scholarly journals The Pseudomonas aeruginosa PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms

mBio ◽  
2017 ◽  
Vol 8 (3) ◽  
Author(s):  
Yasuhiko Irie ◽  
Aled E. L. Roberts ◽  
Kasper N. Kragh ◽  
Vernita D. Gordon ◽  
Jaime Hutchison ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Quorum Sensing ◽  
Public Goods ◽  
Structural Integrity ◽  
Population Level ◽  
Social Benefits ◽  
Extracellular Polysaccharides ◽  
Public Benefits ◽  
Private And Public ◽  
Fitness Benefits

ABSTRACT Extracellular polysaccharides are compounds secreted by microorganisms into the surrounding environment, and they are important for surface attachment and maintaining structural integrity within biofilms. The social nature of many extracellular polysaccharides remains unclear, and it has been suggested that they could function as either cooperative public goods or as traits that provide a competitive advantage. Here, we empirically tested the cooperative nature of the PSL polysaccharide, which is crucial for the formation of biofilms in Pseudomonas aeruginosa. We show that (i) PSL is not metabolically costly to produce; (ii) PSL provides population-level benefits in biofilms, for both growth and antibiotic tolerance; (iii) the benefits of PSL production are social and are shared with other cells; (iv) the benefits of PSL production appear to be preferentially directed toward cells which produce PSL; (v) cells which do not produce PSL are unable to successfully exploit cells which produce PSL. Taken together, this suggests that PSL is a social but relatively nonexploitable trait and that growth within biofilms selects for PSL-producing strains, even when multiple strains are on a patch (low relatedness at the patch level). IMPORTANCE Many studies have shown that bacterial traits, such as siderophores and quorum sensing, are social in nature. This has led to an impression that secreted traits act as public goods, which are costly to produce but benefit both the producing cell and its surrounding neighbors. Theories and subsequent experiments have shown that such traits are exploitable by asocial cheats, but we show here that this does not always hold true. We demonstrate that the Pseudomonas aeruginosa exopolysaccharide PSL provides social benefits to populations but that it is nonexploitable, because most of the fitness benefits accrue to PSL-producing cells. Our work builds on an increasing body of work showing that secreted traits can have both private and public benefits to cells. Many studies have shown that bacterial traits, such as siderophores and quorum sensing, are social in nature. This has led to an impression that secreted traits act as public goods, which are costly to produce but benefit both the producing cell and its surrounding neighbors. Theories and subsequent experiments have shown that such traits are exploitable by asocial cheats, but we show here that this does not always hold true. We demonstrate that the Pseudomonas aeruginosa exopolysaccharide PSL provides social benefits to populations but that it is nonexploitable, because most of the fitness benefits accrue to PSL-producing cells. Our work builds on an increasing body of work showing that secreted traits can have both private and public benefits to cells.

scholarly journals The Pseudomonas aeruginosa PSL polysaccharide is a social but non-cheatable trait in biofilms

2016 ◽  
Author(s):  
Yasuhiko Irie ◽  
Aled E. L. Roberts ◽  
Kasper N. Kragh ◽  
Vernita D. Gordon ◽  
Jaime Hutchison ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Competitive Advantage ◽  
Structural Integrity ◽  
Population Level ◽  
Extracellular Polysaccharides ◽  
Surface Attachment ◽  
Social Nature ◽  
Surrounding Environment ◽  
The Social ◽  
Multiple Strains

ABSTRACTExtracellular polysaccharides are compounds secreted by microorganisms into the surrounding environment and which are important for surface attachment and maintaining structural integrity within biofilms. The social nature of many extracellular polysaccharides remains unclear, and it has been suggested that they could function as either co-operative public goods, or as traits that provide a competitive advantage. Here we empirically test the co-operative nature of the PSL polysaccharide, which is crucial for the formation of biofilms in Pseudomonas aeruginosa. We show that: (1) PSL is not metabolically costly to produce; (2) PSL provides population level benefits in biofilms, for both growth and antibiotic tolerance; (3) the benefits of PSL production are social and are shared with other cells; (4) the benefits of PSL production appear to be preferentially directed towards cells which produce PSL; (5) cells which do not produce PSL are unable to successfully exploit cells which produce PSL. Taken together, this suggests that PSL is a social but relatively non-exploitable trait, and that growth within biofilms selects for PSL-producing strains, even when multiple strains can interact (low relatedness).

