Evolution of flagella
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The evolution of flagella is of great interest to biologists because the three known varieties of flagella (eukaryotic, bacterial, and archaeal) each represent a sophisticated cellular structure that requires the interaction of many different systems.
There are two competing groups of models for the evolutionary origin of the eukaryotic flagellum (referred to as cilium below to distinguish it from its bacterial counterpart). Recent studies on the microtubule organizing center (MTOC) suggest that the most recent ancestor of all eukaryotes already had a complex flagellar apparatus.
Endogenous, autogenous and direct filiation models
These models argue that cilia developed from pre-existing components of the eukaryotic cytoskeleton (which has tubulin and dynein – also used for other functions) as an extension of the mitotic spindle apparatus. The connection can still be seen, first in the various early-branching single-celled eukaryotes that have a microtubule basal body, where microtubules on one end form a spindle-like cone around the nucleus, while microtubules on the other end point away from the cell and form the cilium. A further connection is that the centriole, involved in the formation of the mitotic spindle in many (but not all) eukaryotes, is homologous to the cilium, and in many cases is the basal body from which the cilium grows.
An apparent intermediate stage between spindle and cilium would be a non-swimming appendage made of microtubules with a selectable function like increasing surface area, helping the protozoan to remain suspended in water, increasing the chances of bumping into bacteria to eat, or serving as a stalk attaching the cell to a solid substrate.
Regarding the origin of the individual protein components, an interesting paper on the evolution of dyneins shows that the more complex protein family of ciliary dynein has an apparent ancestor in a simpler cytoplasmic dynein (which itself has evolved from the AAA protein family that occurs widely in all archea, bacteria and eukaryotes). Long-standing suspicions that tubulin was homologous to FtsZ (based on very weak sequence similarity and some behavioral similarities) were confirmed in 1998 by the independent resolution of the 3-dimensional structures of the two proteins.
These models argue that the cilium evolved from a symbiotic spirochete that attached to a primitive eukaryote or archaebacterium (archaea). The modern version of the hypothesis was first proposed by Lynn Margulis. The hypothesis, though very well publicized, was never widely accepted by the experts, in contrast to Margulis' arguments for the symbiotic origin of mitochondria and chloroplasts. Margulis did strongly promote and publish versions of this hypothesis until the end of her life.
The primary point in favor of the symbiotic hypothesis is that there are eukaryotes that use symbiotic spirochetes as their motility organelles (some parabasalids inside termite guts, such as Mixotricha and Trichonympha). While this is an example of co-option and the flexibility of biological systems, none of the proposed homologies that have been reported between cilia and spirochetes have stood up to further scrutiny. The homology of tubulin to the bacterial replication and cytoskeletal protein FtsZ is a major argument against Margulis, as FtsZ alike protein (see Prokaryotic cytoskeleton) is apparently found natively in archaea, providing an endogenous ancestor to tubulin (as opposed to Margulis' hypothesis, that an archaea acquired tubulin from a symbiotic spirochete).
An approach to the evolutionary origin of the bacterial flagellum is suggested by the fact that a subset of flagellar components is similar to the Type III secretory and transport system.
All currently known nonflagellar Type III transport systems serve the function of injecting toxin into eukaryotic cells. It is hypothesised that the flagellum evolved from the type three secretory system. For example, the bubonic plague bacterium Yersinia pestis has an organelle assembly very similar to a complex flagellum, except that is missing only a few flagellar mechanisms and functions, such as a needle to inject toxins into other cells. The hypothesis that the flagellum evolved from the type three secretory system has been challenged by recent phylogenetic research that strongly suggests the type three secretory system evolved from the flagellum through a series of gene deletions. It is also a possibility that the flagellum could have evolved from a currently undiscovered system with similar flagellar traits or a currently extinct organelle/organism. As such, the type three secretory system supports the hypothesis that the flagellum evolved from a simpler bacterial secretion system.
The recently elucidated archaeal flagellum is analogous, not homologous, to the bacterial one. In addition to no sequence similarity being detected between the genes of the two systems, the archaeal flagellum appears to grow at the base rather than the tip, and is about 15 nanometers (nm) in diameter rather than 20. Sequence comparison indicates that the archaeal flagellum is homologous to Type IV pili. (pili are filamentous structures outside the cell). Interestingly, some Type IV pili can retract. Pilus retraction provides the driving force for a different form of bacterial motility called "twitching" or "social gliding" which allows bacterial cells to crawl along a surface. Thus Type IV pili can, in different bacteria, promote either swimming or crawling. Type IV pili are assembled through the Type II transport system. So far, no species of bacteria is known to use its Type IV pili for both swimming and crawling.
Testable outlines exist for the origin of each of the three motility systems, and avenues for further research are clear; for prokaryotes, these avenues include the study of secretion systems in free-living, nonvirulent prokaryotes. In eukaryotes, the mechanisms of both mitosis and cilial construction, including the key role of the centriole, need to be much better understood. A detailed survey of the various nonmotile appendages found in eukaryotes is also necessary.
Finally, the study of the origin of all of these systems would benefit greatly from a resolution of the questions surrounding deep phylogeny, as to what are the most deeply branching organisms in each domain, and what are the interrelationships between the domains.
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