Adaptive evolution by optimizing expression levels in different environments (original) (raw)
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Physiological and Biochemical Zoology, 2005
Transcription profiling (quantitative analysis of RNA abundance) can provide a genome-wide picture of gene expression changes that accompany organismal adaptation to a new environment. Here, we used DNA microarrays to characterize genome-wide changes in transcript abundance in three replicate lines of the bacterium E. coli grown for 2,000 generations at a stressful high temperature (41.5ЊC). Across these lines, 12% of genes significantly changed expression during high-temperature adaptation; the majority of these changes (55%) were less than twofold increments or decrements. Thirty-nine genes, four times the number expected by chance alone, exhibited moderately or highly replicated expression changes across lines. Expression changes within a priori defined functional categories showed an even greater level of replication than did individual genes. Expression changes in the phenotypically defined stress genes and adaptation functional categories were important in evolutionary adaptation to high temperature.
Genome Research, 2005
Laboratory evolution can be used to address fundamental questions about adaptation to selection pressures and, ultimately, the process of evolution. In this study, we investigated the reproducibility of growth phenotypes and global gene expression states during adaptive evolution. The results from parallel, replicate adaptive evolution experiments of Escherichia coli K-12 MG1655 grown on either lactate or glycerol minimal media showed that (1) growth phenotypes at the endpoint of evolution are convergent and reproducible; (2) endpoints of evolution have different underlying gene expression states; and (3) the evolutionary gene expression response involves a large number of compensatory expression changes and a smaller number of adaptively beneficial expression changes common across evolution strains. Gene expression changes initially showed a large number of differentially expressed genes in response to an environmental change followed by a return of most genes to a baseline expression level, leaving a relatively small set of differentially expressed genes at the endpoint that varied between evolved populations.
Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation
Nature Reviews Genetics, 2008
| Organisms are constantly exposed to a wide range of environmental changes, including both short-term changes during their lifetime and longer-term changes across generations. Stress-related gene expression programmes, characterized by distinct transcriptional mechanisms and high levels of noise in their expression patterns, need to be balanced with growth-related gene expression programmes. A range of recent studies give fascinating insight into cellular strategies for keeping gene expression in tune with physiological needs dictated by the environment, promoting adaptation to both short-and long-term environmental changes. Not only do organisms show great resilience to external challenges, but emerging data suggest that they also exploit these challenges to fuel phenotypic variation and evolutionary innovation. nATuRE REvIEWS | genetics voluME 9 | AuguST 2008 | 583
Genome evolution and adaptation in a long-term experiment with Escherichia coli
Nature, 2009
The relationship between rates of genomic evolution and organismal adaptation remains uncertain, despite considerable interest. The feasibility of obtaining genome sequences from experimentally evolving populations offers the opportunity to investigate this relationship with new precision. Here we sequence genomes sampled through 40,000 generations from a laboratory population of Escherichia coli. Although adaptation decelerated sharply, genomic evolution was nearly constant for 20,000 generations. Such clock-like regularity is usually viewed as the signature of neutral evolution, but several lines of evidence indicate that almost all of these mutations were beneficial. This same population later evolved an elevated mutation rate and accumulated hundreds of additional mutations dominated by a neutral signature. Thus, the coupling between genomic and adaptive evolution is complex and can be counterintuitive even in a constant environment. In particular, beneficial substitutions were surprisingly uniform over time, whereas neutral substitutions were highly variable.
Genetics, 2006
Twelve populations of Escherichia coli evolved in and adapted to a glucose-limited environment from a common ancestor. We used two-dimensional protein electrophoresis to compare two evolved clones, isolated from independently derived populations after 20,000 generations. Exceptional parallelism was detected. We compared the observed changes in protein expression profiles with previously characterized global transcription profiles of the same clones; this is the first time such a comparison has been made in an evolutionary context where these changes are often quite subtle. The two methodologies exhibited some remarkable similarities that highlighted two different levels of parallel regulatory changes that were beneficial during the evolution experiment. First, at the higher level, both methods revealed extensive parallel changes in the same global regulatory network, reflecting the involvement of beneficial mutations in genes that control the ppGpp regulon. Second, both methods detected expression changes of identical gene sets that reflected parallel changes at a lower level of gene regulation. The protein profiles led to the discovery of beneficial mutations affecting the malT gene, with strong genetic parallelism across independently evolved populations. Functional and evolutionary analyses of these mutations revealed parallel phenotypic decreases in the maltose regulon expression and a high level of polymorphism at this locus in the evolved populations.
