Evolutionary transitions in bacterial symbiosis

Sachs, Joel; Skophammer, Ryan G.; Regus, John U.

doi:10.1073/pnas.1100304108

Cited by 296 publications

(341 citation statements)

References 116 publications

(261 reference statements)

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“…In contrast, both the opportunity for horizontal transmission, and within-host symbiont diversity, could lead to conflicts that select for less cooperative symbionts (22,46). Consistent with the predicted role of transmission route, the evolutionary transition from a parasitic to a mutualistic lifestyle in a range of bacterial lineages is associated with the loss of horizontal transmission (47).…”

Section: What Conditions Lead To Negligible Conflict Within Groups?mentioning

confidence: 80%

Major evolutionary transitions in individuality

West

Fisher

Gardner

et al. 2015

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

300

412

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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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Section: What Conditions Lead To Negligible Conflict Within Groups?mentioning

confidence: 80%

Major evolutionary transitions in individuality

West

Fisher

Gardner

et al. 2015

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

300

412

View full text Add to dashboard Cite

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“…While there is debate on the origin and the maintenance of these mechanisms [20 -23], their viability as an evolutionary stable state [15][16][17]24], and how we can distinguish between them in natural systems [20,22,25], all three mechanisms share a common outcome: the host increases the relative fitness of more beneficial partners and/or decreases the relative fitness of less beneficial or exploitative partners. Given the recurrent observation of exploitative partners [4,8,26], selection on stabilizing mechanisms is predicted to be strong because exploitative symbionts are assumed to have negative effects on host fitness [13,16,[27][28][29][30] (but see [31]). If there is a cost to stabilizing mechanisms, in the absence of exploiters, selection will favour the loss of host stabilizing traits [17].…”

Section: Introductionmentioning

confidence: 99%

Standing genetic variation in host preference for mutualist microbial symbionts

Simonsen

Stinchcombe

2014

Proc. R. Soc. B.

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Many models of mutualisms show that mutualisms are unstable if hosts lack mechanisms enabling preferential associations with mutualistic symbiotic partners over exploitative partners. Despite the theoretical importance of mutualism-stabilizing mechanisms, we have little empirical evidence to infer their evolutionary dynamics in response to exploitation by non-beneficial partners. Using a model mutualism-the interaction between legumes and nitrogen-fixing soil symbionts-we tested for quantitative genetic variation in plant responses to mutualistic and exploitative symbiotic rhizobia in controlled greenhouse conditions. We found significant broad-sense heritability in a legume host's preferential association with mutualistic over exploitative symbionts and selection to reduce frequency of associations with exploitative partners. We failed to detect evidence that selection will favour the loss of mutualism-stabilizing mechanisms in the absence of exploitation, as we found no evidence for a fitness cost to the host trait or indirect selection on genetically correlated traits. Our results show that genetic variation in the ability to preferentially reduce associations with an exploitative partner exists within mutualisms and is under selection, indicating that micro-evolutionary responses in mutualism-stabilizing traits in the face of rapidly evolving mutualistic and exploitative symbiotic bacteria can occur in natural host populations.

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“…Rhizobia are phylogenetically disparate bacteria distributed in many genera of a-and b-proteobacteria intermixed with saprophytes and pathogens from which they may have evolved (Bontemps et al, 2010;Sachs et al, 2011). A bulk of evidence indicates that the large phylogenetic diversity of rhizobia originates from repeated and independent events of lateral gene transfer (LGT) of key symbiotic functions carried by plasmids or islands to nonsymbiotic bacterial recipient genomes (Sullivan and Ronson, 1998;Rogel et al, 2001;Ramsay et al, 2006Ramsay et al, , 2009.…”

Section: Introductionmentioning

confidence: 99%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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Soil bacteria known as rhizobia are able to establish an endosymbiosis with legumes that takes place in neoformed nodules in which intracellularly hosted bacteria fix nitrogen. Intracellular accommodation that facilitates nutrient exchange between the two partners and protects bacteria from plant defense reactions has been a major evolutionary step towards mutualism. Yet the forces that drove the selection of the late event of intracellular infection during rhizobium evolution are unknown. To address this question, we took advantage of the previous conversion of the plant pathogen Ralstonia solanacearum into a legume-nodulating bacterium that infected nodules only extracellularly. We experimentally evolved this draft rhizobium into intracellular endosymbionts using serial cycles of legume-bacterium cocultures. The three derived lineages rapidly gained intracellular infection capacity, revealing that the legume is a highly selective environment for the evolution of this trait. From genome resequencing, we identified in each lineage a mutation responsible for the extracellular-intracellular transition. All three mutations target virulence regulators, strongly suggesting that several virulence-associated functions interfere with intracellular infection. We provide evidence that the adaptive mutations were selected for their positive effect on nodulation. Moreover, we showed that inactivation of the type three secretion system of R. solanacearum that initially allowed the ancestral draft rhizobium to nodulate, was also required to permit intracellular infection, suggesting a similar checkpoint for bacterial invasion at the early nodulation/root infection and late nodule cell entry levels. We discuss our findings with respect to the spread and maintenance of intracellular infection in rhizobial lineages during evolutionary times.

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Evolutionary transitions in bacterial symbiosis

Cited by 296 publications

References 116 publications

Major evolutionary transitions in individuality

Major evolutionary transitions in individuality

Standing genetic variation in host preference for mutualist microbial symbionts

Experimental evolution of nodule intracellular infection in legume symbionts

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