scholarly journals Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies

2016 ◽  
Vol 82 (22) ◽  
pp. 6498-6506 ◽  
Author(s):  
Eric L. Bruger ◽  
Christopher M. Waters
Keyword(s):  
Growth Rate ◽  
Quorum Sensing ◽  
Experimental Evidence ◽  
Fundamental Problem ◽  
Growth Yield ◽  
Cellular Growth ◽  
Growth Strategies ◽  
High Cell ◽  
Content Type ◽  
Cell Densities

ABSTRACTCommunication has been suggested as a mechanism to stabilize cooperation. In bacteria, chemical communication, termed quorum sensing (QS), has been hypothesized to fill this role, and extracellular public goods are often induced by QS at high cell densities. Here we show, with the bacteriumVibrio harveyi, that QS provides strong resistance against invasion of a QS defector strain by maximizing the cellular growth rate at low cell densities while achieving maximum productivity through protease upregulation at high cell densities. In contrast, QS mutants that act as defectors or unconditional cooperators maximize either the growth rate or the growth yield, respectively, and thus are less fit than the wild-type QS strain. Our findings provide experimental evidence that regulation mediated by microbial communication can optimize growth strategies and stabilize cooperative phenotypes by preventing defector invasion, even under well-mixed conditions. This effect is due to a combination of responsiveness to environmental conditions provided by QS, lowering of competitive costs when QS is not induced, and pleiotropic constraints imposed on defectors that do not perform QS.IMPORTANCECooperation is a fundamental problem for evolutionary biology to explain. Conditional participation through phenotypic plasticity driven by communication is a potential solution to this dilemma. Thus, among bacteria, QS has been proposed to be a proximate stabilizing mechanism for cooperative behaviors. Here, we empirically demonstrate that QS inV. harveyiprevents cheating and subsequent invasion by nonproducing defectors by maximizing the growth rate at low cell densities and the growth yield at high cell densities, whereas an unconditional cooperator is rapidly driven to extinction by defectors. Our findings provide experimental evidence that QS regulation prevents the invasion of cooperative populations by QS defectors even under unstructured conditions, and they strongly support the role of communication in bacteria as a mechanism that stabilizes cooperative traits.

The intra-genus and inter-species quorum-sensing autoinducers exert distinct control over Vibrio cholerae biofilm formation and dispersal

2019 ◽  
Author(s):  
Andrew A. Bridges ◽  
Bonnie L. Bassler
Keyword(s):  
Quorum Sensing ◽  
Vibrio Cholerae ◽  
Cell Density ◽  
Biofilm Formation ◽  
Specific Information ◽  
High Cell ◽  
Coincidence Detector ◽  
Sensing System ◽  
Quorum Sensing System ◽  
Cell Densities

AbstractVibrio cholerae possesses multiple quorum-sensing systems that control virulence and biofilm formation among other traits. At low cell densities, when quorum-sensing autoinducers are absent, V. cholerae forms biofilms. At high cell densities, when autoinducers have accumulated, biofilm formation is repressed and dispersal occurs. Here, we focus on the roles of two well-characterized quorum-sensing autoinducers that function in parallel. One autoinducer, called CAI-1, is used to measure vibrio abundance, and the other autoinducer, called AI-2, is a broadly-made universal autoinducer that is presumed to enable V. cholerae to assess the total bacterial cell density of the vicinal community. The two V. cholerae autoinducers funnel information into a shared signal relay pathway. This feature of the quorum-sensing system architecture has made it difficult to understand how specific information can be extracted from each autoinducer, how the autoinducers might drive distinct output behaviors, and in turn, how the bacteria use quorum sensing to distinguish self from other in bacterial communities. We develop a live-cell biofilm formation and dispersal assay that allows examination of the individual and combined roles of the two autoinducers in controlling V. cholerae behavior. We show that the quorum-sensing system works as a coincidence detector in which both autoinducers must be present simultaneously for repression of biofilm formation to occur. Within that context, the CAI-1 quorum-sensing pathway is activated when only a few V. cholerae cells are present, whereas the AI-2 pathway is activated only at much higher cell density. The consequence of this asymmetry is that exogenous sources of AI-2, but not CAI-1, contribute to satisfying the coincidence detector to repress biofilm formation and promote dispersal. We propose that V. cholerae uses CAI-1 to verify that some of its kin are present before committing to the high-cell-density quorum-sensing mode, but it is, in fact, the universal autoinducer AI-2, that sets the pace of the V. cholerae quorum-sensing program. This first report of unique roles for the different V. cholerae autoinducers suggests that detection of self fosters a distinct outcome from detection of other.

