Archaellum

An **archaellum** (plural: *archaella*, formerly **archaeal flagellum**) is a unique whip-like structure on the cell surface of many archaea. The name was proposed in 2012 following studies that showed it to be evolutionarily and structurally different from the bacterial and eukaryotic flagella. The archaellum is functionally the same – it can be rotated and is used to swim in liquid environments. The archaellum was found to be structurally similar to the type IV pilus.

## History

In 1977, archaea were first classified as a separate group of prokaryotes in the three-domain system of Carl Woese and George E. Fox, based on the differences in the sequence of ribosomal RNA (16S rRNA) genes. This domain possesses numerous fundamental traits distinct from both the bacterial and the eukaryotic domains. Many archaea possess a rotating motility structure that at first seemed to resemble the bacterial and eukaryotic flagella. The flagellum (Latin for whip) is a lash-like appendage that protrudes from the cell. In the last two decades, it was discovered that the archaeal flagella, although functionally similar to bacterial and eukaryotic flagella, structurally resemble bacterial type IV pili. Bacterial type IV pili are surface structures that can be extended and retracted to give a twitching motility and are used to adhere to or move on solid surfaces; their "tail" proteins are called pilins. To underline these differences, Ken Jarrell and Sonja-Verena Albers proposed to change the name of the archaeal flagellum to archaellum.

## Structure

### Components

Most proteins that make up the archaellum are encoded within one genetic locus. This genetic locus contains 7-13 genes which encode proteins involved in either assembly or function of the archaellum. The genetic locus contains genes encoding archaellins (*flaA* and *flaB*) - the structural components of the filament - and motor components (*flaI*, *flaJ*, *flaH*). The locus furthermore encodes accessory proteins (*FlaG*, *FlaF*, *FlaX*) and signaling components (FlaC, FlaD, FlaE). Genetic analysis in different archaea revealed that each of these components is essential for assembly of the archaellum. Whereas most of the fla-associated genes are generally found in Euryarchaeota, one or more of these genes are absent from the fla-operon in Crenarchaeota. The prepilin peptidase (called PibD in crenarchaeota and FlaK in euryarchaeota) is essential for the maturation of the archaellins and is generally encoded elsewhere on the chromosome.

Functional characterization has only been performed for FlaI, a Type II/IV secretion system ATPase super-family member and PibD/FlaK. FlaI forms a hexamer which hydrolyses ATP and most likely generates energy to assemble the archaellum. PibD cleaves the N-terminus of the archaellins before they can be assembled. FlaH (PDB: 2DR3​) has a RecA-like fold and inactive ATPase domains. FlaH and FlaJ are the two other core components that together with FlaI to form a core platform/motor. FlaX acts as a scaffold around the motor in Crenarchaeota. The exact role of accessory proteins FlaF and FlaG is poorly understood. The genes coding for the signaling components such as flaC, flaD, flaE are only present in Euryarchaeota and interact with Chemotaxis proteins (e.g., CheY, CheD and CheC2) to sense environmental signals (such as exposure to light of specific wavelength, nutrient conditions etc.).

### Structure and assembly: type IV pilus and archaellum

In the 1980s, Dieter Oesterhelt’s laboratory showed for the first time that haloarchaea switch the rotation of their archaellum from clockwise to counterclockwise upon blue light pulses. This led microbiologists to believe that the archaeal motility structure is not only functionally, but also structurally reminiscent of bacterial flagella. However, in contrast to flagellins, archaellins are produced as preproteins which are processed by a specific peptidase prior to assembly. Their signal peptide is homologous to class III signal peptides of type IV prepilins that are processed in Gram-negative bacteria by the peptidase PilD. In crenarchaeota PibD and in euryarchaeota FlaK are PilD homologs, that are essential for the maturation of the archaellins. Furthermore, archaellins are N-glycosylated which has not been described for bacterial flagellins, where O-linked glycosylation is evident. Two other components of the archaellum assembly system, namely, FlaI and FlaJ are homologous to components of type IV pili, PilB and PilC, respectively. Moreover, the structure of the archaellum filament resembles archaeal and bacterial type IV pili as it has no central lumen excluding the possibility that it might assembled in a similar fashion like bacterial flagella via a type III secretion system. Additionally, it was demonstrated that the rotation of the archaellum is dependent on ATP concentration in the cell rather than PMF (proton motive force) as in the bacterial flagellum.

### Functional analogs

Despite the limited number of details presently available regarding the structure and assembly of archaellum, it has become increasingly evident from multiple studies that archaella play important roles in a variety of cellular processes in archaea. In spite of the structural dissimilarities with the bacterial flagellum, the main function thus far attributed for archaellum is swimming in liquid and semi-solid surfaces. Increasing biochemical and biophysical information has further consolidated the early observations of archaella mediated swimming in archaea. Like the bacterial flagellum, the archaellum also mediates surface attachment and cell-cell communication. However, unlike the bacterial flagellum archaellum has not shown to play a role in archaeal biofilm formation. In archaeal biofilms, the only proposed function is thus far during the dispersal phase of biofilm when archaeal cells escape the community using their archaellum to further initiate the next round of biofilm formation. Also, archaellum have been found to be able to have a metal-binding site.

## Notes

1. ↑ In some species, the names are given as FlgA and FlgB.