Self-destructive cooperation mediated by phenotypic noise

Ackermann, Martin; Stecher, Bärbel; Freed, Nikki E.; Songhet, Pascal; Hardt, Wolf‐Dietrich; Doebeli, Michael

doi:10.1038/nature07067

Cited by 399 publications

(484 citation statements)

References 28 publications

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“…Because infection causes the rapid death of the host, an infected individual has little or no opportunity to reproduce until its death, such that the commitment of suicide might simply hasten an individual's inevitable doom. Our findings demonstrate that altruistic host suicide can clearly be delimited from other forms of suicidal behaviours in microbes, such as cell lysis to release toxins [25] or nutrients [26], cell sacrifices to overcome immune systems [27] or to form fruiting body stalks [28,29]. In contrast to the altruistic suicide described in our study, these other behaviours require substantial relatedness among interacting individuals because suicidal cells lose direct fitness benefits.…”

Section: Discussionmentioning

confidence: 52%

Altruism can evolve when relatedness is low: evidence from bacteria committing suicide upon phage infection

2013

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High relatedness among interacting individuals has generally been considered a precondition for the evolution of altruism. However, kin-selection theory also predicts the evolution of altruism when relatedness is low, as long as the cost of the altruistic act is minor compared with its benefit. Here, we demonstrate evidence for a low-cost altruistic act in bacteria. We investigated Escherichia coli responding to the attack of an obligately lytic phage by committing suicide in order to prevent parasite transmission to nearby relatives. We found that bacterial suicide provides large benefits to survivors at marginal costs to committers. The cost of suicide was low, because infected cells are moribund, rapidly dying upon phage infection, such that no more opportunity for reproduction remains. As a consequence of its marginal cost, host suicide was selectively favoured even when relatedness between committers and survivors approached zero. Altogether, our findings demonstrate that low-cost suicide can evolve with ease, represents an effective host-defence strategy, and seems to be widespread among microbes. Moreover, low-cost suicide might also occur in higher organisms as exemplified by infected social insect workers leaving the colony to die in isolation.

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Section: Discussionmentioning

confidence: 52%

Altruism can evolve when relatedness is low: evidence from bacteria committing suicide upon phage infection

2013

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“…Bistable production of the SPI-1 T3SS in S. Typhimurium has also recently been described (77)(78)(79). The authors observed that nearly 100% of S. Typhimurium cells interacting with intestinal tissues were positive for SPI-1 expression while only 15% of cells in the intestinal lumen were positive (77). The presence of both SPI-1 ϩ and SPI-1 Ϫ cells seems to be important for stabilizing the virulence traits of S. Typhimurium (78).…”

Section: Discussionmentioning

confidence: 81%

“…In Vibrio cholerae, bimodal expression of ToxT results in virulent and nonvirulent cell subpopulations (76). Bistable production of the SPI-1 T3SS in S. Typhimurium has also recently been described (77)(78)(79). The authors observed that nearly 100% of S. Typhimurium cells interacting with intestinal tissues were positive for SPI-1 expression while only 15% of cells in the intestinal lumen were positive (77).…”

Section: Discussionmentioning

confidence: 98%

Bistable Expression of CsgD in Salmonella enterica Serovar Typhimurium Connects Virulence to Persistence

