Evolution of flagella
Encyclopedia
The evolution
of flagella is of great interest to biologist
s because the three known varieties of flagella (eukaryotic
, bacteria
l, and archaea
l) each represent a sophisticated cellular structure that requires the interaction of many different systems.
flagellum (referred to as cilium
below to distinguish it from its bacterial counterpart).
). 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
.
The primary point in favor of the symbiotic hypothesis is that there are eukaryotes that use symbiotic spirochetes as their motility
organelle
s (some parabasalid
s 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/cytoskeletal
protein FtsZ is a major argument against Margulis, as FtsZ is apparently found native in archaea
, 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.
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.
.
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. 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.
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.
)?
Evolution
Evolution is any change across successive generations in the heritable characteristics of biological populations. Evolutionary processes give rise to diversity at every level of biological organisation, including species, individual organisms and molecules such as DNA and proteins.Life on Earth...
of flagella is of great interest to biologist
Biologist
A 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 (eukaryotic
Eukaryote
A eukaryote is an organism whose cells contain complex structures enclosed within membranes. Eukaryotes may more formally be referred to as the taxon Eukarya or Eukaryota. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear...
, bacteria
Bacteria
Bacteria are a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria have a wide range of shapes, ranging from spheres to rods and spirals...
l, and archaea
Archaea
The Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon...
l) each represent a sophisticated cellular structure that requires the interaction of many different systems.
Eukaryotic flagellum
There are two competing groups of models for the evolutionary origin of the eukaryoticEukaryote
A eukaryote is an organism whose cells contain complex structures enclosed within membranes. Eukaryotes may more formally be referred to as the taxon Eukarya or Eukaryota. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear...
flagellum (referred to as cilium
Cilium
A cilium is an organelle found in eukaryotic cells. Cilia are slender protuberances that project from the much larger cell body....
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 (archaeaArchaea
The Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon...
). The modern version of the hypothesis was first proposed by Lynn Margulis
Lynn Margulis
Lynn Margulis was an American biologist and University Professor in the Department of Geosciences at the University of Massachusetts Amherst. She is best known for her theory on the origin of eukaryotic organelles, and her contributions to the endosymbiotic theory, which is now generally accepted...
. 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
Endosymbiotic theory
The endosymbiotic theory concerns the mitochondria, plastids , and possibly other organelles of eukaryotic cells. According to this theory, certain organelles originated as free-living bacteria that were taken inside another cell as endosymbionts...
.
The primary point in favor of the symbiotic hypothesis is that there are eukaryotes that use symbiotic spirochetes as their motility
Motility
Motility is a biological term which refers to the ability to move spontaneously and actively, consuming energy in the process. Most animals are motile but the term applies to single-celled and simple multicellular organisms, as well as to some mechanisms of fluid flow in multicellular organs, in...
organelle
Organelle
In 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 bilayer....
s (some parabasalid
Parabasalid
The 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 termite
Termite
Termites are a group of eusocial insects that, until recently, were classified at the taxonomic rank of order Isoptera , but are now accepted as the epifamily Termitoidae, of the cockroach order Blattodea...
guts, such as Mixotricha and Trichonympha
Trichonympha
Trichonympha is a genus of parabasalian protists that live in the intestines of many, if not most, termite species. They are 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 tubulin
Tubulin
Tubulin 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/cytoskeletal
Cytoskeleton
The cytoskeleton is a cellular "scaffolding" or "skeleton" contained within a cell's cytoplasm and is made out of protein. The cytoskeleton is present in all cells; it was once thought to be 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 archaea
Archaea
The Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon...
, 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.
Endogenous, autogenous and 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
Tubulin 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 dynein
Dynein
Dynein 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 spindle
Mitotic spindle
In cell biology, the spindle fibers are 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 microtubule
Microtubule
Microtubules are a component of the cytoskeleton. These rope-like polymers of tubulin can grow as long as 25 micrometers and are highly dynamic. The outer diameter of microtubule is about 25 nm. Microtubules are important for maintaining cell structure, providing platforms for intracellular...
basal body
Basal body
A basal body is an organelle formed from a centriole, and 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 centriole
Centriole
A Centriole is a barrel-shaped cell structure found in most animal eukaryotic cells, though it is 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.
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
Type three secretion system is a protein appendage 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 plague
Bubonic plague
Plague is a deadly infectious disease that is caused by the enterobacteria Yersinia pestis, named after the French-Swiss bacteriologist Alexandre Yersin. Primarily carried by rodents and spread to humans via fleas, the disease is notorious throughout history, due to the unrivaled scale of death...
bacterium Yersinia pestis
Yersinia pestis
Yersinia pestis is a Gram-negative rod-shaped bacterium. 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 evolved
Natural selection
Natural selection is the nonrandom process by which biologic traits become either more or less common in a population as a function of differential reproduction of their bearers. It is a key mechanism of evolution....
from a simpler bacterial secretion system.
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. (piliPilus
right|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 ancestorLast universal ancestor
The last universal ancestor , also called the last universal common ancestor , or the cenancestor, 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...
)?