Black Queen Hypothesis, partial privatization, and quorum sensing evolution

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 nonpr...

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Main Authors: Lucas Santana Souza, Yasuhiko Irie, Shigetoshi Eda
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9710793/?tool=EBI
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author Lucas Santana Souza
Yasuhiko Irie
Shigetoshi Eda
author_facet Lucas Santana Souza
Yasuhiko Irie
Shigetoshi Eda
author_sort Lucas Santana Souza
collection DOAJ
description 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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spelling doaj.art-63f3c617346a44ea8f5f6b92cc3045d62022-12-22T04:21:58ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-011711Black Queen Hypothesis, partial privatization, and quorum sensing evolutionLucas Santana SouzaYasuhiko IrieShigetoshi EdaMicroorganisms 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.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9710793/?tool=EBI
spellingShingle Lucas Santana Souza
Yasuhiko Irie
Shigetoshi Eda
Black Queen Hypothesis, partial privatization, and quorum sensing evolution
PLoS ONE
title Black Queen Hypothesis, partial privatization, and quorum sensing evolution
title_full Black Queen Hypothesis, partial privatization, and quorum sensing evolution
title_fullStr Black Queen Hypothesis, partial privatization, and quorum sensing evolution
title_full_unstemmed Black Queen Hypothesis, partial privatization, and quorum sensing evolution
title_short Black Queen Hypothesis, partial privatization, and quorum sensing evolution
title_sort black queen hypothesis partial privatization and quorum sensing evolution
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9710793/?tool=EBI
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