View source for Evolution of flagella

{{Short description|Origin of three known varieties of flagella}}
{{Use dmy dates|date=October 2023}}
{{evolutionary biology}}

The '''evolution of flagella''' is of great interest to [[biologist]]s because the three known varieties of [[flagella]] – ([[eukaryote|eukaryotic]], [[bacteria]]l, and [[archaea]]l) each represent a sophisticated cellular structure that requires the interaction of many different systems.{{Citation needed|date=October 2022}}

==Eukaryotic flagellum==
There are two competing groups of models for the evolutionary origin of the [[Eukaryote|eukaryotic]] flagellum (referred to as [[cilium]] below to distinguish it from its bacterial counterpart). Recent studies on the [[microtubule organizing center]] suggest that the most recent ancestor of all eukaryotes already had a complex flagellar apparatus.<ref>{{Cite journal |doi = 10.1111/tpj.12145|pmid = 23398214|title = Evolution of microtubule organizing centers across the tree of eukaryotes|journal = The Plant Journal|volume = 75|issue = 2|pages = 230–244|year = 2013|last1 = Yubuki|first1 = Naoji|last2 = Leander|first2 = Brian S.|doi-access = free}}</ref>

===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]]{{spaced ndash}} 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 [[Homology (biology)|homologous]] to the cilium, and in many cases ''is'' the basal body from which the cilium grows.

An intermediate stage between spindle and cilium would be a non-swimming appendage made of microtubules with a function subject to [[natural selection]], such as increasing surface area, helping the protozoan 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, a paper on the evolution of dyneins<ref>{{Cite journal|author=Gibbons IR |title=Dynein family of motor proteins: present status and future questions |journal=Cell Motility and the Cytoskeleton |volume=32 |issue=2 |pages=136–44 |year=1995 |pmid=8681396 |doi=10.1002/cm.970320214}}</ref><ref>{{Cite journal|vauthors=Asai DJ, Koonce MP |title=The dynein heavy chain: structure, mechanics and evolution |journal=Trends in Cell Biology |volume=11 |issue=5 |pages=196–202 |date=May 2001 |pmid=11316608 |doi=10.1016/S0962-8924(01)01970-5}}</ref> 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 archaea, 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.

===Symbiotic/endosymbiotic/exogenous models===
These models argue that the cilium evolved from a [[symbiotic]] [[Gracilicutes]] (ancestor of [[spirochete]] and [[Prosthecobacter]]) that attached to a primitive eukaryote or archaebacterium ([[archaea]]).

The modern version of the hypothesis was first proposed by [[Lynn Margulis]].<ref>{{Cite journal|author=Sagan L |title=On the origin of mitosing cells |journal=Journal of Theoretical Biology |volume=14 |issue=3 |pages=255–74 |date=March 1967 |pmid=11541392 |doi=10.1016/0022-5193(67)90079-3}}</ref> The hypothesis, though very well publicized, was never widely accepted by the experts, in contrast to Margulis' arguments for the [[Endosymbiotic theory|symbiotic origin of mitochondria and chloroplasts]]. Margulis did strongly promote and publish versions of this hypothesis until the end of her life.<ref>{{Cite book |first=Lynn |last=Margulis |title=Symbiotic planet: a new look at evolution |publisher=Basic Books |location=New York |year=1998 |isbn=978-0-465-07271-2 |oclc=39700477 |url=https://archive.org/details/symbioticplanetn00marg }}{{Page needed|date=September 2010}}</ref>

One primary point in favor of the symbiotic hypothesis was that there are eukaryotes that use symbiotic spirochetes as their [[motility]] [[organelle]]s (some [[parabasalid]]s inside [[termite]] guts, such as ''[[Mixotricha]]'' and ''[[Trichonympha]]'').  
This is an example of co-option and the flexibility of biological systems, and the proposed homologies that have been reported between cilia and spirochetes have stood up to further scrutiny.

Margulis' hypothesis suggests that an archaea acquired [[tubulin]] proteins from a [[eubacter]] ancestor of [[Prosthecobacter]]. However, the homology of [[tubulin]] to the bacterial replication and [[cytoskeleton|cytoskeletal]] protein [[FtsZ]] (see [[Prokaryotic cytoskeleton]]), which was apparently native in [[archaea]], suggesting an endogenous origin of tubulin rather than a symbiotic transfer.

