Density‐dependent private benefit leads to bacterial mutualism

Jimenez, Paul; Scheuring, István

doi:10.1111/evo.14241

Cited by 5 publications

(13 citation statements)

References 58 publications

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“…Why is metabolic specialization supported in previous models but not in ours [ 12 , 13 , 17 ]? There are two possible reasons that may explain this.…”

Section: Discussioncontrasting

confidence: 66%

“…The Black Queen Hypothesis predicts that cooperation can be maintained in two main ways: by favoring a strain producing all cooperative goods (a fully producing strain) [ 12 – 14 ] or by favoring different complementary strains, each producing a cooperative good (i.e., metabolic specialization) [ 12 , 13 ]. These two predictions were also found in models that involved constitutive (QS-independent) production of goods.…”

Section: Introductionmentioning

confidence: 99%

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Black Queen Hypothesis, partial privatization, and quorum sensing evolution

2022

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Microorganisms produce costly cooperative goods whose benefit is partially shared with nonproducers, called ‘mixed’ goods. The Black Queen Hypothesis predicts that partial privatization has two major evolutionary implications. First, to favor strains producing several types of mixed goods over nonproducing strains. Second, to favor the maintenance of cooperative traits through different strains instead of having all cooperative traits present in a single strain (metabolic specialization). Despite the importance of quorum sensing regulation of mixed goods, it is unclear how partial privatization affects quorum sensing evolution. Here, we studied the influence of partial privatization on the evolution of quorum sensing. We developed a mathematical population genetics model of an unstructured microbial population considering four strains that differ in their ability to produce an autoinducer (quorum sensing signaling molecule) and a mixed good. Our model assumes that the production of the autoinducers and the mixed goods is constitutive and/or depends on quorum sensing. Our results suggest that, unless autoinducers are costless, partial privatization cannot favor quorum sensing. This result occurs because with costly autoinducers: (1) a strain that produces both autoinducer and goods (fully producing strain) cannot persist in the population; (2) the strain only producing the autoinducer and the strain producing mixed goods in response to the autoinducers cannot coexist, i.e., metabolic specialization cannot be favored. Together, partial privatization might have been crucial to favor a primordial form of quorum sensing—where autoinducers were thought to be a metabolic byproduct (costless)—but not the transition to nowadays costly autoinducers.

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“…Why is metabolic specialization supported in previous models but not in ours [ 12 , 13 , 17 ]? There are two possible reasons that may explain this.…”

Section: Discussioncontrasting

confidence: 66%

Section: Introductionmentioning

confidence: 99%

Black Queen Hypothesis, partial privatization, and quorum sensing evolution

2022

View full text Add to dashboard Cite

show abstract

“…The Black Queen Hypothesis predicts that cooperation can be maintained in two main ways. By favoring a strain producing all cooperative goods (a fully producing strain) [12][13][14] or by favoring different complementary strains, each producing a cooperative good (i.e., metabolic specialization) [12,13]. These two predictions were also found in models that involved constitutively (QSindependent) production of goods.…”

Section: Introductionmentioning

confidence: 72%

“…First, while we have one mixed good and one autoinducer whose production is QSdependent and QS-independent, earlier black queen models had two mixed goods being produced without the regulation by QS. Second, in earlier studies, metabolic specialization might occur because these models assumed that complementary strains are equally fit in their analysis [12,13,17]. While being equally fit is a justifiable assumption when each strain only produces one of two mixed goods, this assumption is unsuitable in our model because one strain only produces the autoinducer (Ag) and the other only the mixed good (aG).…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, whether partially privatized benefits foster QS via metabolic specialization (i.e., via one strain only producing autoinducers and the other only responding to it) is unclear. That is because metabolic specialization has only been demonstrated by mathematical models assuming a costless regulation of two mixed goods (13,14,17). The problem is that while a QSindependent regulation of two mixed goods might be costless, a QS-regulation requires the production of autoinducers, which is costly.…”

Section: Introductionmentioning

confidence: 99%

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Black Queen Hypothesis, partial privatization, and quorum sensing evolution

Souza

Irie

Eda

2022

Preprint

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Microorganisms produce costly cooperative goods whose benefit is partially shared with nonproducers, called ‘mixed’ goods. The Black Queen Hypothesis predicts that partially privatization of benefits from the mixed goods has two major evolutionary implications. First, to favor strains producing several mixed goods over nonproducing strains. Second, to favor the maintenance of cooperative traits through different strains instead of having all cooperative traits present in a single strain (metabolic specialization). Despite the importance of quorum sensing regulation of mixed goods, it is not clear how partial privatization of benefits affects quorum sensing evolution. Here, we studied the influence of partial privatization of benefits on the evolution of quorum sensing. We developed a mathematical population genetics model of an unstructured microbial population considering four strains that differ in their ability to produce an autoinducer (quorum sensing signaling molecule) and a mixed good. Our model assumes that the production of the autoinducers and the mixed goods is constitutive and/or depends on quorum sensing. Our results suggest that partially privatized benefits cannot foster quorum sensing. This result occurs because: (1) a strain that produces both autoinducer and good (fully producing strain) cannot persist in the population; (2) the strain only producing the autoinducer and the strain producing mixed goods in response to the autoinducers cannot coexist, i.e., metabolic specialization cannot be fostered.

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Eco-evolutionary modelling of microbial syntrophy indicates the robustness of cross-feeding over cross-facilitation

Boza

Barabás

Scheuring

et al. 2023

Sci Rep

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Syntrophic cooperation among prokaryotes is ubiquitous and diverse. It relies on unilateral or mutual aid that may be both catalytic and metabolic in nature. Hypotheses of eukaryotic origins claim that mitochondrial endosymbiosis emerged from mutually beneficial syntrophy of archaeal and bacterial partners. However, there are no other examples of prokaryotic syntrophy leading to endosymbiosis. One potential reason is that when externalized products become public goods, they incite social conflict due to selfish mutants that may undermine any mutualistic interactions. To rigorously evaluate these arguments, here we construct a general mathematical framework of the ecology and evolution of different types of syntrophic partnerships. We do so both in a general microbial and in a eukaryogenetic context. Studying the case where partners cross-feed on each other’s self-inhibiting waste, we show that cooperative partnerships will eventually dominate over selfish mutants. By contrast, systems where producers actively secrete enzymes that cross-facilitate their partners’ resource consumption are not robust against cheaters over evolutionary time. We conclude that cross-facilitation is unlikely to provide an adequate syntrophic origin for endosymbiosis, but that cross-feeding mutualisms may indeed have played that role.

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Density‐dependent private benefit leads to bacterial mutualism

Cited by 5 publications

References 58 publications

Black Queen Hypothesis, partial privatization, and quorum sensing evolution

Black Queen Hypothesis, partial privatization, and quorum sensing evolution

Black Queen Hypothesis, partial privatization, and quorum sensing evolution

Eco-evolutionary modelling of microbial syntrophy indicates the robustness of cross-feeding over cross-facilitation

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