scholarly journals Sociality in Escherichia coli: Enterochelin Is a Private Good at Low Cell Density and Can Be Shared at High Cell Density

2015 ◽  
Vol 197 (13) ◽  
pp. 2122-2128 ◽  
Author(s):  
Rebecca L. Scholz ◽  
E. Peter Greenberg
Keyword(s):  
Escherichia Coli ◽  
Cell Density ◽  
Iron Acquisition ◽  
Partial Privatization ◽  
High Cell ◽  
Wild Type ◽  
Content Type ◽  
Cell Densities ◽  
The Cost ◽  
Low Cell Density

ABSTRACTMany bacteria produce secreted iron chelators called siderophores, which can be shared among cells with specific siderophore uptake systems regardless of whether the cell produces siderophores. Sharing secreted products allows freeloading, where individuals use resources without bearing the cost of production. Here we show that theEscherichia colisiderophore enterochelin is not evenly shared between producers and nonproducers. Wild-typeEscherichia coligrows well in low-iron minimal medium, and an isogenic enterochelin synthesis mutant (ΔentF) grows very poorly. The enterochelin mutant grows well in low-iron medium supplemented with enterochelin. At high cell densities the ΔentFmutant can compete equally with the wild type in low-iron medium. At low cell densities the ΔentFmutant cannot compete. Furthermore, the growth rate of the wild type is unaffected by cell density. The wild type grows well in low-iron medium even at very low starting densities. Our experiments support a model where at least some enterochelin remains associated with the cells that produce it, and the cell-associated enterochelin enables iron acquisition even at very low cell density. Enterochelin that is not retained by producing cells at low density is lost to dilution. At high cell densities, cell-free enterochelin can accumulate and be shared by all cells in the group. Partial privatization is a solution to the problem of iron acquisition in low-iron, low-cell-density habitats. Cell-free enterochelin allows for iron scavenging at a distance at higher population densities. Our findings shed light on the conditions under which freeloaders might benefit from enterochelin uptake systems.IMPORTANCESociality in microbes has become a topic of great interest. One facet of sociality is the sharing of secreted products, such as the iron-scavenging siderophores. We present evidence that theEscherichia colisiderophore enterochelin is relatively inexpensive to produce and is partially privatized such that it can be efficiently shared only at high producer cell densities. At low cell densities, cell-free enterochelin is scarce and only enterochelin producers are able to grow in low-iron medium. Because freely shared products can be exploited by freeloaders, this partial privatization may help explain how enterochelin production is stabilized inE. coliand may provide insight into when enterochelin is available for freeloaders.

scholarly journals Transcriptome-Based Analysis of the Pantoea stewartii Quorum-Sensing Regulon and Identification of EsaR Direct Targets

2014 ◽  
Vol 80 (18) ◽  
pp. 5790-5800 ◽  
Author(s):  
Revathy Ramachandran ◽  
Alison Kernell Burke ◽  
Guy Cormier ◽  
Roderick V. Jensen ◽  
Ann M. Stevens
Keyword(s):  
Quorum Sensing ◽  
Cell Envelope ◽  
Regulatory Protein ◽  
Homoserine Lactone ◽  
Sequencing Analysis ◽  
Mobility Shift ◽  
Content Type ◽  
Proteomic Approach ◽  
Stewart's Wilt ◽  
Cell Densities

