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 spirochaete-like 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.

Figure 1

Diagram of structures common to all motile cilia and flagella. Longitudinal view to the left shows the relationship between the axoneme and basal body, and the location of intraflagellar transport (IFT) motors between axonemal doublet microtubules and the flagellar membrane. Transition fibers attached to the basal body separate the flagellar membrane domain from the rest of the cell membrane. Cross sectional views to the right show structures in flagella, including the nine outer doublet and two single central pair microtubules (top) and the nine triplet microtubules of basal bodies (bottom).

Figure 2

Diagram of probable evolutionary divergence that generated all existing branches of eukaryotic organisms. Under the name of each branch or clade is a the name of a representative genus in that clade that contains species with typical motile 9+2 flagella. Based on recent studies of rare gene fusion events, as well as more traditional sequence comparisons, the entire tree is divided into two superclades, unikonts and bikonts.

Figure 3

Proposed steps in the transition from an early eukaryote, with a polarized morphology based on asymmetric placement of a microtubule organizing center, but lacking flagella (left), through an intermediate with a protoflagellum that supported gliding and limited bending (center), to the last common eukaryotic ancestor, with a fully developed, motile 9+2 flagellum (right).