==Bacterial flagellum==
{{microbial and microbot movement|biological motors}}

There is good evidence that the bacterial flagellum includes and might even be based on a [[Type three secretion system|Type III secretory and transport system]], given the similarity of proteins in both systems.<ref>{{cite journal | title=Adaptivity and dynamics in type III secretion systems | vauthors=Milne-Davies B, Wimmi S, Diepold A | journal=Molecular Microbiology | volume=115 | issue=3 | pages=395–411 | date=March 2021 | pmid=33251695 | doi=10.1111/mmi.14658 | doi-access=free }}</ref>

All currently known nonflagellar Type III transport systems serve the function of exporting (injecting) [[toxins|toxin]] into eukaryotic cells.  Similarly, flagella grow by exporting [[flagellin]] through the flagellar machinery. 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 it is missing only a few flagellar mechanisms and functions, such as a needle to inject toxins into other cells. As such, the type three secretory system supports the hypothesis that the flagellum [[natural selection|evolved]] from a simpler [[bacterial secretion system]].

However, the true relationship could be the reverse: recent phylogenetic research strongly suggests the type three secretory system evolved from the flagellum through a series of gene deletions.<ref>{{cite journal | pmid = 23028376 | date = 2012 | last1 = Abby | first1 = S. S. | last2 = Rocha | first2 = E. P. | title = The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems | journal = PLOS Genetics | volume = 8 | issue = 9 | article-number = e1002983 | doi = 10.1371/journal.pgen.1002983 | doi-access = free | pmc = 3459982 }}</ref>

[[Reactive oxygen species]] (ROS) generated by flagellation can cause oxidative damage to DNA and are mutagenic with researchers asking "Did the innovation of a functional flagellum impact either the short- or long-term rate of bacterial evolution?".<ref name="t665">{{cite journal |last=Bhattacharyya |first=Souvik |last2=Lopez |first2=Shelby |last3=Singh |first3=Abhyudai |last4=Harshey |first4=Rasika M. |year=2024 |title=Flagellar motility is mutagenic |journal=Proceedings of the National Academy of Sciences |publisher=Proceedings of the National Academy of Sciences |volume=121 |issue=41 |page= |doi=10.1073/pnas.2412541121 |issn=0027-8424 |doi-access=free|pmc=11474059 }}</ref>

===Eubacterial flagellum ===
Eubacterial flagellum is a multifunctional organelle. It is also one of a range of motility systems in bacteria. The structure of the organelle appears like a motor, shaft and a propeller.<ref name="Young&Taner2004">Young, Matt & [[Taner Edis|Edis, Taner]] (2004). ''Why Intelligent Design Fails: A Scientific Critique of the New Creationism'' {{ISBN|0-8135-3433-X}} Rutgers University press New Brunswick, New Jersey, and London.72-84.</ref> However, the structure of eubacterial flagellae varies based on whether their motor systems run on protons or sodium, and on the complexity of the flagellar whip.<ref>Berry, R. M., and J. P. Armitage. 1999. "The Bacterial Flagella Motor." Advances in Microbial Physiology {{ISBN|978-0-12-027749-0}}. v. 49: 291–337.</ref> The evolutionary origin of eubacterial flagellae is probably an example of indirect evolution. A hypothesis on the evolutionary pathway of the eubacterial flagellum argues that a secretory system evolved first, based around the SMC rod- and pore-forming complex. This is presumed to be the common ancestor of the type-III secretory system and the flagellar system. Then, an ion pump was introduced to this structure which improved secretion. The ion pump later became the motor protein. This was followed by the emergence of the proto-flagellar filament as part of the protein-secretion structure. Gliding-twitching motility arose at this stage or later and was then refined into swimming motility.<ref name="Young&Taner2004"/>

==Archaeal flagellum==
{{Further|Archaellum}}
The recently elucidated archaeal flagellum, or ''[[archaellum]]'', is [[Analogy (biology)|analogous]]—but not [[Sequence homology|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 [[nanometer]]s (nm) in diameter rather than 20.