ABSTRACTPantoeastewartiisubsp.stewartiiis a proteobacterium that causes Stewart's wilt disease in corn plants. The bacteria form a biofilm in the xylem of infected plants and produce capsule that blocks water transport, eventually causing wilt. At low cell densities, the quorum-sensing (QS) regulatory protein EsaR is known to directly repress expression ofesaRitself as well as the genes for the capsular synthesis operon transcription regulator,rcsA, and a 2,5-diketogluconate reductase,dkgA. It simultaneously directly activates expression of genes for a putative small RNA,esaS, the glycerol utilization operon,glpFKX, and another transcriptional regulator,lrhA. At high bacterial cell densities, all of this regulation is relieved when EsaR binds an acylated homoserine lactone signal, which is synthesized constitutively over growth. QS-dependent gene expression is critical for the establishment of disease in the plant. However, the identity of the full set of genes controlled by EsaR/QS is unknown. A proteomic approach previously identified around 30 proteins in the QS regulon. In this study, a whole-transcriptome, next-generation sequencing analysis of rRNA-depleted RNA from QS-proficient and -deficientP. stewartiistrains was performed to identify additional targets of EsaR. EsaR-dependent transcriptional regulation of a subset of differentially expressed genes was confirmed by quantitative reverse transcription-PCR (qRT-PCR). Electrophoretic mobility shift assays demonstrated that EsaR directly bound 10 newly identified target promoters. Overall, the QS regulon ofP. stewartiiorchestrates three major physiological responses: capsule and cell envelope biosynthesis, surface motility and adhesion, and stress response.

scholarly journals The Fur-Iron Complex Modulates Expression of the Quorum-Sensing Master Regulator, SmcR, To Control Expression of Virulence Factors in Vibrio vulnificus

2013 ◽  
Vol 81 (8) ◽  
pp. 2888-2898 ◽  
Author(s):  
In Hwang Kim ◽  
Yancheng Wen ◽  
Jee-Soo Son ◽  
Kyu-Ho Lee ◽  
Kun-Soo Kim
Keyword(s):  
Quorum Sensing ◽  
Cell Density ◽  
Virulence Factors ◽  
Vibrio Vulnificus ◽  
High Cell Density ◽  
Iron Complex ◽  
High Cell ◽  
Mobility Shift ◽  
Master Regulator ◽  
Content Type

ABSTRACTThe genevvpE, encoding the virulence factor elastase, is a member of the quorum-sensing regulon inVibrio vulnificusand displays enhanced expression at high cell density. We observed that this gene was repressed under iron-rich conditions and that the repression was due to a Fur (ferricuptakeregulator)-dependent repression ofsmcR, a gene encoding a quorum-sensing master regulator with similarity toluxRinVibrio harveyi. A gel mobility shift assay and a footprinting experiment demonstrated that the Fur-iron complex binds directly to two regions upstream ofsmcR(−82 to −36 and −2 to +27, with respect to the transcription start site) with differing affinities. However, binding of the Fur-iron complex is reversible enough to allow expression ofsmcRto be induced by quorum sensing at high cell density under iron-rich conditions. Under iron-limiting conditions, Fur fails to bind either region and the expression ofsmcRis regulated solely by quorum sensing. These results suggest that two biologically important environmental signals, iron and quorum sensing, converge to direct the expression ofsmcR, which then coordinates the expression of virulence factors.

scholarly journals The Quorum Sensing Regulator CinR Hierarchically Regulates Two Other Quorum Sensing Pathways in Ligand-Dependent and -Independent Fashions in Rhizobium etli

2015 ◽  
Vol 197 (9) ◽  
pp. 1573-1581 ◽  
Author(s):  
Huiming Zheng ◽  
Yiling Mao ◽  
Qingcheng Zhu ◽  
Jun Ling ◽  
Na Zhang ◽  
...  
Keyword(s):  
Quorum Sensing ◽  
Homoserine Lactone ◽  
Nodule Formation ◽  
Rhizobium Etli ◽  
Wild Type ◽  
Content Type ◽  
Nitrogen Fixation Activity ◽  
Regulatory Cascade ◽  
Regulatory Systems ◽  
Cell Densities

