EXPLORING THE SOCIOBIOLOGY OF PYOVERDIN-PRODUCING<i>PSEUDOMONAS</i>

Zhang, Xuexian; Rainey, Paul B.

doi:10.1111/evo.12183

Cited by 86 publications

(123 citation statements)

References 86 publications

(207 reference statements)

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“…In contrast to this pattern, we observed further degradation of pyoverdine production in the pvdS_prom background almost exclusively in iron-rich environments regardless of spatial structure. Because pyoverdine is not needed under iron-rich conditions, yet still expressed in low amounts [14,25], we assume that selection against pyoverdine production represents the erosion of an unnecessary trait.…”

Section: Discussionmentioning

confidence: 99%

The path to re-evolve cooperation is constrained inPseudomonas aeruginosa

Granato

Kümmerli

2017

Preprint

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Background: A common form of cooperation in bacteria is based on the secretion of beneficial metabolites, shareable as public good among cells within a group. Because cooperation can be exploited by "cheating" mutants, which contribute less or nothing to the public good, there has been great interest in understanding the conditions required for cooperation to remain evolutionarily stable. In contrast, much less is known about whether cheats, once fixed in the population, are able to revert back to cooperation when conditions change. Here, we tackle this question by subjecting experimentally evolved cheats of Pseudomonas aeruginosa, partly deficient for the production of the iron-scavenging public good pyoverdine, to conditions previously shown to favor cooperation. Results: Following approximately 200 generations of experimental evolution, we screened 720 evolved clones for changes in their pyoverdine production levels. We found no evidence for the re-evolution of full cooperation, even in environments with increased spatial structure, and reduced costs of public good production -two conditions that have previously been shown to maintain cooperation. In contrast, we observed selection for complete abolishment of pyoverdine production. The patterns of complete trait degradation were likely driven by "cheating on cheats" in unstructured, iron-limited environments where pyoverdine is important for growth, and selection against a maladaptive trait in iron-rich environments where pyoverdine is superfluous.

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Section: Discussionmentioning

confidence: 99%

The path to re-evolve cooperation is constrained inPseudomonas aeruginosa

Granato

Kümmerli

2017

Preprint

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“…In many ecological situations, bacteria form complex, tightly packed, and spatially structured colonies, such as biofilms, where public good dispersal may be severely reduced compared with planktonic cultures. This raises the questions of how public good molecules circulate between cells in these natural conditions and how cooperation is affected by the population structure (8,(13)(14)(15). Experimental realizations of limited public good dispersal were obtained by tuning the viscosity (16), the distance between colonies of producers and nonproducers (17), or the amount of cell attachment (18).…”

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confidence: 99%

“…In liquid conditions, mutants that do not produce siderophores have, in fact, been shown to outcompete WT strains (5)(6)(7)(8). However, the limited spatial dispersal of public goods can challenge this picture and has been proposed as a general mechanism for explaining the maintenance of cooperation (8)(9)(10)(11)(12). When dispersal is limited, public good molecules tend to stay in the vicinity of the producing subpopulations, allowing them to benefit preferentially from their own production, and thus to balance the advantage of opportunistic nonproducing strains.…”

