Surface association sensitizes Pseudomonas aeruginosa to quorum sensing

Chuang, Sara K.; Vrla, Geoffrey D.; Fröhlich, Kathrin S.

doi:10.1038/s41467-019-12153-1

Cited by 39 publications

(48 citation statements)

References 56 publications

(81 reference statements)

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“…Moreover, the analyses should be performed using static cultures that favour biofilm formation and AHL production and the culture medium can also strongly affect AHL production. Since surface adherence or cell-to-cell adherence is required to activate AHL synthesis in some bacteria 34,48 and specific bacteria modify the gene expression in oral biofilms 4 , these biofilm-promoting cultivation conditions may have triggered the expression of QS-related genes not expressed in axenic cultures or under agitated conditions. Moreover, AHLs may be only produced in mixed cultures, as demonstrated by the increase in AHL production in mixed cultures of P. gingivalis.…”

Section: Discussionmentioning

confidence: 99%

Acyl homoserine lactone-mediated quorum sensing in the oral cavity: a paradigm revisited

Muras

Otero-Casal

Blanc

et al. 2020

Sci Rep

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Acyl homoserine lactones (AHLs), the quorum sensing (QS) signals produced by Gram-negative bacteria, are currently considered to play a minor role in the development of oral biofilm since their production by oral pathogens has not been ascertained thus far. However, we report the presence of AHLs in different oral samples and their production by the oral pathogen Porphyromonas gingivalis. the importance of AHLs is further supported by a very high prevalence of AHL-degradation capability, up to 60%, among bacteria isolated from dental plaque and saliva samples. Furthermore, the widespectrum AHL-lactonase Aii20J significantly inhibited oral biofilm formation in different in vitro biofilm models and caused important changes in bacterial composition. Besides, the inhibitory effect of Aii20J on a mixed biofilm of 6 oral pathogens was verified using confocal microscopy. Much more research is needed in order to be able to associate specific AHLs with oral pathologies and to individuate the key actors in AHL-mediated QS processes in dental plaque formation. However, these results indicate a higher relevance of the AHLs in the oral cavity than generally accepted thus far and suggest the potential use of inhibitory strategies against these signals for the prevention and treatment of oral diseases.

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Section: Discussionmentioning

confidence: 99%

Acyl homoserine lactone-mediated quorum sensing in the oral cavity: a paradigm revisited

Muras

Otero-Casal

Blanc

et al. 2020

Sci Rep

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“…Cellular responses to exogenous RNA were discovered over 20 years ago in C. elegans (Fire et al, 1998), but the natural context in which worms evolved the ability to detect and respond to non-viral RNA remains unclear (Braukmann et al, 2019). Here we have identified a trans-kingdom signaling system that uses components of the RNAi pathway to "read" bacterial small RNAs, particularly P11, which is required for surface-growth of PA14 (Chuang et al, 2019) and virulence (our results). This small RNA-sensing pathway depends on processing through the germline and subsequent communication to neurons, and is independent of the pathways induced by innate immune systems and secreted molecules (Meisel et al, 2014;Papenfort and Bassler, 2016).…”

Section: Elegans Can Identify Bacteria By "Reading" Their Small Rnasmentioning

confidence: 94%

C. elegans “reads” bacterial non-coding RNAs to learn pathogenic avoidance

Kaletsky

Moore²,

Vrla³

et al. 2020

Preprint

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C. elegans is exposed to many different bacteria in its environment, and must distinguish pathogenic from nutritious bacterial food sources. Here, we show that a single exposure to purified small RNAs isolated from pathogenic Pseudomonas aeruginosa (PA14) is sufficient to induce pathogen avoidance, both in the treated animals and in four subsequent generations of progeny. The RNA interference and piRNA pathways, the germline, and the ASI neuron are required for bacterial small RNA-induced avoidance behavior and transgenerational inheritance. A single non-coding RNA, P11, is both necessary and sufficient to convey learned avoidance of PA14, and its C. elegans target, maco-1, is required for avoidance. A natural microbiome Pseudomonas isolate, GRb0427, can induce avoidance via its small RNAs, and the wild C. elegans strain JU1580 responds similarly to bacterial sRNA. Our results suggest that this ncRNA-dependent mechanism evolved to survey the worm's microbial environment, use this information to make appropriate behavioral decisions, and pass this information on to its progeny.

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“…However, previous reports demonstrated that in high-density liquid cultures, rhlR mutants have increased expression of the pqsABCDE genes [13], indicating that RhlR acts to repress this operon. We recently reported that a small RNA immediately upstream of pqsA, Lrs1, is also surface induced [33] and has a RhlR binding site in its promoter. Since the lrs1 sequence is predicted to form a secondary structure that could disrupt pqsABCDE promoter activity, we hypothesized that RhlR could exert either positive or negative effects on pqsABCDE expression depending on whether the transcript made by the Lrs1 promoter is terminated.…”

Section: Plos Pathogensmentioning

confidence: 99%

Cytotoxic alkyl-quinolones mediate surface-induced virulence in Pseudomonas aeruginosa

et al. 2020

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Surface attachment, an early step in the colonization of multiple host environments, activates the virulence of the human pathogen P. aeruginosa. However, the downstream toxins that mediate surface-dependent P. aeruginosa virulence remain unclear, as do the signaling pathways that lead to their activation. Here, we demonstrate that alkyl-quinolone (AQ) secondary metabolites are rapidly induced upon surface association and act directly on host cells to cause cytotoxicity. Surface-induced AQ cytotoxicity is independent of other AQ functions like quorum sensing or PQS-specific activities like iron sequestration. We further show that packaging of AQs in outer-membrane vesicles (OMVs) increases their cytotoxicity to host cells but not their ability to stimulate downstream quorum sensing pathways in bacteria. OMVs lacking AQs are significantly less cytotoxic, suggesting these molecules play a role in OMV cytotoxicity, in addition to their previously characterized role in OMV biogenesis. AQ reporters also enabled us to dissect the signal transduction pathways downstream of the two known regulators of surface-dependent virulence, the quorum sensing receptor, LasR, and the putative mechanosensor, PilY1. Specifically, we show that PilY1 regulates surfaceinduced AQ production by repressing the AlgR-AlgZ two-component system. AlgR then induces RhlR, which can induce the AQ biosynthesis operon under specific conditions. These findings collectively suggest that the induction of AQs upon surface association is both necessary and sufficient to explain surface-induced P. aeruginosa virulence.

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Surface association sensitizes Pseudomonas aeruginosa to quorum sensing

Cited by 39 publications

References 56 publications

Acyl homoserine lactone-mediated quorum sensing in the oral cavity: a paradigm revisited

Acyl homoserine lactone-mediated quorum sensing in the oral cavity: a paradigm revisited

C. elegans “reads” bacterial non-coding RNAs to learn pathogenic avoidance

Cytotoxic alkyl-quinolones mediate surface-induced virulence in Pseudomonas aeruginosa

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