ABSTRACTMany rhizobial species use complexN-acyl-homoserine lactone (AHL)-based quorum sensing (QS) systems to monitor their population density and regulate their symbiotic interactions with their plant hosts. There are at least three LuxRI-type regulatory systems inRhizobium etliCFN42: CinRI, RaiRI, and TraRI. In this study, we show that CinI, RaiI, and TraI are responsible for synthesizing all AHLs under the tested conditions. The activation of these AHL synthase genes requires their corresponding LuxR-type counterparts. We further demonstrate that CinRI is at the top of the regulatory cascade that activates RaiRI and TraRI QS systems. Moreover, we discovered that CinR possesses a specific affinity to bindcinIpromoter in the absence of its cognate AHL ligand, thereby activatingcinItranscription. Addition of AHLs leads to improved binding to thecinIpromoter and enhancedcinIexpression. Furthermore, we found that compared to the wild type, thecinRmutation displayed reduced nodule formation, andcinR,raiR, andtraImutants show significantly lower levels of nitrogen fixation activity than the wild type. These results suggest that the complex QS regulatory systems inR. etliplay an important role in its symbiosis with legume hosts.IMPORTANCEMany bacteria use quorum sensing (QS) to monitor their cell densities and coordinately regulate a number of physiological functions. Rhizobia often have diverse and complex LuxR/LuxI-type quorum sensing systems that may be involved in symbiosis and N2fixation. In this study, we identified three LuxR/LuxI-type QS systems inRhizobium etliCFN42: CinRI, RaiRI, and TraRI. We established a complex network of regulation between these QS components and found that these QS systems played important roles in symbiosis processes.

scholarly journals Experimental Evidence for Adaptation to Species-Specific Gut Microbiota in House Mice

mSphere ◽  
2019 ◽  
Vol 4 (4) ◽  
Author(s):  
Andrew H. Moeller ◽  
João C. Gomes-Neto ◽  
Sara Mantz ◽  
Hatem Kittana ◽  
Rafael R. Segura Munoz ◽  
...  
Keyword(s):  
Growth Rate ◽  
Gut Microbiota ◽  
Experimental Evidence ◽  
House Mouse ◽  
Phylogenetic Analyses ◽  
Mammalian Species ◽  
Content Type ◽  
Inflammatory Protein ◽  
Species Specific ◽  
The Impact

ABSTRACT The gut microbial communities of mammals have codiversified with host species, and changes in the gut microbiota can have profound effects on host fitness. Therefore, the gut microbiota may drive adaptation in mammalian species, but this possibility is underexplored. Here, we show that the gut microbiota has codiversified with mice in the genus Mus over the past ∼6 million years, and we present experimental evidence that the gut microbiota has driven adaptive evolution of the house mouse, Mus musculus domesticus. Phylogenetic analyses of metagenome-assembled bacterial genomic sequences revealed that gut bacterial lineages have been retained within and diversified alongside Mus species over evolutionary time. Transplantation of gut microbiotas from various Mus species into germfree M. m. domesticus showed that foreign gut microbiotas slowed growth rate and upregulated macrophage inflammatory protein in hosts. These results suggest adaptation by M. m. domesticus to its gut microbiota since it diverged from other Mus species. IMPORTANCE The communities of bacteria that reside within mammalian guts are deeply integrated with their hosts, but the impact of this gut microbiota on mammalian evolution remains poorly understood. Experimental transplantation of the gut microbiota between mouse species revealed that foreign gut microbiotas lowered the host growth rate and upregulated the expression of an immunomodulating cytokine. In addition, foreign gut microbiotas increased host liver sizes and attenuated sex-specific differences in host muscle and fat content. These results suggest that the house mouse has adapted to its species-specific gut microbiota.