Rhamnolipids stabilize quorum sensing mediated cooperation in Pseudomonas aeruginosa

2020 ◽  
Vol 367 (10) ◽  
Author(s):  
Rodolfo García-Contreras ◽  
Daniel Loarca ◽  
Caleb Pérez-González ◽  
J Guillermo Jiménez-Cortés ◽  
Abigail Gonzalez-Valdez ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Quorum Sensing ◽  
Carbon Source ◽  
Public Goods ◽  
Sole Carbon Source ◽  
Regulatory Genes ◽  
Chronic Infections ◽  
Toxic Metabolites ◽  
Serial Cultivation ◽  
Selection Of

ABSTRACT Pseudomonas aeruginosa is one of the main models to study social behaviors in bacteria since it synthesizes several exoproducts, including exoproteases and siderophores and release them to the environment. Exoproteases and siderophores are public goods that can be utilized by the individuals that produce them but also by non-producers, that are considered social cheaters. Molecularly exoprotease cheaters are mutants in regulatory genes such as lasR, and are commonly isolated from chronic infections and selected in the laboratory upon serial cultivation in media with protein as a sole carbon source. Despite that the production of exoproteases is exploitable, cooperators have also ways to restrict the growth and selection of social cheaters, for instance by producing toxic metabolites like pyocyanin. In this work, using bacterial competitions, serial cultivation and growth assays, we demonstrated that rhamnolipids which production is regulated by quorum sensing, selectively affect the growth of lasR mutants and are able to restrict social cheating, hence contributing to the maintenance of cooperation in Pseudomonas aeruginosa populations.

scholarly journals The fitness ofPseudomonas aeruginosaquorum sensing signal cheats is influenced by the diffusivity of the environment

2016 ◽  
Author(s):  
Anne Mund ◽  
Stephen P. Diggle ◽  
Freya Harrison
Keyword(s):  
Quorum Sensing ◽  
Public Goods ◽  
Social Dynamics ◽  
Population Level ◽  
Opportunistic Pathogen ◽  
Signal Molecules ◽  
Wild Type ◽  
Signaling Systems ◽  
Environmental Structure ◽  
Bacterial Quorum

ABSTRACTExperiments examining the social dynamics of bacterial quorum sensing (QS) have focused on mutants which do not respond to signals, and the role of QS-regulated exoproducts as public goods. The potential for QS signal molecules to themselves be social public goods has received much less attention. Here, we analyse how signal-deficient (lasI−) mutants of the opportunistic pathogenPseudomonas aeruginosainteract with wild-type cells in an environment where QS is required for growth. We show that when growth requires a ‘private’ intracellular metabolic mechanism activated by the presence of QS signal,lasI−mutants act as social cheats and outcompete signal-producing wild-type bacteria in mixed cultures, because they can use the signals produced by wild type cells. However, reducing the ability of signal molecules to diffuse through the growth medium, results in signal molecules becoming less accessible to mutants, leading to reduced cheating. Our results indicate that QS signal molecules can be considered as social public goods in a way that has been previously described for other exoproducts, but that spatial structuring of populations reduces exploitation by non-cooperative signal cheats.ImportanceBacteria communicate via signaling molecules to regulate the expression of a whole range of genes. This process, termed quorum sensing (QS), moderates bacterial metabolism in many environmental conditions, from soil and water (where QS-regulated genes influence nutrient cycling) to animal hosts (where QS-regulated genes determine pathogen virulence). Understanding the ecology of QS could therefore yield vital clues as to how we might modify bacterial behaviour for environmental or clinical gains. Here, we demonstrate that QS signals act as shareable public goods. This means that their evolution, and therefore population-level responses to interference with QS, will be constrained by population structure. Further, we show that environmental structure (constraints on signal diffusion) alters the accessibility of QS signals and demonstrates that we need to consider population and environmental structure to help us further our understanding of QS signaling systems.

scholarly journals Positive Autoregulation of an Acyl-Homoserine Lactone Quorum-Sensing Circuit Synchronizes the Population Response

mBio ◽  
2017 ◽  
Vol 8 (4) ◽  
Author(s):  
Rebecca L. Scholz ◽  
E. Peter Greenberg
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Quorum Sensing ◽  
Biological Significance ◽  
Population Level ◽  
Homoserine Lactone ◽  
Acyl Homoserine Lactone ◽  
Wild Type ◽  
Positive Signal ◽  
Signal Production ◽  
Engineered Strain

