The Evolution of Eukaryotic Cilia and Flagella as Motile and Sensory Organelles

Abstract

Eukaryotic cilia and flagella are motile organelles built on a scaffold of doublet microtubules and powered by dynein ATPase motors. Some thirty years ago, two competing views were presented to explain how the complex machinery of these motile organelles had evolved. Overwhelming evidence now refutes the hypothesis that they are the modified remnants of symbiotic spirochaetelike prokaryotes, and supports the hypothesis that they arose from a simpler cytoplasmic microtubule-based intracellular transport system. However, because intermediate stages in flagellar evolution have not been found in living eukaryotes, a clear understanding of their early evolution has been elusive. Recent progress in understanding phylogenetic relationships among present day eukaryotes and in sequence analysis of flagellar proteins have begun to provide a clearer picture of the origins of doublet and triplet microtubules, flagellar dynein motors, and the 9+2 microtubule architecture common to these organelles. We summarize evidence that the last common ancestor of all eukaryotic organisms possessed a 9+2 flagellum that was used for gliding motility along surfaces, beating motility to generate fluid flow, and localized distribution of sensory receptors, and trace possible earlier stages in the evolution of these characteristics. Keywordscilia; flagella; motility; axoneme; microtubule; dynein; intraflagellar transport; central pair; radial spoke; tubulin Evidence for the presence of a 9+2, motile, sensory organelle in the last common eukaryotic ancestor As summarized in Figure 1, typical cilia and flagella (hereafter called flagella, there being no consistent structural or functional difference between organelles with these two designations) are motile projections oriented perpendicular to the cell surface, but they vary in length, in number per cell, and in the patterns of motility that they produce. They are composed of a cylinder (the axoneme) of nine doublet microtubules surrounding two single microtubules and are covered by the cell membrane. Between each pair of flagellar doublets are rows of axonemal dynein ATPases, which power the bending of these organelles, and extending toward the center of the cylinder are radial spokes, which touch upon a central apparatus and regulate axonemal dyneins. This central element consists of two single microtubules, assembled from a unique nucleating site 1 , plus many interconnecting microtubule-associated proteins (reviewed in ref.2). Together they form a structure that provides a cylindrical surface apposing the ends of the radial spokes 3 . mitcheld@upstate.edu, NIH Public Access The nine doublets assemble from a much shorter cylinder of nine triplet microtubules, the basal body or centriole, which is anchored to the cell surface and stabilized in the cytoplasm by other cytoskeletal elements. Basal bodies that anchor flagella are often interchangeable during the cell cycle with centrioles 4 , and these two names should be considered as two functional descriptions for the same structure....

Regulation of a heterodimeric kinesin-2 through an unprocessive motor domain that is turned processive by its partner

“…The question why nature combined two different polypeptide chains to create a heterodimeric motor specifically for ciliary function early in the evolution is intriguing (16,17). To dissect the contribution of the individual heads to the overall processivity in the wild-type KLP11/KLP20 motor, we expressed chimeras containing two identical heads.…”

“…Kinesin-2 apparently coevolved with the ciliary machinery (16,17). However, the evolutionary advantage of combining two different motor proteins is not yet fully understood.…”

Exploring the evolutionary history of centrosomes

“…For instance, centrioles and cilia are entirely missing in Filasteria and Nucleariida, which use actin-based filopodia to crawl along a substrate (figure 1) [45,51,52,55,56,63]. A possible scenario is that the last common ancestor of all Amorphea or even of all eukaryotes was capable of both flagellar and actin-based motility, and different lineages lost one or the other (or both) while adapting to their specific environment [26,27,[64][65][66]. It is thus necessary when attempting to reconstitute the evolutionary history of the microtubule cytoskeleton to consider these aspects as well.…”

Involvement of redox- and phosphorylation-dependent pathways in osmotic adaptation in sperm cells of euryhaline tilapia

“…It should be noted, however, that the roles of cilia and flagella differ: whereas the former play many roles in cell signalling and in the maintenance of cellular homeostasis (reviewed by Bisgrove and Yost, 2006), the latter act to propel sperm to unfertilised eggs. The available evidence suggests that flagella may have evolved from cilia and subsequently developed specific features (Mitchell, 2007). Based on previous studies, it seems reasonable that signals regulating motility and acclimatisation of in these two organelles may differ.…”