scholarly journals High cell densities favor lysogeny: induction of an H20 prophage is repressed by quorum sensing and enhances biofilm formation in Vibrio anguillarum

2020 ◽  
Vol 14 (7) ◽  
pp. 1731-1742 ◽  
Author(s):  
Demeng Tan ◽  
Mads Frederik Hansen ◽  
Luís Nunes de Carvalho ◽  
Henriette Lyng Røder ◽  
Mette Burmølle ◽  
...  
Keyword(s):  
Quorum Sensing ◽  
Biofilm Formation ◽  
Vibrio Anguillarum ◽  
High Cell ◽  
Cell Densities

scholarly journals Proteomic Analysis of the Quorum-Sensing Regulon in Pantoea stewartii and Identification of Direct Targets of EsaR

2013 ◽  
Vol 79 (20) ◽  
pp. 6244-6252 ◽  
Author(s):  
Revathy Ramachandran ◽  
Ann M. Stevens
Keyword(s):  
Quorum Sensing ◽  
Proteomic Analysis ◽  
Homoserine Lactone ◽  
Mobility Shift ◽  
Content Type ◽  
Pantoea Stewartii ◽  
Reverse Transcription Pcr ◽  
Glycerol Facilitator ◽  
Stewart's Wilt ◽  
Cell Densities

ABSTRACTThe proteobacteriumPantoea stewartiisubsp.stewartiicauses Stewart's wilt disease in maize when it colonizes the xylem and secretes large amounts of stewartan, an exopolysaccharide. The success of disease pathogenesis lies in the timing of bacterial virulence factor expression through the different stages of infection. Regulation is achieved through a quorum-sensing (QS) system consisting of the acyl-homoserine lactone (AHL) synthase, EsaI, and the transcription regulator EsaR. At low cell densities, EsaR represses transcription of itself and ofrcsA, an activator of the stewartan biosynthesis operon; it also activatesesaS, which encodes a small RNA (sRNA). Repression or activation ceases at high cell densities when EsaI synthesizes sufficient levels of the AHL ligandN-3-oxo-hexanoyl-l-homoserine lactone to bind and inactivate EsaR. This study aims to identify other genes activated or repressed by EsaR during the QS response. Proteomic analysis identified a QS regulon of more than 30 proteins. Electrophoretic mobility shift assays of promoters of genes encoding differentially expressed proteins distinguished direct targets of EsaR from indirect targets. Additional quantitative reverse transcription-PCR (qRT-PCR) and DNA footprinting analysis established that EsaR directly regulates the promoters ofdkgA,glpF, andlrhA. The proteins encoded bydkgA,glpF, andlrhAare a 2,5-diketogluconate reductase, glycerol facilitator, and transcriptional regulator of chemotaxis and motility, respectively, indicating a more global QS response inP. stewartiithan previously recognized.

scholarly journals The In Planta Transcriptome of Ralstonia solanacearum: Conserved Physiological and Virulence Strategies during Bacterial Wilt of Tomato

mBio ◽  
2012 ◽  
Vol 3 (4) ◽  
Author(s):  
Jonathan M. Jacobs ◽  
Lavanya Babujee ◽  
Fanhong Meng ◽  
Annett Milling ◽  
Caitilyn Allen
Keyword(s):  
Bacterial Wilt ◽  
Ralstonia Solanacearum ◽  
High Cell ◽  
In Planta ◽  
Bacterial Gene ◽  
Content Type ◽  
Xylem Fluid ◽  
Bacterial Gene Expression ◽  
Weed Host ◽  
Cell Densities