MacKenzie

Wang²,

Shivak

et al. 2015

Infect Immun

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f Pathogenic bacteria often need to survive in the host and the environment, and it is not well understood how cells transition between these equally challenging situations. For the human and animal pathogen Salmonella enterica serovar Typhimurium, biofilm formation is correlated with persistence outside a host, but the connection to virulence is unknown. In this study, we analyzed multicellular-aggregate and planktonic-cell subpopulations that coexist when S. Typhimurium is grown under biofilminducing conditions. These cell types arise due to bistable expression of CsgD, the central biofilm regulator. Despite being exposed to the same stresses, the two cell subpopulations had 1,856 genes that were differentially expressed, as determined by transcriptome sequencing (RNA-seq). Aggregated cells displayed the characteristic gene expression of biofilms, whereas planktonic cells had enhanced expression of numerous virulence genes. Increased type three secretion synthesis in planktonic cells correlated with enhanced invasion of a human intestinal cell line and significantly increased virulence in mice compared to the aggregates. However, when the same groups of cells were exposed to desiccation, the aggregates survived better, and the competitive advantage of planktonic cells was lost. We hypothesize that CsgD-based differentiation is a form of bet hedging, with single cells primed for host cell invasion and aggregated cells adapted for persistence in the environment. This allows S. Typhimurium to spread the risks of transmission and ensures a smooth transition between the host and the environment.

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“…Although traits such as sterility raise important evolutionary questions and can be correlated with whether a major transition has occurred, they are neither necessary nor sufficient for a major transition. Indeed, other examples of complete altruism can be found, which are clearly not major transitions, including bacteria bursting suicidally to release factors that reduce competition (59).…”

Section: Conflict and Maximizing Agentsmentioning

confidence: 99%

Major evolutionary transitions in individuality

West

Fisher

Gardner

et al. 2015

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

320

435

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The evolution of life on earth has been driven by a small number of major evolutionary transitions. These transitions have been characterized by individuals that could previously replicate independently, cooperating to form a new, more complex life form. For example, archaea and eubacteria formed eukaryotic cells, and cells formed multicellular organisms. However, not all cooperative groups are en route to major transitions. How can we explain why major evolutionary transitions have or haven't taken place on different branches of the tree of life? We break down major transitions into two steps: the formation of a cooperative group and the transformation of that group into an integrated entity. We show how these steps require cooperation, division of labor, communication, mutual dependence, and negligible within-group conflict. We find that certain ecological conditions and the ways in which groups form have played recurrent roles in driving multiple transitions. In contrast, we find that other factors have played relatively minor roles at many key points, such as within-group kin discrimination and mechanisms to actively repress competition. More generally, by identifying the small number of factors that have driven major transitions, we provide a simpler and more unified description of how life on earth has evolved.T he evolution of life, from simple organic compounds in a primordial soup to the amazing diversity of contemporary organisms, has taken roughly 3.5 billion years. How can we explain the evolution of increasingly complex organisms over this period? A traditional approach has been to consider the succession of taxonomic groups, such as the age of fishes giving rise to the age of amphibians, which gave way to the age of reptiles, and so on. Although this approach has some uses, it is biased toward relatively large plants and animals and lacks a conceptual or predictive framework, in that it suggests we look for different explanations for each succession (1).Twenty years ago, Maynard Smith and Szathmáry (2) revolutionized our understanding of life on earth by showing how the key steps in the evolution of life on earth had been driven by a small number of "major evolutionary transitions." In each transition, a group of individuals that could previously replicate independently cooperate to form a new, more complex life form. For example, genes cooperated to form genomes, archaea and eubacteria formed eukaryotic cells, and cells cooperated to form multicellular organisms (Table 1).The major transitions approach provides a conceptual framework that facilitates comparison across pivotal moments in the history of life (2, 3). It suggests that the same problem arises at each transition: How are the potentially selfish interests of individuals overcome to form mutually dependent cooperative groups? We can then ask whether there are any similarities across transitions in the answers to this problem. Consequently, rather than looking for different explanations for the succession of different taxonomic groups, we ...

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Self-destructive cooperation mediated by phenotypic noise

Cited by 399 publications

References 28 publications

Altruism can evolve when relatedness is low: evidence from bacteria committing suicide upon phage infection

Altruism can evolve when relatedness is low: evidence from bacteria committing suicide upon phage infection

Bistable Expression of CsgD in Salmonella enterica Serovar Typhimurium Connects Virulence to Persistence

Major evolutionary transitions in individuality

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