The
evolutionIn biology, evolution is change in the genetic material of a population of organisms from one generation to the next. Though changes produced in any one generation are normally small, differences accumulate with each generation and can, over time, cause substantial changes in the population, a...
of flagella is of great interest to
biologistA biologist is a scientist devoted to and producing results in biology through the study of life.Typically biologists study organisms and their relationship to their environment. Biologists involved in basic research attempt to discover underlying mechanisms that govern how organisms work...
s because the three known varieties of flagella (
eukaryoticA eukaryote is an organism whose cells contain complex structures enclosed within membranes. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear envelope, within which the genetic material is carried...
, bacterial, and archaebacterial) each represent an extremely sophisticated cellular structure that requires the interaction of many different finely-tuned systems.
There are two competing groups of models for the evolutionary origin of the
eukaryoticA eukaryote is an organism whose cells contain complex structures enclosed within membranes. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear envelope, within which the genetic material is carried...
flagellum (referred to as
ciliumA cilium is an organelle found in eukaryotic cells. Cilia are tail-like projections.There are two types of cilia: motile cilia and non-motile, or primary, cilia, which typically serve as sensory organelles...
below to distinguish it from its bacterial counterpart).
These models argue some version of the idea that the cilium evolved from a symbiotic spirochete that attached to a primitive eukaryote or archaebacterium (
archaeaThe Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon . They have no cell nucleus or any other organelles within their cells...
).
The
evolutionIn biology, evolution is change in the genetic material of a population of organisms from one generation to the next. Though changes produced in any one generation are normally small, differences accumulate with each generation and can, over time, cause substantial changes in the population, a...
of flagella is of great interest to
biologistA biologist is a scientist devoted to and producing results in biology through the study of life.Typically biologists study organisms and their relationship to their environment. Biologists involved in basic research attempt to discover underlying mechanisms that govern how organisms work...
s because the three known varieties of flagella (
eukaryoticA eukaryote is an organism whose cells contain complex structures enclosed within membranes. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear envelope, within which the genetic material is carried...
, bacterial, and archaebacterial) each represent an extremely sophisticated cellular structure that requires the interaction of many different finely-tuned systems.
The eukaryotic flagellum
There are two competing groups of models for the evolutionary origin of the
eukaryoticA eukaryote is an organism whose cells contain complex structures enclosed within membranes. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear envelope, within which the genetic material is carried...
flagellum (referred to as
ciliumA cilium is an organelle found in eukaryotic cells. Cilia are tail-like projections.There are two types of cilia: motile cilia and non-motile, or primary, cilia, which typically serve as sensory organelles...
below to distinguish it from its bacterial counterpart).
Symbiotic/endosymbiotic/exogenous models
These models argue some version of the idea that the cilium evolved from a symbiotic spirochete that attached to a primitive eukaryote or archaebacterium (
archaeaThe Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon . They have no cell nucleus or any other organelles within their cells...
). The modern version of the hypothesis was first proposed by
Lynn MargulisLynn Margulis is an American biologist and University Professor in the Department of Geosciences at the University of Massachusetts Amherst...
(as Sagan (1967): Margulis was the first wife of the late
Carl SaganCarl Edward Sagan was an American astronomer, astrochemist, author, and highly successful popularizer of astronomy, astrophysics and other natural sciences...
). 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 chloroplastsThe endosymbiotic theory concerns the origins of mitochondria and plastids , which are organelles of eukaryotic cells. According to this theory, these organelles originated as separate prokaryotic organisms that were taken inside the cell as endosymbionts...
.
The primary point in favor of the symbiotic hypothesis is that there are eukaryotes that use symbiotic spirochetes as their
motilityMotility is a biological term which refers to the ability to move spontaneously and actively, consuming energy in the process. It can apply to either single-celled or multicellular organisms. Motile marine animals are commonly called free-swimming...
organelleIn cell biology, an organelle is a specialized subunit within a cell that has a specific function, and is usually separately enclosed within its own lipid membrane....
s (some
parabasalidThe parabasalids are group of flagellate protozoa, most of which are symbiotic in animals. These include a variety of forms found in the guts of termites and cockroaches, many of which have symbiotic bacteria that help them digest wood. Some other species are human pathogens.-Characteristics:The...
s inside
termiteThe termites are a group of eusocial insects usually classified at the taxonomic rank of order Isoptera . Along with ants and some bees and wasps which are all placed in the separate order Hymenoptera, termites divide labour among gender lines, produce overlapping generations and take care of...
guts, such as
Mixotricha and
TrichonymphaTrichonympha is a genus of parabasalian protists that live in the intestines of many, if not most, termite species. They are important symbiotes, in that they break down the cellulose in the wood and plant fibers their hosts eat....