Sequence comparison indicates that the archaeal flagellum is homologous to bacterial [[Type IV pili]], filamentous structures outside the cell.<ref>{{Cite journal|doi=10.1139/m94-011 |vauthors=Faguy DM, Jarrell KF, Kuzio J, Kalmokoff ML |title=Molecular analysis of archael flagellins: similarity to the type IV pilin-transport superfamily widespread in bacteria |journal=Canadian Journal of Microbiology |volume=40 |issue=1 |pages=67–71 |date=January 1994 |pmid=7908603}}</ref> Pilus retraction provides enables a different form of bacterial motility called "twitching" or "social gliding" which allows bacterial cells to crawl along a surface, They are assembled through the [[Type II secretion system]]. They can also promote swimming, but 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, as to what are the most deeply branching organisms in each domain, and what are the interrelationships between the domains.

==See also==

* [[Last universal ancestor]]

==References==
{{Reflist}}

==Further reading==
*{{Cite journal |first1=Tim |last1=Wong |first2=Arezou |last2=Amidi |first3=Alexandra |last3=Dodds |first4=Sara |last4=Siddiqi |first5=Jing |last5=Wang |first6=Tracy |last6=Yep |first7=Dorjee G. |last7=Tamang |first8=Milton H. |last8=Saier |year=2007 |title=Evolution of the Bacterial Flagellum: Cumulative evidence indicates that flagella developed as modular systems, with many components deriving from other systems |journal=Microbe |volume=2 |issue=7 |pages=335–40 |url=http://saier-144-51.ucsd.edu/~saier/bimm130/reading130/week4/paper4c.pdf |access-date=1 December 2009 |archive-url=https://web.archive.org/web/20120315064959/http://saier-144-51.ucsd.edu/~saier/bimm130/reading130/week4/paper4c.pdf |archive-date=15 March 2012 }}
*{{Cite news|first=Dan |last=Jones |date=16 February 2008 |title=Uncovering the evolution of the bacterial flagellum |url=https://www.newscientist.com/article/mg19726431.900-uncovering-the-evolution-of-the-bacterial-flagellum.html |work=[[New Scientist]] |access-date=1 December 2009}}
*{{Cite journal|vauthors=Hall JL, Ramanis Z, Luck DJ |title=Basal body/centriolar DNA: molecular genetic studies in Chlamydomonas |journal=Cell |volume=59 |issue=1 |pages=121–32 |date=October 1989 |pmid=2571418 |doi=10.1016/0092-8674(89)90875-1}}
*{{Cite journal|vauthors=Pallen MJ, Matzke NJ |title=From The Origin of Species to the origin of bacterial flagella |journal=Nature Reviews. Microbiology |volume=4 |issue=10 |pages=784–90 |date=October 2006 |pmid=16953248 |doi=10.1038/nrmicro1493}}
*{{Cite book |first=Lynn |last=Margulis |title=Symbiosis in cell evolution: life and its environment on the early Earth |publisher=W. H. Freeman |location=San Francisco |year=1981 |isbn=978-0-7167-1255-8 |oclc=6982472 |url=https://archive.org/details/symbiosisincelle00marg }}
*{{Cite journal|author=Margulis L |date=April 1993 |title=The Inheritance of Acquired Microbes |journal=Citation Classic Commentaries |volume=36 |issue=16 |pages=9–10 |url=http://www.garfield.library.upenn.edu/classics1993/A1993KK54300001.pdf}}

==External links==
*[https://web.archive.org/web/20091205220001/http://pandasthumb.org/archives/evolution/irreducible-complexity/flagellum-evolution/ Flagellum Evolution at The Panda's Thumb]
*{{Cite web|author=Matzke NJ |date=September 2006 |title=Evolution in (Brownian) space: a model for the origin of the bacterial flagellum |work=Talk Reason |url=http://www.talkdesign.org/faqs/flagellum.html |access-date=1 December 2009}}

{{Evolution}}

{{DEFAULTSORT:Evolution of Flagella}}
[[Category:Evolution by phenotype|Flagellum]]