ABSTRACTMany proteobacteria utilize acyl-homoserine lactone quorum-sensing signals. At low population densities, cells produce a basal level of signal, and when sufficient signal has accumulated in the surrounding environment, it binds to its receptor, and quorum-sensing-dependent genes can be activated. A common characteristic of acyl-homoserine lactone quorum sensing is that signal production is positively autoregulated. We have examined the role of positive signal autoregulation inPseudomonas aeruginosa. We compared population responses and individual cell responses in populations of wild-typeP. aeruginosato responses in a strain with the signal synthase gene controlled by an arabinose-inducible promoter so that signal was produced at a constant rate per cell regardless of cell population density. At a population level, responses of the wild type and the engineered strain were indistinguishable, but the responses of individual cells in a population of the wild type showed greater synchrony than the responses of the engineered strain. Although sufficient signal is required to activate expression of quorum-sensing-regulated genes, it is not sufficient for activation of certain genes, the late genes, and their expression is delayed until other conditions are met. We found that late gene responses were reduced in the engineered strain. We conclude that positive signal autoregulation is not a required element in acyl-homoserine lactone quorum sensing, but it functions to enhance synchrony of the responses of individuals in a population. Synchrony might be advantageous in some situations, whereas a less coordinated quorum-sensing response might allow bet hedging and be advantageous in other situations.IMPORTANCEThere are many quorum-sensing systems that involve a transcriptional activator, which responds to an acyl-homoserine lactone signal. In all of the examples studied, the gene coding for signal production is positively autoregulated by the signal, and it has even been described as essential for a quorum-sensing response. We have used the opportunistic pathogenPseudomonas aeruginosaas a model to show that positive autoregulation is not required for a robust quorum-sensing response. We also show that positive autoregulation of signal production enhances the synchrony of the response. This information enhances our general understanding of the biological significance of how acyl-homoserine lactone quorum-sensing circuits are arranged.

scholarly journals The Fitness of Pseudomonas aeruginosa Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment

mBio ◽  
2017 ◽  
Vol 8 (3) ◽  
Author(s):  
Anne Mund ◽  
Stephen P. Diggle ◽  
Freya Harrison
Keyword(s):  
Quorum Sensing ◽  
Public Goods ◽  
Population Level ◽  
Bacterial Metabolism ◽  
Signal Molecules ◽  
Wild Type ◽  
Signaling Systems ◽  
Pathogen Virulence ◽  
Environmental Structure ◽  
Animal Hosts

ABSTRACT Experiments examining the social dynamics of bacterial quorum sensing (QS) have focused on mutants which do not respond to signals and the role of QS-regulated exoproducts as public goods. The potential for QS signal molecules to themselves be social public goods has received much less attention. Here, we analyze how signal-deficient (lasI) mutants of the opportunistic pathogen Pseudomonas aeruginosa interact with wild-type cells in an environment where QS is required for growth. We show that when growth requires a “private” intracellular metabolic mechanism activated by the presence of QS signal, lasI mutants act as social cheats and outcompete signal-producing wild-type bacteria in mixed cultures, because they can exploit the signals produced by wild-type cells. However, reducing the ability of signal molecules to diffuse through the growth medium results in signal molecules becoming less accessible to mutants, leading to reduced cheating. Our results indicate that QS signal molecules can be considered social public goods in a way that has been previously described for other exoproducts but that spatial structuring of populations reduces exploitation by noncooperative signal cheats. IMPORTANCE Bacteria communicate via signaling molecules to regulate the expression of a whole range of genes. This process, termed quorum sensing (QS), moderates bacterial metabolism under many environmental conditions, from soil and water (where QS-regulated genes influence nutrient cycling) to animal hosts (where QS-regulated genes determine pathogen virulence). Understanding the ecology of QS could therefore yield vital clues to how we might modify bacterial behavior for environmental or clinical gains. Here, we demonstrate that QS signals act as shareable public goods. This means that their evolution, and therefore population-level responses to interference with QS, will be constrained by population structure. Further, we show that environmental structure (constraints on signal diffusion) alters the accessibility of QS signals and demonstrates that we need to consider population and environmental structure to help us further our understanding of QS signaling systems. IMPORTANCE Bacteria communicate via signaling molecules to regulate the expression of a whole range of genes. This process, termed quorum sensing (QS), moderates bacterial metabolism under many environmental conditions, from soil and water (where QS-regulated genes influence nutrient cycling) to animal hosts (where QS-regulated genes determine pathogen virulence). Understanding the ecology of QS could therefore yield vital clues to how we might modify bacterial behavior for environmental or clinical gains. Here, we demonstrate that QS signals act as shareable public goods. This means that their evolution, and therefore population-level responses to interference with QS, will be constrained by population structure. Further, we show that environmental structure (constraints on signal diffusion) alters the accessibility of QS signals and demonstrates that we need to consider population and environmental structure to help us further our understanding of QS signaling systems.

