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Even closely related prokaryotes show an astounding diversity in theirability to grow in different nutritional environments. Mechanistically, thisdiversity arises predominantly through horizontal gene transfer, the exchangeof DNA between individuals from different strains. It has been hypothesizedthat complex metabolic adaptations--those requiring the acquisition of multipledistinct DNA segments--can evolve via selectively neutral intermediate steps;an alternative explanation rests on the existence of intermediate environmentsthat make each individual DNA acquisition adaptive. However, it is unclear howimportant changing environments are compared to neutral explorations ofphenotype space; more fundamentally, it is unknown what fraction of metabolicadaptations are indeed complex. Here, we use metabolic network simulations toshow that all 3,363 phenotypic innovations observed in the evolutionary historyof 53 E. coli strains arose through the acquisition of a single DNA segment;while we found no evidence for the contribution of selectively neutralprocesses, 10.6% of adaptations to previously unviable environments relied onthe support of DNA acquisitions on earlier phylogenetic branches. 97.0% of allmetabolic phenotypes accessible for the E. coli pan-genome could be bestowed onany ancestral strain by transferring a single DNA segment from one of theextant strains. These results demonstrate an amazing ability of the E. colilineage to quickly adapt to previously inaccessible environments through asingle DNA acquisition, an ability likely to be mirrored in other clades ofgeneralist bacteria.

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