Co-Swarming and Local Collapse: Quorum Sensing Conveys Resilience to Bacterial Communities by Localizing Cheater Mutants in Pseudomonas aeruginosa

Venturi, Vittorio; Bertani, Iris; Kerényi, Ádám; Netotea, Sergiu; Pongor, Sándor

doi:10.1371/journal.pone.0009998

Cited by 52 publications

(58 citation statements)

References 25 publications

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“…These data suggest that OmpA is most important during initial stages of Sodalis gut colonization, as cells that lack this protein can reach normal densities over time. Interestingly, previous studies using other model systems have shown that mutant bacteria can "cheat" their colonization defect by cross-feeding off relevant protein products produced by endogenous bacteria also present in the system (30,38,45,46). We thus investigated whether Sodalis ⌬OmpA cells are able to colonize wild-type tsetse by cheating off the Sodalis naturally found in these flies.…”

Section: Gmmmentioning

confidence: 99%

OmpA-Mediated Biofilm Formation Is Essential for the Commensal Bacterium Sodalis glossinidius To Colonize the Tsetse Fly Gut

Maltz

Weiss

O’Neill

et al. 2012

Appl Environ Microbiol

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Many bacteria successfully colonize animals by forming protective biofilms. Molecular processes that underlie the formation and function of biofilms in pathogenic bacteria are well characterized. In contrast, the relationship between biofilms and host colonization by symbiotic bacteria is less well understood. Tsetse flies (Glossina spp.) house 3 maternally transmitted symbionts, one of which is a commensal (Sodalis glossinidius) found in several host tissues, including the gut. We determined that Sodalis forms biofilms in the tsetse gut and that this process is influenced by the Sodalis outer membrane protein A (OmpA). Mutant Sodalis strains that do not produce OmpA (Sodalis ⌬OmpA mutants) fail to form biofilms in vitro and are unable to colonize the tsetse gut unless endogenous symbiotic bacteria are present. Our data indicate that in the absence of biofilms, Sodalis ⌬OmpA mutant cells are exposed to and eliminated by tsetse's innate immune system, suggesting that biofilms help Sodalis evade the host immune system. Tsetse is the sole vector of pathogenic African trypanosomes, which also reside in the fly gut. Acquiring a better understanding of the dynamics that promote Sodalis colonization of the tsetse gut may enhance the development of novel disease control strategies.

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Section: Gmmmentioning

confidence: 99%

OmpA-Mediated Biofilm Formation Is Essential for the Commensal Bacterium Sodalis glossinidius To Colonize the Tsetse Fly Gut

Maltz

Weiss

O’Neill

et al. 2012

Appl Environ Microbiol

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“…I reasoned that due to its immunity to cheating and its global benefit to the population, the diverged QS strain (R 2 S 2 ) would perform better than the original QS strain (R 1 S 1 ) when each strain competes with the intermediate strain R 2 S 1 in a structured population (18)(19)(20). I analyzed the two competitions in the bottlenecked growth model for various bottleneck sizes ( Fig.…”

Section: Divergence Is Positively Selected By Rounds Of Cheating Andmentioning

confidence: 99%

“…From a social perspective these can be characterized as "public goods"-costly actions to the individual that benefit the whole population (SI Text, section 1). As such, QS was shown both theoretically (14-16) and experimentally (17)(18)(19)(20) to be susceptible to invasion by QS mutants that act as "cheaters" and exploit the public goods produced by a functioning QS strain. Such cheating can be repressed by mechanisms that increase relatedness and lead to preferential assortment of cooperators and cheaters through structured populations (21-24).…”

mentioning

confidence: 99%

Social conflict drives the evolutionary divergence of quorum sensing

Eldar

2011

Proc. Natl. Acad. Sci. U.S.A.

