Archaellum

Abstract

Each of the three domains of life contains its own unique swimming apparatus. The archaellum (formerly called archaeal flagellum) is a unique, ‘tail‐like’ structure used for motility by single‐celled organisms belonging to the domain Archaea. Although archaella are functionally similar to the flagella found on bacteria, they differ significantly in structure and mode of assembly. Archaella are evolutionarily related to type IV pili, and each of the two systems shares several key homologues required for assembly of the respective structures. Recent studies have contributed much to our knowledge concerning the regulation of the operon encoding the archaellum proteins. In addition, the elucidation of the structures of most of the Fla proteins involved in archaella structure and function, coupled with detailed atomic models of the archaellum, including the motor, has provided major insights into how this unique motility organelle is assembled and functions, often in harsh environments inhabited by many archaea.

Key Concepts

  • Each of the three domains of life has a unique motility apparatus, which have recently been assigned distinct names (Archaea: archaellum; Bacteria: flagellum and Eukaryotes: cilium).
  • The archaellum is functionally equivalent to flagellum but is evolutionarily related to a type IV pilus, with the archaella and type IV pili systems sharing important homologues.
  • Archaea have the ability to regulate the synthesis of archaella depending on growth conditions, such as available nutrients and temperature.
  • There can be crosstalk in the regulation of archaella with adhesive pili, allowing the cells under certain conditions to make only one type of appendage, either for swimming or adhesion.
  • N‐Glycosylation of the major filament proteins, the archaellins, is widespread and essential under normal conditions for assembly of filaments.
  • The ATPase responsible for assembly of the archaellins into the filament, that is, FlaI, is also responsible for the hydrolysis of ATP that powers the rotation of archaella.
  • In many archaea, the archaellum interacts with a bacterial‐like chemotaxis system that requires novel chemotaxis proteins to act as adaptors to connect the systems.
  • Not all archaellated species have an associated chemotaxis system.
  • Knowledge of the structure and assembly of archaella has greatly increased in the past 5 years with atomic models of several archaella structures as well as structures of most of the individual archaella proteins and their interaction partners.

Keywords: Archaea; N‐linked glycosylation; type IV pilus; Methanococcus; Sulfolobus; motor; signal peptide; motility; biofilm; chemotaxis

Figure 1. Electron micrographs showing archaellated cells of Methanococcus maripaludis, Sulfolobus acidocaldarius and purified archaella from Methanococcus voltae. Arrows in (a) and (b) point to archaella. Circle in (c) encompasses the curved proximal regions of several archaella which end in a knob‐like structure. Bars equal 500 nm. Archaella in (c) are 12 nm in diameter. (a) Ding et al. . Licensed under CC BY. (b) Courtesy of Shamphavi Sivabalasarma. (c) Courtesy of Dr. Aizawa.
Figure 2. Organisation of fla operons of select archaea including ones that have been a focus of archaellum structure, function, regulation and/or chemotaxis. Genes in black are chemotaxis genes, while those depicted in white are genes of unknown function. Hfx. volcanii has two copies of flaD (flaD1 and flaD2) located in operons adjacent to the fla operon. Hb. salinarum has five archaellin genes. flaA1 and flaA2 are cotranscribed but located at a site distinct from the fla operon.
Figure 3. Current archaellum structure and assembly model featuring atomic structures and class averages of the individual Fla proteins. The membrane protein FlaJ forms the archaellum assembly platform in the cytoplasmic membrane. FlaI, the hexameric ATPase (PDB: 4II7), interacts with FlaH (PDB: 4YDS) and FlaX (2D class average of S. acidocaldarius FlaXc taken from Chaudhury et al. ) to form the cytoplasmic part of the archaellum motor. Periplasmic FlaG (PDB: 5TUH) loses its membrane domain in order to build into a filament that is capped off by a FlaG–FlaF (PDB: 5TUG) complex. The FlaG–FlaF complex binds to the S‐layer, thus acting as the stator for the rotating machinery. The archaellin FlaB (PBD: 5O4U) assembles into the actual archaellum filament that eventually rotates to drive the cell forward. FlaB maintains its membrane domain that serves as hydrophobic core of the mature filament. Chaudhury et al. . Reproduced with permission of John Wiley & Sons.
Figure 4. Composite model of the archaellum machinery, including the motor, in Pyrococcus furiosus. The archaellum filament is composed of multiple copies of a single archaellin FlaB0. Light blue, FlaB0 monomers and filament (from helical reconstruction); hazy magenta, S‐layer; solid yellow, blue, green and purple, motor complex; hazy blue, cell membrane; hazy green, polar cap; solid orange, hexagonal protein array (from different subtomogram averages). Putative positions of protein subunits are indicated. The membrane protein FlaJ is almost completely embedded in the cytoplasmic membrane and, due to the high contrast of the lipid bilayer, is invisible in the tomograms. Dashed grey lines, putative interaction with polar cap. Daum et al. . Licensed under CC BY.
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Further Reading

Albers SV and Jarrell KF (2015) The archaellum: how archaea swim. Frontiers in Microbiology 6: 23.

Berry J‐E and Pelicic V (2015) Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives. FEMS Microbiology Reviews 39: 134–154.

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Jarrell KF, Ding Y, Nair DB and Siu S (2013) Surface appendages of archaea: structure, function, genetics and assembly. Life (Basel) 3: 86–117.

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Nair DB and Jarrell KF (2015) Pilin processing follows a different temporal route than that of archaellins in Methanococcus maripaludis. Life (Basel) 5: 85–101.

Pohlschroder M, Ghosh A, Tripepi M and Albers SV (2011) Archaeal type IV pilus‐like structures–evolutionarily conserved prokaryotic surface organelles. Current Opinion in Microbiology 14: 357–363.

Schlesner M, Miller A, Besir H, et al. (2012) The protein interaction network of a taxis signal transduction system in a halophilic archaeon. BMC Microbiology 12: 272.

van Wolferen M, Orell A and Albers SV (2018) Archaeal biofilm formation. Nature Reviews Microbiology 16: 699–713.

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Jarrell, Ken F, Tripp, Patrick, and Albers, Sonja‐Verena(May 2020) Archaellum. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000386.pub3]