). 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
tubulinTubulin is one of several members of a small family of globular proteins. The most common members of the tubulin family are α-tubulin and β-tubulin, the proteins that make up microtubules. Each has a molecular weight of approximately 55 kiloDaltons. Microtubules are assembled from dimers of α- and...
to the bacterial replication/
cytoskeletalThe cytoskeleton is a cellular "scaffolding" or "skeleton" contained within the cytoplasm. The cytoskeleton is present in all cells; it was once thought this structure was unique to eukaryotes, but recent research has identified the prokaryotic cytoskeleton...
protein FtsZ is a major argument against Margulis, as FtsZ is apparently found native in
archaeaThe Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon . They have no cell nucleus or any other organelles within their cells...
, providing an endogenous ancestor to tubulin (as opposed to Margulis' hypothesis, that an archaea acquired tubulin from a symbiotic spirochete).
At present the symbiotic hypothesis for the origin of cilia seems to be limited to Margulis and a few of her associates. Margulis is, though, still strongly promoting and publishing a revised version of her hypothesis (Margulis' 1998 book
Symbiotic planet: a new look at evolution has some frank autobiographical comments about her support of the symbiotic hypothesis for the origin of the cilium).
Endogenous/autogenous/direct filiation models
Contrasting with the symbiotic models, these models argue that cilia developed from pre-existing components of the eukaryotic cytoskeleton (which has
tubulinTubulin is one of several members of a small family of globular proteins. The most common members of the tubulin family are α-tubulin and β-tubulin, the proteins that make up microtubules. Each has a molecular weight of approximately 55 kiloDaltons. Microtubules are assembled from dimers of α- and...
and
dyneinDynein is a motor protein in cells which converts the chemical energy contained in ATP into the mechanical energy of movement. Dynein transports various cellular cargo by "walking" along cytoskeletal microtubules towards the minus-end of the microtubule, which is usually oriented towards the cell...
—also used for other functions) as an extension of the
mitotic spindleIn cell biology, the spindle apparatus is the structure that separates the chromosomes into the daughter cells during cell division. It is part of the cytoskeleton in eukaryotic cells...
apparatus. The connection can still be seen, first in the various early-branching single-celled eukaryotes that have a
microtubuleMicrotubules are one of the components of the cytoskeleton. They have a diameter of 25 nm and length varying from 200 nanometers to 25 micrometers. Microtubules serve as structural components within cells and are involved in many cellular processes including mitosis, cytokinesis, and vesicular...
basal body.A basal body is an organelle formed from a centriole, a short cylindrical array of microtubules. It is found at the base of a eukaryotic undulipodium and serves as a nucleation site for the growth of the axoneme microtubules...
, 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
centrioleA centriole is a barrel-shaped cell structure found in most animal eukaryotic cells, though absent in higher plants and most fungi. The walls of each centriole are usually composed of nine triplets of microtubules...
, 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.
The bacterial flagellum
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 systemType three secretion system is a protein structure, an organelle, found in several Gram-negative bacteria....
.
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 plaguePlague is a deadly infectious disease caused by the enterobacteria Yersinia pestis . Plague is a zoonotic, primarily carried by rodents and spread to humans via fleas. Plague is notorious throughout history, due to the unrivaled scale of death and devastation it brought...
bacterium
Yersinia pestisYersinia pestis is a Gram-negative rod-shaped bacterium belonging to the family Enterobacteriaceae. It is a facultative anaerobe that can infect humans and other animals....
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. 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
evolvedNatural selection is the process by which heritable traits that make it more likely for an organism to survive and successfully reproduce become more common in a population over successive generations...
from a simpler bacterial secretion system.
The archaeal flagellum
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 (
piliright|thumb|350px|Schematic drawing of bacterial conjugation. 1- Donor cell produces pilus. 2- Pilus attaches to recipient cell, brings the two cells together. 3- The mobile plasmid is nicked and a single strand of DNA is then transferred to the recipient cell...
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.
Further research
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—what are the most deeply branching organisms in each domain, and what are the interrelationships between the domains (see
Last universal ancestorThe last universal ancestor is the most recent organism from which all organisms now living on Earth descend. Thus it is the most recent common ancestor of all current life on Earth...
)?
External links