The archaellum: how Archaea swim

Abstract

Recent studies on archaeal motility have shown that the archaeal motility structure is unique in several aspects. Although it fulfills the same swimming function as the bacterial flagellum, it is evolutionarily and structurally related to the type IV pilus. This was the basis for the recent proposal to term the archaeal motility structure the "archaellum." This review illustrates the key findings that led to the realization that the archaellum was a novel motility structure and presents the current knowledge about the structural composition, mechanism of assembly and regulation, and the posttranslational modifications of archaella.

Keywords: archaeal flagellum; archaellum; motility; motor complex; type IV pili.

FIGURE 1

(A) Negative stained electron microscopic image of Methanococcus maripaludis. Bar length 500 nm. Picture courtesy of S.-I. Aizawa and K. Uchida. (B) Current model of the crenarchaeal archaellum. After the pre-archaellin has been processed by PibD/FlaK, the motor complex assembles the filament. The motor complex is formed by the ring-forming scaffold protein FlaX in which FlaH and FlaI interact most probably with the integral membrane protein FlaJ. The dimeric soluble domain of FlaF interacts with the S-layer. FlaG most probably has a similar function as FlaF as it’s soluble domain has homologies to the one from FlaF.

FIGURE 2

Organization of archaella operons. Archaella operons of three of the archaeal kingdoms Crenarchaeota, Thaumarchaeota and Euryarchaeota are depicted. The fla genes are abbreviated using the respective letter of the fla gene. Homologous genes are shown in the same color. Genes of unknown function are depicted in white. In the strain where chemotaxis genes are adjacent to the archaellum operon they are partially depicted. MCP, methyl accepting chemotaxis protein; che genes, genes encoding parts of the chemosensory system; htrl, methyl accepting transducer.

FIGURE 3

The archaeal type IV prepilin peptidases. (A) Crystal structure of FlaK from M. maripaludis. Model was constructed with Pymol (www.pymol.org) using the pdb file 3SOX. The GXDG motif is indicated as well as the localization of the membrane. It is clear that the active site is directed toward the cytoplasmic side of the membrane where cleavage of the class III signal peptide occurs. (B) The N-terminal archaellin sequences of M. maripaludis, S. acidocaldarius, and Hfx. volcanii are shown. The arrow indicates the cleavage site and the blue box delineates the hydrophobic, membrane inserted part of the mature N-terminus of the proteins. FlaK is specific for the archaellins in M. maripaludis, whereas PibD processes a variety of class III signal peptide containing substrates in various archaea.

FIGURE 4

Overview of the factors that influence the expression of the S. acidocaldarius archaellum operon. The one component membrane factors ArnR/R1, as well as the biofilm regulator AbfR1, are positive regulators of the flaB promoter. The two kinases ArnC and ArnD (Saci_1193 and Saci_1694, respectively), here depicted as ePK (eukaryotic like protein kinase) phosphorylate ArnA and ArnB which leads to repression of flaB expression. Deletion mutants of the phosphatase PP2A have a hypermotile phenotype, however, the specific target of the phosphatase is not known.