ABSTRACTPlant xylem fluid is considered a nutrient-poor environment, but the bacterial wilt pathogenRalstonia solanacearumis well adapted to it, growing to 108to 109 CFU/g tomato stem. To better understand howR. solanacearumsucceeds in this habitat, we analyzed the transcriptomes of two phylogenetically distinctR. solanacearumstrains that both wilt tomato, strains UW551 (phylotype II) and GMI1000 (phylotype I). We profiled bacterial gene expression at ~6 × 108 CFU/ml in culture or in plant xylem during early tomato bacterial wilt pathogenesis. Despite phylogenetic differences, these two strains expressed their 3,477 common orthologous genes in generally similar patterns, with about 12% of their transcriptomes significantly alteredin plantaversus in rich medium. Several primary metabolic pathways were highly expressed during pathogenesis. These pathways included sucrose uptake and catabolism, and components of these pathways were encoded by genes in thescrABYcluster. A UW551scrAmutant was significantly reduced in virulence on resistant and susceptible tomato as well as on potato and the epidemiologically important weed hostSolanum dulcamara. FunctionalscrAcontributed to pathogen competitive fitness during colonization of tomato xylem, which contained ~300 µM sucrose.scrAexpression was induced by sucrose, but to a much greater degree by growthin planta. Unexpectedly, 45% of the genes directly regulated by HrpB, the transcriptional activator of the type 3 secretion system (T3SS), were upregulatedin plantaat high cell densities. This result modifies a regulatory model based on bacterial behavior in culture, where this key virulence factor is repressed at high cell densities. The active transcription of these genes in wilting plants suggests that T3SS has a biological role throughout the disease cycle.IMPORTANCERalstonia solanacearumis a widespread plant pathogen that causes bacterial wilt disease. It inflicts serious crop losses on tropical farmers, with major economic and human consequences. It is also a model for the many destructive microbes that colonize the water-conducting plant xylem tissue, which is low in nutrients and oxygen. We extracted bacteria from infected tomato plants and globally identified the biological functions thatR. solanacearumexpresses during plant pathogenesis. This revealed the unexpected presence of sucrose in tomato xylem fluid and the pathogen’s dependence on host sucrose for virulence on tomato, potato, and the common weed bittersweet nightshade. Further,R. solanacearumwas highly responsive to the plant environment, expressing several metabolic and virulence functions quite differently in the plant than in pure culture. These results reinforce the utility of studying pathogens in interaction with hosts and suggest that selecting for reduced sucrose levels could generate wilt-resistant crops.

scholarly journals Optimal strategy for public good production is set by balancing intertemporal trade-off between population growth rate and carrying capacity

2021 ◽  
Author(s):  
Manasi S. Gangan ◽  
Marcos M. Vasconcelos ◽  
Urbashi Mitra ◽  
Odilon Camara ◽  
James Q Boedicker
Keyword(s):  
Growth Rate ◽  
Quorum Sensing ◽  
Public Goods ◽  
Public Good ◽  
Cell Density ◽  
Carrying Capacity ◽  
Cellular Growth ◽  
Logistic Growth ◽  
Trade Off ◽  
Good Production

Public goods are biomolecules that contribute to the community welfare. Their production can benefit populations in many ways, such as by providing access to previously unutilized resources. However, public good production has often been energetically costly, resulting in a reduction in the cellular growth rate. To reduce this cost, populations have evolved strategies to regulate biosynthesis of public good. Among these cell densities dependent regulation of public goods, as accomplished by quorum sensing, is a widely studied mechanism. Given that the fitness costs and benefits of public good production must be balanced, adoption of quorum sensing as a regulatory pathway by bacterial cells may have parallels with several economic principles that are used to study optimal investment decisions. Here, we explore the regulation of a public good, whose benefit is an increase in the carrying capacity, through experimental measurements of growth for engineered strains of Escherichia coli and analysis of those results using a modified logistic growth model. By varying the cell density at which the production of the public good was activated, we showed sharply-peaked optimum population fitness. Analysis further revealed that cell density associated with maximum public good benefits was determined by the trade-off between the cost of public good production, in terms of reduced growth rate, and benefits received from public good, in the form of increased carrying capacity. Moreover, our model showed that cells with luxRI quorum sensing seem to upregulate public good expression when the benefits from the production was immediate. These results demonstrate a case where a biological system apparently has evolved to optimize the timing of public good production to account for short-term costs and delays in reaping a future benefit.

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