The last bacterial common ancestor encoded a complex flagellum

Abstract

Bacterial flagella are rotary nanomachines that enable motility in diverse environments. Although more than 40 genes are required to assemble, operate, and regulate a functional flagellum in model organisms, only 24 flagellar genes have previously been inferred to be conserved across bacteria. This discrepancy raises a fundamental question: did the last bacterial common ancestor encode a simpler, partial flagellum that was elaborated later in a lineage-specific manner, or does the apparent absence of conserved components reflect limitations in detecting highly diverged homologs? Here we combine large-scale profile- and sequence-based searches across a comprehensive bacterial genome set with conserved sequence signatures, gene-tree clustering and flagellar gene-neighborhood evidence to reconstruct the ancestral complexity of bacterial flagellar systems. We identify 28 additional flagellar gene families whose distributions and evolutionary histories support an origin before major bacterial diversification, yielding a 52-gene ancestral flagellum. The ancestral flagellum included all proteins of the secretion/export apparatus, basal body, axial components, motor-force generators and regulatory checkpoints required to build and operate a functional, contemporary flagellum. These findings revise models of early bacterial evolution and overturn the notion that the ancestral flagellum was genetically minimal. Instead, they suggest that the last bacterial common ancestor possessed a highly complex flagellar system comprising more components than are typically found in extant bacteria, many of whose flagella appear to have been shaped by lineage-specific gene loss.