Evolution of a family of molecular Rube Goldberg contraptions

Abstract

Case studies of the evolution of molecular machines remain scarce. One of the most diverse and widespread homologous families of machines is the type IV filament (TFF) superfamily, comprised of type IV pili, type II secretion systems (T2SSs), archaella, and other less-well-characterized families. These families have functions including twitching motility, effector export, rotary propulsion, nutrient uptake, DNA uptake, and even electrical conductance, but it is unclear how such diversity evolved from a common ancestor. In this issue, Denise and colleagues take a significant step toward understanding evolution of the TFF superfamily by determining a global phylogeny and using it to infer an evolutionary pathway. Results reveal that the superfamily predates the divergence of Bacteria and Archaea, and show how duplications, acquisitions, and losses coincide with changes in function. Surprises include that tight adherence (Tad) pili were horizontally acquired from Archaea and that T2SSs were relatively recently repurposed from type IV pili. Results also enable better understanding of the function of the ATPase family that powers the superfamily. The study highlights the role of tinkering by exaptation-the repurposing of pre-existing functions for new roles-in the diversification of molecular machines.

Fig 1. The global phylogeny of the TFF superfamily suggests their evolutionary pathway.

A schematic based on the results from Denise and colleagues [29] capturing salient branch topologies and selected protein acquisition and loss events anticipated by parsimony. The upper major clade represents archaeal TFF superfamily members; the lower major clade represents Bacteria. The phylogeny suggests that the TFF superfamily was present in the LUCA. Archaea and Bacteria evolved distinct TFF families based on nuanced changes in core and accessory components, and Tad pili were a horizontal transfer from Archaea to Bacteria. Black hexagons represent archaeal S-layer; green mesh represents bacterial peptidoglycan. Aap, archaeal adhesive pilus; Com, competence; Epd, EppA dependent; LUCA, last universal common ancestor; MSH, mannose-sensitive hemagglutinin; Tad, tight adherence; TFF, type IV filament; T2SS, type II secretion system; T4aP, type IVa pilus; T4bP, type IVb pilus; Ups, UV-inducible pilus.