Cheating fosters species co-existence in well-mixed bacterial communities

Leinweber, Anne; Inglis, R. Fredrik; Kümmerli, Rolf

doi:10.1038/ismej.2016.195

Cited by 81 publications

(83 citation statements)

References 63 publications

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“…Shaking is supposed to increase the mixing of cells and public goods, and has been shown to improve pyoverdine cheating abilities in P. aeruginosa (Leinweber et al. ). We found the opposite to be the case for the Burkholderia siderophores (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

et al. 2019

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Explaining how cooperation can persist in the presence of cheaters, exploiting the cooperative acts, is a challenge for evolutionary biology. Microbial systems have proved extremely useful to test evolutionary theory and identify mechanisms maintaining cooperation. One of the most widely studied system is the secretion and sharing of iron‐scavenging siderophores by Pseudomonas bacteria, with many insights gained from this system now being considered as hallmarks of bacterial cooperation. Here, we introduce siderophore secretion by the bacterium Burkholderia cenocepacia H111 as a novel parallel study system, and show that this system behaves differently. For ornibactin, the main siderophore of this species, we discovered a novel mechanism of how cheating can be prevented. Particularly, we found that secreted ornibactin cannot be exploited by ornibactin‐defective mutants because ornibactin receptor and synthesis genes are co‐expressed from the same operon, such that disruptive mutations in synthesis genes compromise receptor availability required for siderophore uptake and cheating. For pyochelin, the secondary siderophore of this species, we found that cheating was possible, but the relative success of cheaters was positive frequency dependent, thus diametrically opposite to the Pseudomonas and other microbial systems. Altogether, our results highlight that expanding our repertoire of microbial study systems leads to new discoveries and suggest that there is an enormous diversity of social interactions out there in nature, and we might have only looked at the tip of the iceberg so far.

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Section: Resultsmentioning

confidence: 99%

“…), and that cheaters perform best in shaken cultures (Leinweber et al. ), at high cell density (Ross‐Gillespie et al. ) and when rare (Ross‐Gillespie et al.…”

Section: Discussionmentioning

confidence: 99%

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

et al. 2019

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“…These levels of iron supplementation have previously been shown to either reduce pyoverdine production to intermediate levels (1 μM FeCl 3 ) or to completely stall pyoverdine synthesis (40 μM FeCl 3 ) [14]. Furthermore, competition experiments between PAO1 cooperators and their cheating isogenic knock-out mutant (PAO1 ΔpvdD ΔpchEF), deficient for siderophore production, revealed that cheats could only invade without the supplementation of extra iron [13].…”

Section: Strains and Growth Conditionsmentioning

confidence: 99%

“…Previous work revealed that increased spatial structure maintains cooperation because it reduces pyoverdine diffusion and cell dispersal. In other words, spatial structure ensures that pyoverdine sharing occurs predominantly among producer cells [13,[18][19][20]. The second factor involves the relative costs and benefits of pyoverdine production [14,17].…”

Section: Introductionmentioning

confidence: 99%

The path to re-evolve cooperation is constrained inPseudomonas aeruginosa

Granato

Kümmerli

2017

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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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“…; Leinweber et al. ). In intraspecific competition, the secreted siderophores can be shared as public goods between cells that possess a compatible receptor for uptake.…”

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The bacteriumPseudomonas aeruginosasenses and gradually responds to interspecific competition for iron

2018

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Phenotypic plasticity in response to competition is a well-described phenomenon in higher organisms. Here, we show that also bacteria have the ability to sense the presence of competitors and mount fine-tuned responses to match prevailing levels of competition. In our experiments, we studied interspecific competition for iron between the bacterium Pseudomonas aeruginosa (PA) and its competitor Burkholderia cenocepacia (BC). We focused on the ability of PA to phenotypically adjust the production of pyoverdine, an iron-scavenging siderophore. We found that PA upregulates pyoverdine production early on during competition under condition of low iron availability. This plastic upregulation was fine-tuned in response to the level of competition imposed by BC, and seems to confer a relative fitness benefit to PA in the form of an earlier initiation of growth. At later time points, however, PA showed reduced growth in mixed compared to monoculture, suggesting that competitive responses are costly. Altogether, our results demonstrate that phenotypic plasticity in siderophore production plays an important role in interspecific competition for iron. Upregulating siderophore production may be a powerful strategy to lock iron away from competing species, and to reserve this nutrient for strain members possessing the compatible receptor for uptake.

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Cheating fosters species co-existence in well-mixed bacterial communities

Cited by 81 publications

References 63 publications

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

The path to re-evolve cooperation is constrained inPseudomonas aeruginosa

The bacteriumPseudomonas aeruginosasenses and gradually responds to interspecific competition for iron

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