Evolution of global regulatory networks during a long‐term experiment withEscherichia coli

Abstract

Evolution has shaped all living organisms on Earth, although many details of this process are shrouded in time. However, it is possible to see, with one's own eyes, evolution as it happens by performing experiments in defined laboratory conditions with microbes that have suitably fast generations. The longest-running microbial evolution experiment was started in 1988, at which time twelve populations were founded by the same strain of Escherichia coli. Since then, the populations have been serially propagated and have evolved for tens of thousands of generations in the same environment. The populations show numerous parallel phenotypic changes, and such parallelism is a hallmark of adaptive evolution. Many genetic targets of natural selection have been identified, revealing a high level of genetic parallelism as well. Beneficial mutations affect all levels of gene regulation in the cells including individual genes and operons all the way to global regulatory networks. Of particular interest, two highly interconnected networks -- governing DNA superhelicity and the stringent response -- have been demonstrated to be deeply involved in the phenotypic and genetic adaptation of these experimental populations.

RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media

“…Mutations to genes encoding transcription regulatory hubs have been found previously in long-term adaptive evolutions of E. coli (29); the mutations to RNAP genes arising in E. coli during adaption to GMM in our experiment are additional examples of an adaptive strategy that targets a regulatory hub, in this case RNAP itself. We found (i) mutations to rpoB and rpoC genes corresponding to the RNAP jaw and SI3 regions were consistently selected for during adaptive evolution of MG1655 in GMM; (ii) these mutations are adaptive for growth of MG1655 in minimal media, at the cost of slower growth in rich media; (iii) these mutations reprogrammed the kinetic parameters of RNAP by decreasing the longevity of open complexes at a promoter, by decreasing pausing, and by increasing elongation rate; (iv) gene expression profiling and the genome-wide RNAP dynamic binding map are consistent with a redistribution of the polymerase from stringently controlled TUs to other parts of the genome; and (v) the mutations caused profound gene expression changes, including strong down-regulation of acid resistance, curlin, and fimbria genes, and sometimes motility genes.…”

Gene expression analysis of E. coli strains provides insights into the role of gene regulation in diversification

“…In bacteria, the importance of gene-expression as a governing factor for evolution, habitat adaptation and diversification is recognized as well (c.f. Philippe et al, 2007) and initial data from a pioneer study that correlated global protein expression profiles with evolutionary relatedness in the Shewanella genus are available (Konstantinidis et al, 2009). However, the field is largely unexplored and global, omics-based data specifically investigating the link between gene regulation and phylogeny under different culture conditions are needed to understand the role of gene expression in bacterial diversification.…”

Laboratory evolution of Geobacter sulfurreducens for enhanced growth on lactate via a single-base-pair substitution in a transcriptional regulator

“…Genomic changes promoting adaptation to new substrates have included mutations that enhance the kinetics of enzymes acting on the substrate (Fong et al, 2005a, b;Herring et al, 2006;Conrad et al, 2009;Lee and Palsson, 2010) and mutations in promoter regions and global regulatory elements (Treves et al, 1998;Herring et al, 2006;Pelosi et al, 2006); as well as RNA polymerases (Herring et al, 2006;Conrad et al, 2010). Surprisingly, there have been fewer reports of adaptation to the use of a new substrate via mutations in known transcriptional regulators (Philippe et al, 2007;Barrick et al, 2009) despite the fact that changes in transcriptional regulators are thought to have key roles in the evolution of new microbial species (Dekel and Alon, 2005;Babu and Aravind, 2006;Babu et al, 2007), a concept further supported with the observation that transcriptional regulatory networks evolve and change faster than other collaborative biological networks such as protein interaction networks and metabolic pathway networks (Shou et al, 2011).…”