Each of the three Domains of life, Eukarya, Bacteria and Archaea, have swimming structures that were all originally called flagella, despite the fact that none were evolutionarily related to either of the other two. Surprisingly, this was true even in the two prokaryotic Domains of Bacteria and Archaea. Beginning in the 1980s, evidence gradually accumulated that convincingly demonstrated that the motility organelle in Archaea was unrelated to that found in Bacteria, but surprisingly shared significant similarities to type IV pili. This information culminated in the proposal, in 2012, that the ‘archaeal flagellum’ be assigned a new name, the archaellum. In this review, we provide a historical overview on archaella and motility research in Archaea, beginning with the first simple observations of motile extreme halophilic archaea a century ago up to state-of-the-art cryo-tomography of the archaellum motor complex and filament observed today. In addition to structural and biochemical data which revealed the archaellum to be a type IV pilus-like structure repurposed as a rotating nanomachine (Beeby et al. 2020), we also review the initial discoveries and subsequent advances using a wide variety of approaches to reveal: complex regulatory events that lead to the assembly of the archaellum filaments (archaellation); the roles of the various archaellum proteins; key posttranslational modifications of the archaellum structural subunits; evolutionary relationships; functions of archaella other than motility and the biotechnological potential of this fascinating structure. The progress made in understanding the structure and assembly of the archaellum is highlighted by comparing early models to what is known today.

Motile archaea swim by means of a molecular machine called the archaellum. This structure consists of a filament attached to a membrane-embedded motor. The archaellum is found exclusively in members of the archaeal domain, but the core of its motor shares homology with the motor of type IV pili (T4P). Here, we provide an overview of the different components of the archaellum machinery and hypothetical models to explain how rotary motion of the filament is powered by the archaellum motor.

Motile archaea are propelled by the archaellum, whose motor complex consists of the membrane protein ArlJ, the ATPase ArlI, and the ATP‐binding protein ArlH. Despite its essential function and the existence of structural and biochemical data on ArlH, the role of ArlH in archaellum assembly and function remains elusive. ArlH is a structural homolog of KaiC, the central component of the cyanobacterial circadian clock. Since autophosphorylation and dephosphorylation of KaiC are central properties for the function of KaiC, we asked whether autophosphorylation is also a property of ArlH proteins. We observed that both ArlH from the euryarchaeon Pyrococcus furiosus (PfArlH) and from the crenarchaeon Sulfolobus acidocaldarius (SaArlH) have autophosphorylation activity. Using a combination of single‐molecule fluorescence measurements and biochemical assays, we show that autophosphorylation of ArlH is closely linked to its oligomeric state when bound to hexameric ArlI. These experiments also strongly suggest that ArlH is a hexamer in its ArlI‐bound state. Mutagenesis of the putative catalytic residue (Glu‐57 in SaArlH) in ArlH results in a reduced autophosphorylation activity and abolished archaellation and motility in S. acidocaldarius, indicating that optimum phosphorylation activity of ArlH is essential for archaellation and motility.

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