pro-peptides of these systems are secreted and further 65 processed, and that the mature peptides modulate the transcriptional program of P. 66 polymyxa. We further show that these quorum sensing systems are conserved throughout 67 the Paenibacillaceae family of bacteria, with some bacteria encoding over 25 different 68 peptide-receptor pairs in a single genome. 69 Results 70 Identification of RRNPP-like peptide-receptor pairs in P. polymyxa ATCC 842 71 All members of the RRNPP family of intracellular peptide receptors contain a C-terminal 72 tetratricopeptide repeat (TPR) or TPR-like domain, which forms the peptide-binding 73 pocket in the receptor protein19,30. To search for possible such quorum sensing systems in 74 P. polymyxa we first scanned all annotated protein-coding genes of the type strain P. 75 polymyxa ATCC 84231 for TPR domains using TPRpred32 (Methods). As TPR domains are 76 found in diverse protein types, we manually analyzed the genomic vicinity of the identified 77 TPR-containing proteins to search for a peptide-encoding gene characteristic of quorum 78 sensing systems. We found two TPR domain genes that were immediately followed by a 79 short open reading frame with a predicted N-terminal hydrophobic helix, typical of a signal 80 peptide that targets the pro-peptide for secretion33 (Fig. 1a). Two-gene operons that encode bioRxiv preprint doi: https://doi.org/10.1101/767517; this version posted September 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 81 the receptor followed by its cognate peptide are a hallmark of many known members of 82 the RRNPP family of quorum sensing systems19. 83 We then used BLAST to search for additional homologs of the two putative TPR-domain 84 receptors in the P. polymyxa ATCC 842 genome (Methods). This search revealed 14 85 additional homologous genes that were not initially recognized by TPRpred, in most cases 86 because their C-terminal TPR domains were divergent and did not pass the default 87 threshold of the TPRpred software. We found that all but three of the homologs had a short 88 ORF (32-50 aa) encoded immediately downstream to them. We denote these putative 89 communication systems as Alo (Autoinducer peptide Locus), with predicted Alo receptor 90 genes designated aloR and the cognate peptide-encoded gene aloP. We number Alo loci in 91 the P. polymyxa ATCC 842 genome from alo1 to alo16 (Fig. 1b). 92 93 Fig. 1: Alo systems identified in P. polymyxa. (a) Schematic representation of aloR-aloP operon 94 organization and putative peptide processing. HTH, helix-turn-helix; TPR, tetratricopeptide repeat. (b) Alo 95 loci identified in P. polymyxa ATCC 842. For the aloR receptor genes, the locus tag in the IMG database34 is 96 specified. Blue sequence in AloP peptides represents the predicted N-terminal signal sequence for 97 secretion, as predicted by Phobius35 (Methods). Asterisks (*) mark cases in which the aloP gene was absent 98 or found as a degenerate sequence. bioRxiv preprint doi: https://doi.org/10.1101/767517; this version posted September 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 99 Alo systems are ubiquitous in P. polymyxa strains 100 Examining the genomes of 13 additional P.
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