scholarly journals Quorum Sensing Protects Pseudomonas aeruginosa against Cheating by Other Species in a Laboratory Coculture Model

2015 ◽  
Vol 197 (19) ◽  
pp. 3154-3159 ◽  
Author(s):  
Nicole E. Smalley ◽  
Dingding An ◽  
Matthew R. Parsek ◽  
Josephine R. Chandler ◽  
Ajai A. Dandekar
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Quorum Sensing ◽  
Public Goods ◽  
Public Good ◽  
Hydrogen Cyanide ◽  
Cooperative Behavior ◽  
Bacterial Species ◽  
Cell Communication ◽  
Content Type ◽  
Burkholderia Multivorans

ABSTRACTMany species of bacteria use a cell-cell communication system called quorum sensing (QS) to coordinate group activities. QS systems frequently regulate the production of exoproducts. Some of these products, such as proteases, are “public goods” that are shared among the population and vulnerable to cheating by nonproducing members of the population. Because the QS system of the opportunistic pathogenPseudomonas aeruginosaregulates several public goods, it can serve as a model for studying cooperation. Bacteria also commonly regulate antimicrobial production through QS. In this study, we focused on the hypothesis that QS-regulated antimicrobials may be important forP. aeruginosato protect against cheating by another bacterial species,Burkholderia multivorans.We assessed laboratory cocultures ofP. aeruginosaandB. multivoransand investigated the importance of threeP. aeruginosaQS-regulated antimicrobials, hydrogen cyanide, rhamnolipids, and phenazines, for competition. We found thatP. aeruginosadominates cocultures withB. multivoransand that the three antimicrobials together promoteP. aeruginosacompetitiveness, with hydrogen cyanide contributing the greatest effect. We show that these QS-regulated antimicrobials are also critical forP. aeruginosato preventB. multivoransfrom cheating under nutrient conditions where both species require aP. aeruginosaquorum-regulated protease for growth. Together our results highlight the importance of antimicrobials in protecting cooperating populations from exploitation by other species that can act as cheaters.IMPORTANCECooperative behaviors are threatened by social cheating, wherein individuals do not produce but nonetheless benefit from shared public goods. Bacteria have been shown to use several genetic mechanisms to restrain the emergence of cheaters from within the population, but public goods might also be used by other bacterial species in the vicinity. We demonstrate that a public good produced byPseudomonas aeruginosacan be used by another species,Burkholderia multivorans, to obtain carbon and energy. We also show thatP. aeruginosaantimicrobials that are coregulated with the public good prevent invasion by the cheating species. Our results demonstrate that cross-species cheating can occur and that coregulation of public goods with antimicrobials may stabilize cooperative behavior in mixed microbial communities.

scholarly journals Ecology drives the evolution of diverse siderophore-production strategies in the opportunistic human pathogen Pseudomonas aeruginosa

2021 ◽  
Author(s):  
Alexandre R.T. Figueiredo ◽  
Andreas Wagner ◽  
Rolf Kümmerli
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Quorum Sensing ◽  
Public Goods ◽  
Communication Systems ◽  
Social Evolution ◽  
Iron Starvation ◽  
Evolutionary Forces ◽  
Social Traits ◽  
Selection For ◽  
Opportunistic Human Pathogen

