Abstract

Processes of molecular innovation require tinkering and shifting in the function of existing genes. How this occurs in terms of molecular evolution at long evolutionary scales remains poorly understood. Here, we analyse the natural history of a vast group of membrane-associated molecular systems in Bacteria and Archaea—the type IV filament (TFF) superfamily—that diversified in systems involved in flagellar or twitching motility, adhesion, protein secretion, and DNA uptake. The phylogeny of the thousands of detected systems suggests they may have been present in the last universal common ancestor. From there, two lineages—a bacterial and an archaeal—diversified by multiple gene duplications, gene fissions and deletions, and accretion of novel components. Surprisingly, we find that the ‘tight adherence’ (Tad) systems originated from the interkingdom transfer from Archaea to Bacteria of a system resembling the ‘EppA-dependent’ (Epd) pilus and were associated with the acquisition of a secretin. The phylogeny and content of ancestral systems suggest that initial bacterial pili were engaged in cell motility and/or DNA uptake. In contrast, specialised protein secretion systems arose several times independently and much later in natural history. The functional diversification of the TFF superfamily was accompanied by genetic rearrangements with implications for genetic regulation and horizontal gene transfer: systems encoded in fewer loci were more frequently exchanged between taxa. This may have contributed to their rapid evolution and spread across Bacteria and Archaea. Hence, the evolutionary history of the superfamily reveals an impressive catalogue of molecular evolution mechanisms that resulted in remarkable functional innovation and specialisation from a relatively small set of components.

Highlights

  • New complex forms, functions, and molecular systems arise by the shift in function of elements that may have evolved to tackle different adaptive needs [1]

  • These models give a detailed account of Diversification of the type IV filament superfamily the genetic composition and organisation of the systems

  • We could not build models for type IVb pilus (T4bP) and mannose-sensitive hemagglutinin pilus (MSH) systems at this point because too few systems were described in the literature

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Summary

Introduction

New complex forms, functions, and molecular systems arise by the shift in function (cooption) of elements that may have evolved to tackle different adaptive needs [1]. A remarkable illustration of these processes is provided by the type IV filament (TFF) superfamily of bacterial and archaeal systems that include the type II secretion system (T2SS), the type IVa pilus (T4aP), the type IVb pilus (T4bP), the mannose-sensitive hemagglutinin pilus (MSH), the tight adherence (Tad) pilus, the competence pilus (Com), and the type IV-related pili in Archaea (Archaeal-T4P), which includes the archaeal flagella (archaellum) These systems have core homologous components, sometimes in multiple copies, and present similarities in terms of macromolecular architecture throughout Bacteria and Archaea (Fig 1) [12,13,14]. These systems were analysed using phylogenetic techniques to characterise the history of the TFF superfamily, clarify the relationships among its members, and decipher the molecular evolution mechanisms underlying its functional diversification. This integrative analysis provided a consistent scenario for the diversification of the superfamily involving processes of gene duplication, fission, transfer, accretion, and mutation

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