Novel genes arise from genomic deletions across the bacterial tree of life

Abstract

Bacteria are hosts to enormous genic diversity. How new genes emerge, functionalize, and spread remain longstanding questions. Here, we explore a mechanism by which adaptive deletions fuse distant gene fragments. Unlike other gene birth mechanisms that begin with rare, neutral mutations, these "deletion-born fusions" reach high frequency by hitch-hiking on the deletion. The deletion-driven proliferation of the fusion prolongs the mutational supply within these genes before loss, providing additional opportunities for neofunctionalization. We document one such gene fixing and expressing in a long-term E. coli evolution experiment, and identify additional fusion events in the Mycobacterium tuberculosis-bovis split. Finally, we develop a scalable systematic screen to detect these genes in all 2.4 million public single-isolate genomes and identify deletion-born fusions across the bacterial tree of life. These findings challenge the notion that deletions are solely destructive and highlight their role as potential catalysts for evolutionary innovation.