Social Evolution Selects for Redundancy in Bacterial Quorum Sensing

Even-Tov, Eran; Bendori, Shira Omer; Valastyan, Julie S.; Ke, Xiaobo; Pollak, Shaul; Bareia, Tasneem; Ben-Zion, Ishay; Bassler, Bonnie L.; Eldar, Avigdor

doi:10.1371/journal.pbio.1002386

Cited by 68 publications

(85 citation statements)

References 49 publications

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“…However, our experimental results demonstrate this is not the case in V. harveyi. The generality of this effect is unknown, and any differences are likely to depend on specific features of the system, such as signal redundancy and stability, within-population heterogeneity, and QS system architecture (38)(39)(40)(41). In this case, conditional PG production provided by QS would act as a proximate mechanism to stabilize cooperation, allowing ultimate stabilizing mechanisms of cooperation, such as kin selection, to act (42).…”

Section: Discussionmentioning

confidence: 99%

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies

Bruger

Waters

2016

Appl Environ Microbiol

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Communication 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 bacterium Vibrio 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 in V. harveyi prevents 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. Cooperative behavior is a widespread phenomenon that pervades all levels of biological organization and has helped to catalyze all major transitions in the history of life (1). Extensive cooperation is also prevalent among microbes and plays fundamental roles in many bacterial processes, including biofilm formation, virulence, bioenergy, host-microbe interactions, and the formation of stable communities that maintain essential ecosystem functions (2-7). One class of microbial cooperative behaviors is the production of public goods (PG), i.e., products that provide benefits to both producers and nonproducers within a community. In the context of PG, individuals that contribute by producing the good are defined as cooperators, while nonproducers are defined as defectors. Importantly, defectors are not always inherently cheaters but are capable of cheating if they reap fitness advantages by exploiting social behaviors (8-10). Conditional participation through phenotyp...

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Section: Discussionmentioning

confidence: 99%

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies

Bruger

Waters

2016

Appl Environ Microbiol

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“…2016). The central hypothesis of this work is that strains that have acquired new QS receptors are selected via facultative cheating.…”

Section: Complexity In Qs Network Architecturementioning

confidence: 99%

Specificity and complexity in bacterial quorum-sensing systems

Hawver

Jung

2016

FEMS Microbiology Reviews

235

161

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Quorum sensing (QS) is a microbial cell-to-cell communication process that relies on the production and detection of chemical signals called autoinducers (AIs) to monitor cell density and species complexity in the population. QS allows bacteria to behave as a cohesive group and coordinate collective behaviors. While most QS receptors display high specificity to their AI ligands, others are quite promiscuous in signal detection. How do specific QS receptors respond to their cognate signals with high fidelity? Why do some receptors maintain low signal recognition specificity? In addition, many QS systems are composed of multiple intersecting signaling pathways: what are the benefits of preserving such a complex signaling network when a simple linear ‘one-to-one’ regulatory pathway seems sufficient to monitor cell density? Here, we will discuss different molecular mechanisms employed by various QS systems that ensure productive and specific QS responses. Moreover, the network architectures of some well-characterized QS circuits will be reviewed to understand how the wiring of different regulatory components achieves different biological goals.

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“…Finally, although we have shown that S. gallinarium induces [ GAR + ] via lactic acid, it is entirely possible that other molecules could also fuel this cross-kingdom interaction in diverse ecological niches. There is also precedent in mechanisms of quorum sensing for competition among inducers secreted by different bacteria (Drescher et al, 2014; Even-Tov et al, 2016). …”

Section: Discussionmentioning

confidence: 99%

A common bacterial metabolite elicits prion-based bypass of glucose repression

Garcia

Dietrich

Clardy

et al. 2016

eLife

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Robust preference for fermentative glucose metabolism has motivated domestication of the budding yeast Saccharomyces cerevisiae. This program can be circumvented by a protein-based genetic element, the [GAR+] prion, permitting simultaneous metabolism of glucose and other carbon sources. Diverse bacteria can elicit yeast cells to acquire [GAR+], although the molecular details of this interaction remain unknown. Here we identify the common bacterial metabolite lactic acid as a strong [GAR+] inducer. Transient exposure to lactic acid caused yeast cells to heritably circumvent glucose repression. This trait had the defining genetic properties of [GAR+], and did not require utilization of lactic acid as a carbon source. Lactic acid also induced [GAR+]-like epigenetic states in fungi that diverged from S. cerevisiae ~200 million years ago, and in which glucose repression evolved independently. To our knowledge, this is the first study to uncover a bacterial metabolite with the capacity to potently induce a prion.DOI: http://dx.doi.org/10.7554/eLife.17978.001

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Social Evolution Selects for Redundancy in Bacterial Quorum Sensing

Cited by 68 publications

References 49 publications

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies

Specificity and complexity in bacterial quorum-sensing systems

A common bacterial metabolite elicits prion-based bypass of glucose repression

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