AbstractBacteria often cooperate by secreting molecules that can be shared as public goods between cells. Because the production of public goods is subject to cheating by mutants that exploit the good without contributing to it, there has been great interest in elucidating the evolutionary forces that maintain cooperation. However, little is known on how bacterial cooperation evolves under conditions where cheating is unlikely of importance. Here we use experimental evolution to follow changes in the production of a model public good, the iron-scavenging siderophore pyoverdine, of the bacterium Pseudomonas aeruginosa. After 1200 generations of evolution in nine different environments, we observed that cheaters only reached high frequency in liquid medium with low iron availability. Conversely, when adding iron to reduce the cost of producing pyoverdine, we observed selection for pyoverdine hyper-producers. Similarly, hyper-producers also spread in populations evolved in highly viscous media, where relatedness between interacting individuals is higher. Whole-genome sequencing of evolved clones revealed that hyper-production is associated with mutations/deletions in genes encoding quorum-sensing communication systems, while cheater clones had mutations in the iron-starvation sigma factor or in pyoverdine biosynthesis genes. Our findings demonstrate that bacterial social traits can evolve rapidly in divergent directions, with particularly strong selection for increased levels of cooperation occurring in environments where individual dispersal is reduced, as predicted by social evolution theory. Moreover, we establish a regulatory link between pyoverdine production and quorum-sensing, showing that increased cooperation at one trait (pyoverdine) can be associated with the loss (quorum-sensing) of another social trait.

scholarly journals Deletion of the PA4427-PA4431 Operon of Pseudomonas aeruginosa PAO1 Increased Antibiotics Resistance and Reduced Virulence and Pathogenicity by Affecting Quorum Sensing and Iron Uptake

2021 ◽  
Vol 9 (5) ◽  
pp. 1065
Author(s):  
Lixin Shen ◽  
Lang Gao ◽  
Mengjiao Yang ◽  
Jian Zhang ◽  
Yulu Wang ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Quorum Sensing ◽  
Respiratory Chain ◽  
Chain Complex ◽  
Complex Iii ◽  
Extracellular Polysaccharides ◽  
Antibiotics Resistance ◽  
Bacterial Survival ◽  
Pseudomonas Aeruginosa Pao1 ◽  
Application Potential

The respiratory chain is very important for bacterial survival and pathogenicity, yet the roles of the respiratory chain in P. aeruginosa remain to be fully elucidated. Here, we not only proved experimentally that the operon PA4427-PA4431 of Pseudomonas aeruginosa PAO1 encodes respiratory chain complex III (cytobc1), but also found that it played important roles in virulence and pathogenicity. PA4429–31 deletion reduced the production of the virulence factors, including pyocyanin, rhamnolipids, elastase, and extracellular polysaccharides, and it resulted in a remarkable decrease in pathogenicity, as demonstrated in the cabbage and Drosophila melanogaster infection models. Furthermore, RNA-seq analysis showed that PA4429–31 deletion affected the expression levels of the genes related to quorum-sensing systems and the transport of iron ions, and the iron content was also reduced in the mutant strain. Taken together, we comprehensively illustrated the function of the operon PA4427–31 and its application potential as a treatment target in P. aeruginosa infection.

scholarly journals Protist predation can favour cooperation within bacterial species

2013 ◽  
Vol 9 (5) ◽  
pp. 20130548 ◽  
Author(s):  
Ville-Petri Friman ◽  
Stephen P. Diggle ◽  
Angus Buckling
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Quorum Sensing ◽  
Public Goods ◽  
Trophic Interactions ◽  
Bacterial Species ◽  
Cell Signalling ◽  
Opportunistic Pathogen ◽  
Wild Type ◽  
Floating Cell ◽  
Cell Aggregations

Here, we studied how protist predation affects cooperation in the opportunistic pathogen bacterium Pseudomonas aeruginosa , which uses quorum sensing (QS) cell-to-cell signalling to regulate the production of public goods. By competing wild-type bacteria with QS mutants (cheats), we show that a functioning QS system confers an elevated resistance to predation. Surprisingly, cheats were unable to exploit this resistance in the presence of cooperators, which suggests that resistance does not appear to result from activation of QS-regulated public goods. Instead, elevated resistance of wild-type bacteria was related to the ability to form more predation-resistant biofilms. This could be explained by the expression of QS-regulated resistance traits in densely populated biofilms and floating cell aggregations, or alternatively, by a pleiotropic cost of cheating where less resistant cheats are selectively removed from biofilms. These results show that trophic interactions among species can maintain cooperation within species, and have further implications for P. aeruginosa virulence in environmental reservoirs by potentially enriching the cooperative and highly infective strains with functional QS system.

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