Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli

Herron, Matthew D.; Doebeli, Michael

doi:10.1371/journal.pbio.1001490

Cited by 196 publications

(236 citation statements)

References 59 publications

(76 reference statements)

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“…The aceB gene encodes malate synthase, which catalyzes the second bypass step of the glyoxylate shunt, and iclR encodes a transcriptional repressor of the aceBAK operon (32). Mutations in iclR commonly arise in evolution experiments with E. coli that use glucose-limited medium because they improve the utilization of acetate, a transient byproduct of E. coli growth on glucose (38).…”

Section: Some Mutations Evolved In One Temperature Regime Are Alsomentioning

confidence: 99%

Specificity of genome evolution in experimental populations of Escherichia coli evolved at different temperatures

Deatherage

Kepner

Bennett

et al. 2017

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

118

101

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Isolated populations derived from a common ancestor are expected to diverge genetically and phenotypically as they adapt to different local environments. To examine this process, 30 populations ofEscherichia coliwere evolved for 2,000 generations, with six in each of five different thermal regimes: constant 20 °C, 32 °C, 37 °C, 42 °C, and daily alternations between 32 °C and 42 °C. Here, we sequenced the genomes of one endpoint clone from each population to test whether the history of adaptation in different thermal regimes was evident at the genomic level. The evolved strains had accumulated ∼5.3 mutations, on average, and exhibited distinct signatures of adaptation to the different environments. On average, two strains that evolved under the same regime exhibited ∼17% overlap in which genes were mutated, whereas pairs that evolved under different conditions shared only ∼4%. For example, all six strains evolved at 32 °C had mutations innadR, whereas none of the other 24 strains did. However, a population evolved at 37 °C for an additional 18,000 generations eventually accumulated mutations in the signature genes strongly associated with adaptation to the other temperature regimes. Two mutations that arose in one temperature treatment tended to be beneficial when tested in the others, although less so than in the regime in which they evolved. These findings demonstrate that genomic signatures of adaptation can be highly specific, even with respect to subtle environmental differences, but that this imprint may become obscured over longer timescales as populations continue to change and adapt to the shared features of their environments.

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Section: Some Mutations Evolved In One Temperature Regime Are Alsomentioning

confidence: 99%

Specificity of genome evolution in experimental populations of Escherichia coli evolved at different temperatures

Deatherage

Kepner

Bennett

et al. 2017

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

118

101

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“…Some have argued that evolution is fundamentally stochastic and unpredictable [3], while others have proposed that constraints commonly limit available phenotypic options, leading to parallelism and predictability [4]. Although parallel genotypic adaptation has been demonstrated across a diverse range of taxa at the intraspecific level [5][6][7][8][9][10][11], the widespread occurrence of parallel evolution across a clade has only rarely been shown [12,13]. The potential role of environmental change in driving parallel evolution also remains poorly understood [14].…”

Section: Introductionmentioning

confidence: 99%

Multiple evolutionary origins of Australian soil-burrowing cockroaches driven by climate change in the Neogene

Tong

Rose

et al. 2016

Proc. R. Soc. B.

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Parallel evolution is the independent appearance of similar derived phenotypes from similar ancestral forms. It is of key importance in the debate over whether evolution is stochastic and unpredictable, or subject to constraints that limit available phenotypic options. Nevertheless, its occurrence has rarely been demonstrated above the species level. Climate change on the Australian landmass over the last approximately 20 Myr has provided conditions conducive to parallel evolution, as taxa at the edges of shrinking mesic habitats adapted to drier biomes. Here, we investigate the phylogeny and evolution of Australian soil-burrowing and wood-feeding blaberid cockroaches. Soil burrowers (subfamily Geoscapheinae) are found in relatively dry sclerophyllous and scrubland habits, whereas wood feeders (subfamily Panesthiinae) are found in rainforest and wet sclerophyll. We sequenced and analysed mitochondrial and nuclear markers from 142 specimens, and estimated the evolutionary time scale of the two subfamilies. We found evidence for the parallel evolution of soil-burrowing taxa from wood-feeding ancestors on up to nine occasions. These transitions appear to have been driven by periods of aridification during the Miocene and Pliocene across eastern Australia. Our results provide an illuminating example of climate-driven parallel evolution among species.

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“…All lineages exhibited comparable mutational rates over 2000 generations of laboratory evolution including a small fraction of synonymous mutations (Table 1, Supplementary Table 1). Non-synonymous mutations increased throughout the laboratory evolution trials on a per generation per lineage basis, a behavior observed in non-hybrid control lineages and in various adaptive evolution experiments (Barrick and Lenski 2013;Conrad et al 2011;Herron and Doebeli 2013;Lang and Desai 2014;Tenaillon et al 2016). Mutations were observed in the same suite of genes across all lineages, hybrid and control.…”

Section: Comparative Analysis Of Mutational Trends Across Lineagesmentioning

confidence: 72%

“…Prior laboratory evolution studies that report mutations in genes that are also detected in our study include Barrick et al 2009, Maddamsetti et al 2015, Dillon et al 2016, Conrad 2009, Herron and Doebeli 2013and Phillips et al 2016 Gene Function Number of lineages that accumulated a non-synonymous mutation over 20% frequency (Table 1). However, five out of the six ancient-modern hybrid lineages (and none of the other control lineages) evolved mutations in the thrT/tufB promoter region, with four variant alleles being observed (Lee et al 1981).…”

Section: Promoter-level Mutations Upregulate Ancient Ef-tu Expressionmentioning

confidence: 83%

Experimental evolution of Escherichia coli harboring an ancient translation protein

Kaçar

Tran

et al. 2016

Preprint

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The ability to design synthetic genes and engineer biological systems at the genome scale opens new means by which to characterize phenotypic states and the responses of biological systems to perturbations. One emerging method involves inserting artificial genes into bacterial genomes, and examining how the genome and its new genes adapt to each other. Here we report the development and implementation of a modified approach to this method, in which phylogenetically inferred genes are inserted into a microbial genome, and laboratory evolution is then used to examine the adaptive potential of the resulting hybrid genome. Specifically, we engineered an approximately 700-million-year old inferred ancestral variant of tufB, an essential gene encoding Elongation Factor Tu, and inserted it in a modern Escherichia coli genome in place of the native tufB gene. While the ancient homolog was not lethal to the cell, it did cause a two-fold decrease in organismal fitness, mainly due to reduced protein dosage. We subsequently evolved replicate hybrid bacterial populations for 2,000 generations in the laboratory, and examined the adaptive response via fitness assays, whole-genome sequencing, proteomics and biochemical assays. We found that the hybrid lineages exhibit a general adaptive strategy in which the fitness cost of the ancient gene was ameliorated in part by up-regulation of protein production. We expect that this ancient-modern recombinant method may pave the way for the synthesis of organisms that exhibit ancient phenotypes, and that laboratory evolution of these organisms may prove useful in elucidating insights into historical adaptive processes.

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Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli

Abstract: The divergence of Escherichia coli bacteria into metabolically distinct ecotypes has a similar genetic basis and similar evolutionary dynamics across independently evolved populations.

Cited by 196 publications

References 59 publications

Specificity of genome evolution in experimental populations of Escherichia coli evolved at different temperatures

Specificity of genome evolution in experimental populations of Escherichia coli evolved at different temperatures

Multiple evolutionary origins of Australian soil-burrowing cockroaches driven by climate change in the Neogene

Experimental evolution of Escherichia coli harboring an ancient translation protein

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