Molecular biology and evolution, 1991
A population of Escherichia coli initiated with a single clone developed extensive morphological and physiological polymorphism after being maintained for 773 generations in glucose-limited continuous culture. To understand the mechanisms of adaptation to this environment, total protein patterns of four adaptive clones and of the parent strains were examined by two-dimensional gel electrophoresis. Approximately 20% of the proteins (approximately 160 in absolute numbers) showed significantly different levels of expression in pairwise comparisons of parent and adapted clones. The extent of these changes points to the importance of mutations with regulatory and/or highly pleiotropic effects in the adaptive process. The four evolved clones all expressed fewer proteins than did the parent strain, supporting the hypothesis of energy conservation during evolutionary change. Forty-two proteins that could be assigned to known cellular functions were identified. The changes in some of them in...
Journal of Bacteriology, 2008
We measured the relative fitness among a set of experimentally evolved Escherichia coli strains differing by a small number of adaptive mutations by directly measuring allelic frequencies in head-to-head competitions using a mass spectrometry-based method. We compared the relative effects of mutations to the same or similar genes acquired in multiple strains when expressed in allele replacement strains. We found that the strongest determinant of fitness among the evolved strains was the impact of beneficial mutations to the RNA polymerase  and  subunit genes. We also identified several examples of epistatic interactions between rpoB/C and glpK mutations and identified two other mutations that are beneficial only in the presence of previously acquired mutations but that have little or no adaptive benefit to the wild-type strain. Allele frequency estimation is shown to be a highly sensitive method for measuring selection rates during competitions between strains differing by as little as a single-nucleotide polymorphism and may be of great use for investigating epistatic interactions.
Bacterial transcriptome reorganization in thermal adaptive evolution
BMC genomics, 2015
Evolution optimizes a living system at both the genome and transcriptome levels. Few studies have investigated transcriptome evolution, whereas many studies have explored genome evolution in experimentally evolved cells. However, a comprehensive understanding of evolutionary mechanisms requires knowledge of how evolution shapes gene expression. Here, we analyzed Escherichia coli strains acquired during long-term thermal adaptive evolution. Evolved and ancestor Escherichia coli cells were exponentially grown under normal and high temperatures for subsequent transcriptome analysis. We found that both the ancestor and evolved cells had comparable magnitudes of transcriptional change in response to heat shock, although the evolutionary progression of their expression patterns during exponential growth was different at either normal or high temperatures. We also identified inverse transcriptional changes that were mediated by differences in growth temperatures and genotypes, as well as n...
2015
Beneficial mutations fuel adaptation by altering phenotypes that enhance the fit of organisms to their environment. However, the phenotypic effects of mutations often depend on ecological context, making the distribution of effects across multiple environments essential to understanding the true nature of beneficial mutations. Studies that address both the genetic basis and ecological consequences of adaptive mutations remain rare. Here, we characterize the direct and pleiotropic fitness effects of a collection of 21 first-step beneficial mutants derived from naive and adapted genotypes used in a long-term experimental evolution of Escherichia coli. Whole-genome sequencing was used to identify most beneficial mutations. In contrast to previous studies, we find diverse fitness effects of mutations selected in a simple environment and few cases of genetic parallelism. The pleiotropic effects of these mutations were predominantly positive but some mutants were highly antagonistic in al...
The effect of environment on adaptation and divergence was examined in two sets of populations of Eschm'chia coli selected for 1000 generations in either maltose-or glucose-limited media. Twelve replicate populations selected in maltose-limited medium improved in fitness in the selected environment, by an average of 22.5%. Statistically significant among-population genetic variation for fitness was observed during the course of the propagation, but this variation was small relative to the fitness improvement. Mean fitness in a novel nutrient environment, glucose-limited medium, improved to the same extent as in the selected environment, with no statistically significant among-population genetic variation. In contrast, 12 replicate populations previously selected for 1000 generations in glucose-limited medium showed no improvement, as a group, in fitness in maltose-limited medium and substantial genetic variation. This asymmetric pattern of correlated responses suggests that small changes in the environment can have profound effects on adaptation and divergence. Genetics 146 471-479 (,Junt., 1997) VISANO et d . 199513) .