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confidence: 99%

Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies

Julou

Mora

Guillon

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

134

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The maintenance of cooperation in populations where public goods are equally accessible to all but inflict a fitness cost on individual producers is a long-standing puzzle of evolutionary biology. An example of such a scenario is the secretion of siderophores by bacteria into their environment to fetch soluble iron. In a planktonic culture, these molecules diffuse rapidly, such that the same concentration is experienced by all bacteria. However, on solid substrates, bacteria form dense and packed colonies that may alter the diffusion dynamics through cell-cell contact interactions. In Pseudomonas aeruginosa microcolonies growing on solid substrate, we found that the concentration of pyoverdine, a secreted iron chelator, is heterogeneous, with a maximum at the center of the colony. We quantitatively explain the formation of this gradient by local exchange between contacting cells rather than by global diffusion of pyoverdine. In addition, we show that this local trafficking modulates the growth rate of individual cells. Taken together, these data provide a physical basis that explains the stability of public goods production in packed colonies.biofilm | evolution | noise | variability | ecology I ron is required for many enzymatic processes, and is therefore an essential nutrient. To overcome the low abundance of free iron in aerobic environments, bacteria, as well as other microorganisms, synthesize and secrete iron-chelating molecules called siderophores (1). Once released in the extracellular environment, siderophores diffuse and complex with iron. Because other bacteria can import them, siderophores can be regarded as public goods (2) and siderophore secretion is often cited as a model system for studying the stability of cooperation (3, 4). In this context, nonproducing mutants, which can enjoy the benefit of siderophores without bearing the cost of their production, have a selective advantage over the WT-producing strain and could, in principle, displace them on evolutionary time scales.This argument usually assumes that public good molecules are readily available to all, as is the case in planktonic cultures, where molecules diffuse freely and rapidly between cells. In liquid conditions, mutants that do not produce siderophores have, in fact, been shown to outcompete WT strains (5-8). However, the limited spatial dispersal of public goods can challenge this picture and has been proposed as a general mechanism for explaining the maintenance of cooperation (8-12). When dispersal is limited, public good molecules tend to stay in the vicinity of the producing subpopulations, allowing them to benefit preferentially from their own production, and thus to balance the advantage of opportunistic nonproducing strains. In many ecological situations, bacteria form complex, tightly packed, and spatially structured colonies, such as biofilms, where public good dispersal may be severely reduced compared with planktonic cultures. This raises the questions of how public good molecules circulate between cells in these natur...

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“…However, the study of microbes also poses significant challenges, foremost among which is a lack of knowledge of the ecological context under which the supposedly cooperative trait has evolved and is maintained (O'Brien and Brockhurst, 2015;Rainey, 2015;Zhang and Rainey, 2013). Here, ecology encapsulates both the biotic (interactions among organisms) and the abiotic (interactions between organisms and their environment) dimensions (see Glossary).…”

Section: Introductionmentioning

confidence: 99%

“…Here, ecology encapsulates both the biotic (interactions among organisms) and the abiotic (interactions between organisms and their environment) dimensions (see Glossary). When seemingly cooperative and cheating traits have been studied in different ecological contexts, a variety of genotypeby-environment interactions have been found that have questioned the appropriateness of sociobiological labels (Driscoll et al, 2011;Dubravcic et al, 2014;Redfield, 2002;Tarnita et al, 2015;Zhang and Rainey, 2013). Moreover, the rapid evolutionary pace also entails that traits can be selected for on a fast timescale that affects the ecology of the microbes, from intraspecific and interspecific interactions to the level of the ecosystem (Lennon and Denef, 2015), leading to crucial ecoevolutionary feedback.…”

Section: Introductionmentioning

confidence: 99%

The ecology and evolution of social behavior in microbes

Tarnita

2017

Journal of Experimental Biology

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Cooperation has been studied extensively across the tree of life, from eusociality in insects to social behavior in humans, but it is only recently that a social dimension has been recognized and extensively explored for microbes. Research into microbial cooperation has accelerated dramatically and microbes have become a favorite system because of their fast evolution, their convenience as lab study systems and the opportunity for molecular investigations. However, the study of microbes also poses significant challenges, such as a lack of knowledge and an inaccessibility of the ecological context (used here to include both the abiotic and the biotic environment) under which the trait deemed cooperative has evolved and is maintained. I review the experimental and theoretical evidence in support of the limitations of the study of social behavior in microbes in the absence of an ecological context. I discuss both the need and the opportunities for experimental investigations that can inform a theoretical framework able to reframe the general questions of social behavior in a clear ecological context and to account for eco-evolutionary feedback.

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EXPLORING THE SOCIOBIOLOGY OF PYOVERDIN-PRODUCINGPSEUDOMONAS

Cited by 86 publications

References 86 publications

The path to re-evolve cooperation is constrained inPseudomonas aeruginosa

The path to re-evolve cooperation is constrained inPseudomonas aeruginosa

Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies

The ecology and evolution of social behavior in microbes

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