Black Queen Hypothesis, partial privatization, and quorum sensing evolution

PLOS ONE RESEARCH ARTICLE Black Queen Hypothesis, partial privatization, and quorum sensing evolution Lucas Santana Souza ID1, Yasuhiko Irie2, Shigetoshi Eda ID3,4* 1 Department of Ecology & Evolutionary Biology, University of Tennessee, Knoxville, Tennessee, United States of America, 2 Department of Physics, Chemistry, and Biology, Linköping University, Linköping, Sweden, 3 Department of Forestry, Wildlife and Fisheries, University of Tennessee Institute of Agriculture, Knoxville, Tennessee, United States of America, 4 Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Souza LS, Irie Y, Eda S (2022) Black Queen Hypothesis, partial privatization, and quorum sensing evolution. PLoS ONE 17(11): e0278449. https://doi.org/10.1371/journal. pone.0278449 Editor: Tiffany B. Taylor, University of Bath, UNITED KINGDOM Received: May 13, 2022 Accepted: November 16, 2022 Published: November 30, 2022 Copyright: © 2022 Souza et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Abstract 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. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by a grant from the Conselho Nacional de Desenvolvimento Cientı́fico e Tecnológico (CNPq <https://www.gov. br/cnpq/pt-br>; Ciência sem Fronteiras scholarship; grant no. 219104/2014-0 to LSS). The sponsor did not play any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. 1 Introduction The maintenance of microbial strains producing costly beneficial goods (cooperators) is challenging to explain because nonproducing strains (cheaters) are expected to outcompete producing strains [1, 2] by taking advantage of the benefits of goods without paying the cost of producing goods. Growing evidence shows that benefits are not always equally shared among PLOS ONE | https://doi.org/10.1371/journal.pone.0278449 November 30, 2022 1 / 21 PLOS ONE Competing interests: The authors have declared that no competing interests exist. Black Queen Hypothesis, partial privatization, and quorum sensing evolution producers and nonproducers [3–5]. These goods, providing privatized and public benefits, have been called “mixed” goods [6]. Morris et al. proposed the Black Queen Hypothesis which predicts that the growth of mixed good producers is favored over that of nonproducers whenever the privatized benefits offset the costs of producing goods [3–5, 7]. The production of mixed goods is regulated by the population density-dependent [8] (and/ or frequency-dependent [9]) gene regulation of bacteria, called quorum sensing (QS) and/or a QS-independent mechanism. One example of mixed goods is pyoverdine, an iron-scavenging siderophores of Pseudomonas aeruginosa [7, 10, 11]. The benefit of siderophore is partially privatized as only a proportion of the molecules is secreted from the bacteria [7, 10]. The partially secreted siderophore provides benefits to nonproducing strains. Another mechanism of partial privatization includes the intracellular cleavage of sucrose into monosaccharides. Some monosaccharides remain within the cell, i.e., they are privatized, and others leak into the extracellular environment [3]. 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. However, despite evidence that QS regulates mixed goods [7, 10], no model analyzed whether these two predictions are valid for QS evolution. There are two reasons for why it is unclear whether partially privatized benefits can favor QS via a fully producing strain which produces both QS signaling molecules (autoinducers) and goods. First, while QS-independent regulation of mixed goods might be costless, QS-regulation itself is costly. Thus, if a mixed good is regulated by a costless, QS-independent mechanism (e.g., constitutively produced), then benefits only need to offset the mixed goods’ costs [3]. However, when mixed goods are QS regulated, privatized benefits need to offset not only the costs of mixed goods but also autoinducers’ cost. Second, experiments that involve QS regulation of a mixed good have successfully shown that the partially privatized benefits suppress the invasion of strains that are not producing mixed goods [15]. The problem is that these studies focus on the interactions between two strains, which might not reflect the case when more than two strains are present [16]. Thus, it is not clear whether partial privatization supports the growth of a fully producing strain. Additionally, whether partial privatization favors QS via metabol (...truncated)