Pang, T. Y. | bioRxiv Science

bioRxiv2017

The adaptive acquisition of single DNA segments drives metabolic evolution across E. coli lineages

Even closely related prokaryotes show an astounding diversity in their ability to grow in different nutritional environments1,2. Mechanistically, this diversity arises predominantly through horizontal gene transfer, the exchange of DNA between individuals from different strains3. It has been hypothesized that complex metabolic adaptations - those requiring the acquisition of multiple distinct DNA segments - can evolve via selectively neutral intermediate steps4,5; an alternative explanation rests on the existence of intermediate environments that make each individual DNA acquisition adaptive6 However, it is unclear how important changing environments6 are compared to neutral explorations of phenotype space5; more fundamentally, it is unknown what fraction of metabolic adaptations are indeed complex. Here, we use metabolic network simulations to show that all 3,363 phenotypic innovations observed in the evolutionary history of 53 E. coli strains arose through the acquisition of a single DNA segment; while we found no evidence for the contribution of selectively neutral processes, 10.6% of adaptations to previously unviable environments relied on the support of DNA acquisitions on earlier phylogenetic branches. 97.0% of all metabolic phenotypes accessible for the E. coli pan-genome could be bestowed on any ancestral strain by transferring a single DNA segment from one of the extant strains. These results demonstrate an amazing ability of the E. coli lineage to quickly adapt to previously inaccessible environments through a single DNA acquisition, an ability likely to be mirrored in other clades of generalist bacteria.

systems biology↗

bioRxiv2016

A coarse-graining, ultrametric approach to resolve the phylogeny of prokaryotic strains with frequent recombination

A frequent event in the evolution of prokaryotic genomes is homologous recombination, where a foreign DNA stretch replaces a genomic region similar in sequence. Recombination can affect the relative position of two genomes in a phylogenetic reconstruction in two different ways: (i) one genome can recombine with a DNA stretch that is similar to the other genome, thereby reducing their pairwise sequence divergence; (ii) one genome can recombine with a DNA stretch from an outgroup genome, increasing the pairwise divergence. While several recombination-aware phylogenetic algorithms exist, many of these cannot account for both types of recombination; some algorithms can, but do so inefficiently. Moreover, many existing algorithms require that a substantial portion of each genome has not been affected by recombination, a sometimes unrealistic assumption. Here, we propose a novel coarse-graining approach for phylogenetic reconstruction (CGP), which is recombination-aware, applicable even if all genomic regions have experienced substantial amounts of recombination, and can be used on both nucleotide and amino acid sequences. CGP considers the local density of substitutions along pairwise genome alignments, fitting a model to the empirical distribution of substitution density to infer the pairwise coalescent time. Given all pairwise coalescent times, CGP reconstructs an ultrametric tree representing vertical inheritance. Based on simulations, we show that the proposed approach can reconstruct ultrametric trees with accurate topology, branch lengths, and root positioning. Applied to a set of E. coli strains, the reconstructed trees are most consistent with gene distributions when inferred from amino acid sequences, a data type that cannot be utilized by many alternative approaches.\n\nAUTHOR SUMMARYIn homologous recombination, segments of foreign DNA overwrite similar segments of a prokaryotic genome. A single recombination event can simultaneously introduce many DNA substitutions. This disturbs phylogenetic signals, making it difficult to reconstruct prokaryotic family trees. While a handful of recombination-aware phylogenetic algorithms have been proposed, most do not take all effects of recombination into account; others rely on the frequently unrealistic assumption that a substantial part of a genome has not been affected by recombination at all. Here, we introduce a novel approach to phylogenetic reconstruction, which estimates the age of the most recent common ancestor of two strains from the density distribution of DNA or amino acid substitutions between their genomes. The proposed phylogenetic tree is the tree most compatible with these age estimates. Based on nucleotide or amino acid sequences, our approach accurately predicts the topology, branch lengths, and root positioning of prokaryotic family trees.

bioinformatics↗