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Rich Repertoire of Quorum Sensing Protein Coding Sequences in CPR and DPANN Associated with Interspecies and Interkingdom Communication.

ABSTRACT: The bacterial candidate phyla radiation (CPR) and the archaeal DPANN superphylum are two novel lineages that have substantially expanded the tree of life due to their large phylogenetic diversity. Because of their ultrasmall size, reduced genome, and lack of core biosynthetic capabilities, most CPR and DPANN members are predicted to be sustained through their interactions with other species. How the few characterized CPR and DPANN symbionts achieve these critical interactions is, however, poorly understood. Here, we conducted an in silico analysis on 2,597 CPR/DPANN genomes to test whether these ultrasmall microorganisms might encode homologs of reference proteins involved in the synthesis and/or the detection of 26 different types of communication molecules (quorum sensing [QS] signals), since QS signals are well-known mediators of intra- and interorganismic relationships. We report the discovery of 5,693 variants of QS proteins distributed across 63 CPR and 6 DPANN phyla and associated with 14 distinct types of communication molecules, most of which were characterized as interspecies QS signals.IMPORTANCE The selection of predicted genes for interspecies communication within the CPR and DPANN genomes sheds some light onto the underlying mechanisms supporting their inferred symbiotic lifestyle. Also, considering the lack of core pathways such as the de novo synthesis of nucleotides or amino acids in the CPR and DPANN lineages, the persistence of these genes highlights how determinant social traits can be for the survival of some microorganisms. Finally, the considerable number of variants of QS proteins identified among the 69 CPR and DPANN phyla substantially expands our knowledge of prokaryotic communication across the tree of life and suggests that the multiplicity of "dialects" in the microbial world is probably larger than previously appreciated.

SUBMITTER: Bernard C

PROVIDER: S-EPMC7567580 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Rich Repertoire of Quorum Sensing Protein Coding Sequences in CPR and DPANN Associated with Interspecies and Interkingdom Communication.

Bernard Charles C Lannes Romain R Li Yanyan Y Bapteste Éric É Lopez Philippe P

mSystems 20201013 5

The bacterial candidate phyla radiation (CPR) and the archaeal DPANN superphylum are two novel lineages that have substantially expanded the tree of life due to their large phylogenetic diversity. Because of their ultrasmall size, reduced genome, and lack of core biosynthetic capabilities, most CPR and DPANN members are predicted to be sustained through their interactions with other species. How the few characterized CPR and DPANN symbionts achieve these critical interactions is, however, poorly ...[more]

PMID: 33051376

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Project description:ABSTRACT Escherichia coli mazEF is a toxin-antitoxin stress-induced module mediating cell death. It requires the quorum-sensing signal (QS) "extracellular death factor" (EDF), the penta-peptide NNWNN (EcEDF), enhancing the endoribonucleolytic activity of E. coli toxin MazF. Here we discovered that E. coli mazEF-mediated cell death could be triggered by QS peptides from the supernatants (SN) of the Gram-positive bacterium Bacillus subtilis and the Gram-negative bacterium Pseudomonas aeruginosa. In the SN of B. subtilis, we found one EDF, the hexapeptide RGQQNE, called BsEDF. In the SN of P. aeruginosa, we found three EDFs: the nonapeptide INEQTVVTK, called PaEDF-1, and two hexadecapeptides, VEVSDDGSGGNTSLSQ, called PaEDF-2, and APKLSDGAAAGYVTKA, called PaEDF-3. When added to a diluted E. coli cultures, each of these peptides acted as an interspecies EDF that triggered mazEF-mediated death. Furthermore, though their sequences are very different, each of these EDFs amplified the endoribonucleolytic activity of E. coli MazF, probably by interacting with different sites on E. coli MazF. Finally, we suggest that EDFs may become the basis for a new class of antibiotics that trigger death from outside the bacterial cells. IMPORTANCE Bacteria communicate with one another via quorum-sensing signal (QS) molecules. QS provides a mechanism for bacteria to monitor each other's presence and to modulate gene expression in response to population density. Previously, we added E. coli EDF (EcEDF), the peptide NNWNN, to this list of QS molecules. Here we extended the group of QS peptides to several additional different peptides. The new EDFs are produced by two other bacteria, Bacillus subtilis and Pseudomonas aeruginosa. Thus, in this study we established a "new family of EDFs." This family provides the first example of quorum-sensing molecules participating in interspecies bacterial cell death. Furthermore, each of these peptides provides the basis of a new class of antibiotics triggering death by acting from outside the cell.

Project description:Quorum sensing (QS) regulates bacterial gene expression and studies suggest quercetin, a flavonol found in onion, as a QS inhibitor. There are no studies showing the anti-QS activity of plants containing quercetin in its native glycosylated forms. This study aimed to evaluate the antimicrobial and anti-QS potential of organic extracts of onion varieties and its representative phenolic compounds quercetin aglycone and quercetin 3-β-D-glucoside in the QS model bacteria Chromobacterium violaceum ATCC 12472, Pseudomonas aeruginosa PAO1, and Serratia marcescens MG1. Three phenolic extracts were obtained: red onion extract in methanol acidified with 2.5% acetic acid (RO-1), white onion extract in methanol (WO-1) and white onion extract in methanol ammonium (WO-2). Quercetin 4-O-glucoside and quercetin 3,4-O-diglucoside were identified as the predominant compounds in both onion varieties using HPLC-DAD and LC-ESI-MS/MS. However, quercetin aglycone, cyanidin 3-O-glucoside and quercetin glycoside were identified only in RO-1. The three extracts showed minimum inhibitory concentration (MIC) values equal to or above 125 μg/ml of dried extract. Violacein production was significantly reduced by RO-1 and quercetin aglycone, but not by quercetin 3-β-D-glucoside. Motility in P. aeruginosa PAO1 was inhibited by RO-1, while WO-2 inhibited S. marcescens MG1 motility only in high concentration. Quercetin aglycone and quercetin 3-β-D-glucoside were effective at inhibiting motility in P. aeruginosa PAO1 and S. marcescens MG1. Surprisingly, biofilm formation was not affected by any extracts or the quercetins tested at sub-MIC concentrations. In silico studies suggested a better interaction and placement of quercetin aglycone in the structures of the CviR protein of C. violaceum ATCC 12472 than the glycosylated compound which corroborates the better inhibitory effect of the former over violacein production. On the other hand, the two quercetins were well placed in the AHLs binding pockets of the LasR protein of P. aeruginosa PAO1. Overall onion extracts and quercetin presented antimicrobial activity, and interference on QS regulated production of violacein and swarming motility.

Dataset Information

Rich Repertoire of Quorum Sensing Protein Coding Sequences in CPR and DPANN Associated with Interspecies and Interkingdom Communication.

Publications

Rich Repertoire of Quorum Sensing Protein Coding Sequences in CPR and DPANN Associated with Interspecies and Interkingdom Communication.

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