Presence of a loner strain maintains cooperation and diversity in well-mixed bacterial communities

Inglis, R. Fredrik; Biernaskie, Jay M.; Gardner, Andy; Kümmerli, Rolf

doi:10.1098/rspb.2015.2682

Cited by 52 publications

(70 citation statements)

References 58 publications

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“…a, with a PA01 cooperator/cheat pair, and a type‐III siderophore producer; the same type produced by our 59.20 cooperator. The difference between the results probably reflects the differences in the costs of siderophore production, the proportion of siderophores shared or proportion retained for personal use (see Inglis et al ., ), which in our case did not have suitable values for the loner effect to occur.…”

Section: Discussioncontrasting

confidence: 54%

The effect of cheats on siderophore diversity in Pseudomonas aeruginosa

Stilwell

Lowe

Buckling

2018

J of Evolutionary Biology

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Cooperation can be maintained if cooperative behaviours are preferentially directed towards other cooperative individuals. Tag‐based cooperation (greenbeards) – where cooperation benefits individuals with the same tag as the actor – is one way to achieve this. Tag‐based cooperation can be exploited by individuals who maintain the specific tag but do not cooperate, and selection to escape this exploitation can result in the evolution of tag diversity. We tested key predictions crucial for the evolution of cheat‐mediated tag diversity using the production of iron‐scavenging pyoverdine by the opportunistic pathogen, Pseduomonas aeruginosa as a model system. Using two strains that produce different pyoverdine types and their respective cheats, we show that cheats outcompete their homologous pyoverdine producer, but are outcompeted by the heterologous producer in well‐mixed environments. As a consequence, co‐inoculating two types of pyoverdine producer and one type of pyoverdine cheat resulted in the pyoverdine type whose cheat was not present having a large fitness advantage. Theory suggests that in such interactions, cheats can maintain tag diversity in spatially structured environments, but that tag‐based cooperation will be lost in well‐mixed populations, regardless of tag diversity. We saw that when all pyoverdine producers and cheats were co‐inoculated in well‐mixed environments, both types of pyoverdine producers were outcompeted, whereas spatial structure (agar plates and compost microcosms), rather than maintaining diversity, resulted in the domination of one pyoverdine producer. These results suggest cheats may play a more limited role in the evolution of pyoverdine diversity than predicted.

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Section: Discussioncontrasting

confidence: 54%

The effect of cheats on siderophore diversity in Pseudomonas aeruginosa

Stilwell

Lowe

Buckling

2018

J of Evolutionary Biology

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“…Similarly, increased carbon availability reduces the relative metabolic costs of pyoverdine production, and thus decreases the advantage of cheaters (Brockhurst et al ., ; Sexton and Schuster, ). Finally, community composition was found to be a key factor determining who interacts with whom, thereby influencing the relative importance of competition versus cooperation (Griffin et al ., ; Inglis et al ., ; Leinweber et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Environmental determinants of pyoverdine production, exploitation and competition in natural Pseudomonas communities

Butaitė

Kramer

Wyder

et al. 2018

Environmental Microbiology

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Many bacteria rely on the secretion of siderophores to scavenge iron from the environment. Laboratory studies revealed that abiotic and biotic factors together determine how much siderophores bacteria make, and whether siderophores can be exploited by non-producing cheaters or be deployed by producers to inhibit competitors. Here, we explore whether these insights apply to natural communities, by comparing the production of the siderophore pyoverdine among 930 Pseudomonas strains from 48 soil and pond communities. We found that pH, iron content, carbon concentration and community diversity determine pyoverdine production levels, and the extent to which strains are either stimulated or inhibited by heterologous (non-self) pyoverdines. While pyoverdine non-producers occurred in both habitats, their prevalence was higher in soils. Environmental and genetic analyses suggest that non-producers can evolve as cheaters, exploiting heterologous pyoverdine, but also due to pyoverdine disuse in environments with increased iron availability. Overall, we found that environmental factors explained between-strain variation in pyoverdine production much better in soils than in ponds, presumably because high strain mixing in ponds impedes local adaption. Our study sheds light on the complexity of natural bacterial communities, and provides first insights into the multivariate nature of siderophore-based iron acquisition and competition among environmental pseudomonads.

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“…While high cell density and diversity can create strong competition in the struggle for nutrients and space [1,2], it can also promote stable networks of cooperation [3,4]. A common way for bacteria to cooperate is through the secretion of nutrientscavenging metabolites, which are shared as "public goods" in the community.…”

Section: Introductionmentioning

confidence: 99%

The path to re-evolve cooperation is constrained in Pseudomonas 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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Presence of a loner strain maintains cooperation and diversity in well-mixed bacterial communities

Cited by 52 publications

References 58 publications

The effect of cheats on siderophore diversity in Pseudomonas aeruginosa

The effect of cheats on siderophore diversity in Pseudomonas aeruginosa

Environmental determinants of pyoverdine production, exploitation and competition in natural Pseudomonas communities

The path to re-evolve cooperation is constrained in Pseudomonas aeruginosa

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