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

TL;DR

This study shows that E. coli can rapidly adapt to new environments through the acquisition of a single DNA segment, with most phenotypic innovations arising from such simple genetic changes, highlighting the efficiency of horizontal gene transfer.

Contribution

It demonstrates that all observed phenotypic innovations in E. coli arose from single DNA segment acquisitions, challenging the idea that complex adaptations require multiple steps.

Findings

97% of phenotypes can be transferred via a single DNA segment

All 3,363 phenotypic innovations involved only one DNA segment acquisition

10.6% of adaptations relied on earlier DNA acquisitions in the phylogeny

Abstract

Even closely related prokaryotes show an astounding diversity in their ability to grow in different nutritional environments. Mechanistically, this diversity arises predominantly through horizontal gene transfer, the exchange of DNA between individuals from different strains. It has been hypothesized that complex metabolic adaptations--those requiring the acquisition of multiple distinct DNA segments--can evolve via selectively neutral intermediate steps; an alternative explanation rests on the existence of intermediate environments that make each individual DNA acquisition adaptive. However, it is unclear how important changing environments are compared to neutral explorations of phenotype space; 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.