Rapid functional activation of a horizontally transferred eukaryotic gene in a bacterial genome in the absence of selection

Horizontal gene transfer has occurred between organisms of all domains of life and contributed substantially to genome evolution in both prokaryotes and eukaryotes. Phylogenetic evidence suggests that eukaryotic genes horizontally transferred to bacteria provided useful new gene functions that improved metabolic plasticity and facilitated adaptation to new environments. How these eukaryotic genes evolved into functional bacterial genes is not known. Here, we have conducted a genetic screen to identify the mechanisms involved in functional activation of a eukaryotic gene after its transfer into a bacterial genome. We integrated a eukaryotic selectable marker gene cassette driven by expression elements from the red alga Porphyridium purpureum into the genome of Escherichia coli. Following growth under non-selective conditions, gene activation events were indentified by antibiotic selection. We show that gene activation in the bacterial recipient occurs at high frequency and involves two major types of spontaneous mutations: deletion and gene amplification. We further show that both mechanisms result in promoter capture and are frequently triggered by microhomology-mediated recombination. Our data suggest that horizontally transferred genes have a high probability of acquiring functionality, resulting in their maintenance if they confer a selective advantage.