A comprehensive history of motility and Archaellation in Archaea

Abstract

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.

Mechanisms for Electron Uptake by Methanosarcina acetivorans during Direct Interspecies Electron Transfer

“…The ability of GAC to rescue the archaellum-deficient strain to enable DIET is consistent with a possible role for archaella in long-range electron transport. However, other, more traditional roles of archaella, such as conferring motility and facilitating attachment ( 40 ), might also help cells locate a DIET partner and/or establish initial interspecies contact. In order to more definitively evaluate a role for the M. acetivorans archaellum in interspecies electron transfer, it will be necessary to follow the approach employed for evaluating the role of Geobacter e-pili in DIET ( 37 ) and construct a strain that expresses an archaellum of with potentially low conductivity.…”

Mechanisms for Electron Uptake byMethanosarcina acetivoransDuring Direct Interspecies Electron Transfer

“…The ability of GAC to rescue the archaella-deficient strain to enable DIET is consistent with a possible archaella role in long-range electron transport. However, other, more traditional roles of archaella, such as conferring motility and facilitating attachment (40) might also help cells locate a DIET partner and/or establish initial interspecies contact. In order to more definitively evaluate a role for the M. acetivorans archaellum in interspecies electron transfer it will be necessary to follow the approach employed for evaluating the role of Geobacter e-pili in DIET (37) and construct a strain that expresses an archaellum of with potentially low conductivity.…”

Towards Elucidating the Rotary Mechanism of the Archaellum Machinery

“…Archaella are found across various archaeal phyla, from the relatively well-characterised Euryarchaeota and Crenarchaeota to less understood organisms, such as the putative ectosymbionts of the DPANN superphylum ( Jarrell et al, 2021 ). The biogenesis of a functional archaellum requires the expression of 7–15 genes, which are usually organised in a cluster—the arl operon—plus a membrane-embedded aspartic acid protease, often encoded elsewhere in the chromosome ( Desmond et al, 2007 ; Pohlschröder et al, 2018 ; Jarrell et al, 2021 ). The aspartic acid protease ArlK/PibD is essential for motility, as it is responsible for cleavage of the class III signal peptide from the filament-forming archaellin subunits ( Bardy and Jarrell, 2002 , 2003 ; Albers et al, 2003 ).…”

“…In Crenarchaeota, a predicted membrane protein called ArlX is thought to form a cytosolic ring that serves as a scaffold for the motor ( Banerjee et al, 2012 ). In Euryarchaeota, ArlX is likely replaced by ArlCDE and in Thaumarchaeota by a yet to be identified protein ( Desmond et al, 2007 ; Jarrell et al, 2021 ).…”

“…In S. acidocaldarius , ArlJ is unstable in the absence of ArlX, indicating that the two proteins interact ( Lassak et al, 2012 ). ArlJ is presumably a platform protein during assembly and acts as a rotor that provides torque to the assembled archaellum filament ( Jarrell et al, 2021 ). Notably, the homologous PilC protein has been suggested to rotate during extension and retraction of Type 4 pili ( Chang et al, 2016 ), a mechanism which could conceivably have been adapted for the rotation of a filament during evolution.…”