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Black Queen Hypothesis, partial privatization, and quorum sensing evolution

View ORCID ProfileLucas Santana Souza, View ORCID ProfileYasuhiko Irie, Shigetoshi Eda
doi: https://doi.org/10.1101/2022.03.11.483843
Lucas Santana Souza
1Department of Ecology & Evolutionary Biology, University of Tennessee Knoxville, Knoxville, Tennessee, U. S. A.
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  • ORCID record for Lucas Santana Souza
Yasuhiko Irie
2Division of Pharmacy and Optometry, School of Health Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, U.K.
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Shigetoshi Eda
3Department of Forestry, Wildlife and Fisheries, University of Tennessee Institute of Agriculture, Knoxville, Tennessee, U. S. A
4Department of Microbiology, University of Tennessee Knoxville, Knoxville, Tennessee, U. S. A.
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  • For correspondence: seda@utk.edu
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Abstract

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.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted March 14, 2022.
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Black Queen Hypothesis, partial privatization, and quorum sensing evolution
Lucas Santana Souza, Yasuhiko Irie, Shigetoshi Eda
bioRxiv 2022.03.11.483843; doi: https://doi.org/10.1101/2022.03.11.483843
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Black Queen Hypothesis, partial privatization, and quorum sensing evolution
Lucas Santana Souza, Yasuhiko Irie, Shigetoshi Eda
bioRxiv 2022.03.11.483843; doi: https://doi.org/10.1101/2022.03.11.483843

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