Evolutionary limits to cooperation in microbial communities

Oliveira, Nuno M.; Niehus, René; Foster, Kevin R.

doi:10.1073/pnas.1412673111

Cited by 203 publications

(233 citation statements)

References 68 publications

Supporting

Mentioning

217

Contrasting

Order By: Relevance

“…Although BQ coexistence does not require any form of reciprocity, many of the interactions I have considered here appear to be genuine mutualisms. It has been suggested that BQ evolution provides an engine for generating mutualistic interactions because it stabilizes coexistence long enough for reciprocal mutations to arise in helpers that force beneficiaries to earn their keep [78][79][80]. Briefly, if the helper in a BQ interaction acquired a loss-of-function mutation that made it dependent on a product leaked by its beneficiary, a genuinely mutualistic interaction would have formed ( Figure 5A).…”

Section: Downstream Consequences Of Bq-facilitated Coexistencementioning

confidence: 99%

Black Queen evolution: the role of leakiness in structuring microbial communities

2015

View full text Add to dashboard Cite

Section: Downstream Consequences Of Bq-facilitated Coexistencementioning

confidence: 99%

Black Queen evolution: the role of leakiness in structuring microbial communities

2015

View full text Add to dashboard Cite

“…Moreover, metabolic interactions are often obligatory (Morris et al, 2013). Thus, a cell that has lost its metabolic autonomy might face difficulties to encounter complementary genotypes to supply it with the metabolites that it requires to grow, thereby limiting the potential of cooperative cross-feeding to evolve in natural microbial communities (Oliveira et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments

et al. 2015

View full text Add to dashboard Cite

Metabolic cross-feeding interactions are ubiquitous in natural microbial communities. However, it remains generally unclear whether the production and exchange of metabolites incurs fitness costs to the producing cells and if so, which ecological mechanisms can facilitate a cooperative exchange of metabolites among unrelated individuals. We hypothesized that positive assortment within structured environments can maintain mutualistic cross-feeding. To test this, we engineered Acinetobacter baylyi and Escherichia coli to reciprocally exchange essential amino acids. Interspecific coculture experiments confirmed that non-cooperating types were selectively favoured in spatially unstructured (liquid culture), yet disfavoured in spatially structured environments (agar plates). Both an individual-based model and experiments with engineered genotypes indicated that a segregation of cross-feeders and non-cooperating auxotrophs stabilized cooperative cross-feeding in spatially structured environments. Chemical imaging confirmed that auxotrophs were spatially excluded from cooperative benefits. Together, these results demonstrate that cooperative crossfeeding between different bacterial species is favoured in structured environments such as bacterial biofilms, suggesting this type of interactions might be common in natural bacterial communities.

show abstract

“…Most empirical studies of laboratory and natural populations suggest that QS systems can be invaded and in some cases destabilized, such as the invasion of both Pseudomonas and Vibrio species by QS defectors (20)(21)(22). In fact, the range of conditions under which cooperation is favored may be quite limited (23). This raises the question of why QS frequently regulates the expression of PG and whether it is in fact advantageous for maintaining cooperative traits.…”

mentioning

confidence: 99%

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies

Bruger

Waters

2016

Appl Environ Microbiol

View full text Add to dashboard Cite

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...

show abstract

Evolutionary limits to cooperation in microbial communities

Cited by 203 publications

References 68 publications

Black Queen evolution: the role of leakiness in structuring microbial communities

Black Queen evolution: the role of leakiness in structuring microbial communities

Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies

Contact Info

Product

Resources

About