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In microbial "quorum sensing" (QS) communication systems, microbes produce and respond to a signaling molecule, enabling a cooperative response at high cell densities. Many species of bacteria show fast, intraspecific, evolutionary divergence of their QS pathway specificity-signaling molecules activate cognate receptors in the same strain but fail to activate, and sometimes inhibit, those of other strains. Despite many molecular studies, it has remained unclear how a signaling molecule and receptor can coevolve, what maintains diversity, and what drives the evolution of cross-inhibition. Here I use mathematical analysis to show that when QS controls the production of extracellular enzymes -"public goods"-diversification can readily evolve. Coevolution is positively selected by cycles of alternating "cheating" receptor mutations and "cheating immunity" signaling mutations. The maintenance of diversity and the evolution of cross-inhibition between strains are facilitated by facultative cheating between the competing strains. My results suggest a role for complex social strategies in the longterm evolution of QS systems. More generally, my model of QS divergence suggests a form of kin recognition where different kin types coexist in unstructured populations.ooperative behavior in bacteria is guided in many cases by quorum sensing (QS) signaling where a response is produced only once a secreted signal's level is sufficient to activate its cognate receptor (1). Multiple bacterial species show intraspecific divergence of their QS systems, where signals from one strain can activate their own receptor but fail to activate and sometimes inhibit a receptor from a different strain (2-7). This divergence seems to be under strong selection, as implied by the functional divergence and is also corroborated by rapid sequence divergence (8-9), the signatures of diversifying selection (10-11), and the spread of divergent QS systems through horizontal gene transfer (3, 12). These observations provoke two related questions: How does this divergence evolve in the first place, and what are the selective advantages that maintain it? Moreover, in some of the systems, a signaling molecule from one strain inhibits a diverged receptor from receiving its own signal (2, 7, 12). It is unclear whether the same evolutionary forces that drive divergence can drive the evolution of cross-inhibition.The cross-inhibition between diverging strains in some of these species and the ecological coexistence of divergent strains in others (13) imply a possible intraspecific social role for this divergence. Therefore, to understand QS diversification, one has to consider it in a social context. It has been shown in numerous species that QS controls the production of secreted substances (e.g., exoproteases, surfactants, and antibiotics; see SI Text, section 1 for further discussion). From a social perspective these can be characterized as "public goods"-costly actions to the individual that benefit the whole population (SI Text, section 1). As such, QS was ...

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“…We share the widespread opinion that the "change of bacterial lifestyle" is crucial for colonizing habitats and infecting susceptible hosts -unfortunately the signalling systems that orchestrate the underlying communication and collaboration mechanisms are not accurately annotated in bacterial genomes. Therefore, a systematic characterization of QS systems in Gram negative bacteria was carried out [68,69] and a modelling effort to map out the theoretically possible consequences of communication and collaboration in bacterial populations was initiated [70][71][72]. Virulence and adaptability of many Gram-negative bacterial species are associated with an N-acylhomoserine lactone (AHL) gene regulation mechanism called quorum sensing (QS).…”

Section: Bacterial Communication and Cooperation In Health And Diseasementioning

confidence: 99%

Clinical Proteomics and Omics Clues Useful in Translational Medicine Research

2014

Omics in Clinical Practice

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Abstract:The currently hyped expectation of personalized medicine is often associated with just achieving the information technology led integration of biomolecular sequencing, expression and histopathological bioimaging data with clinical records at the individual patients' level as if the significant biomedical conclusions would be its more or less mandatory result. It remains a sad fact that many, if not most biomolecular mechanisms that translate the human genomic information into phenotypes are not known and, thus, most of the molecular and cellular data cannot be interpreted in terms of biomedically relevant conclusions. Whereas the historical trend will certainly be into the general direction of personalized diagnostics and cures, the temperate view suggests that biomedical applications that rely either on the comparison of biomolecular sequences and/or on the already known biomolecular mechanisms have much greater chances to enter clinical practice soon. In addition to considering the general trends, we exemplarily review advances in the area of cancer biomarker discovery, in the clinically relevant characterization of patient-specific viral and bacterial pathogens (with emphasis on drug selection for influenza and enterohemorrhagic E. coli) as well as progress in the automated assessment of histopathological images. As molecular and cellular data analysis will become instrumental for achieving desirable clinical outcomes, the role of bioinformatics and computational biology approaches will dramatically grow.Author summary: With DNA sequencing and computers becoming increasingly cheap and accessible to the layman, the idea of integrating biomolecular and clinical patient data seems to become a realistic, short-term option that will lead to patient-specific diagnostics and treatment design for many diseases such as cancer, metabolic disorders, inherited conditions, etc. These hyped expectations will fail since many, if not most biomolecular mechanisms that translate the human genomic information into phenotypes are not known yet and, thus, most of the molecular and cellular data collected will not lead to biomedically relevant conclusions. At the same time, less spectacular biomedical applications based on biomolecular sequence comparison and/or known biomolecular mechanisms have the potential to unfold enormous potential for healthcare and public health. Since the analysis of heterogeneous biomolecular data in context with clinical data will be increasingly critical, the role of bioinformatics and computational biology will grow correspondingly in this process.

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Co-Swarming and Local Collapse: Quorum Sensing Conveys Resilience to Bacterial Communities by Localizing Cheater Mutants in Pseudomonas aeruginosa

Cited by 52 publications

References 25 publications

OmpA-Mediated Biofilm Formation Is Essential for the Commensal Bacterium Sodalis glossinidius To Colonize the Tsetse Fly Gut

OmpA-Mediated Biofilm Formation Is Essential for the Commensal Bacterium Sodalis glossinidius To Colonize the Tsetse Fly Gut

Social conflict drives the evolutionary divergence of quorum sensing

Clinical Proteomics and Omics Clues Useful in Translational Medicine Research

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