A microorganism may have from one to many flagella. Agram-negative bacteriumHelicobacter pylori, for example, uses its flagella to propel itself through the stomach to reach themucous lining where it may colonise the epithelium and potentially cause gastritis, andulcers – a risk factor forstomach cancer.[5] In someswarming bacteria, the flagellum can also function as a sensoryorganelle, being sensitive to wetness outside the cell.[6]
Across thethree domains ofBacteria,Archaea, andEukaryota, the flagellum has a different structure, protein composition, and mechanism of propulsion but shares the same function of providing motility. TheLatin wordflagellum means "whip" to describe its lash-like swimming motion. The flagellum in archaea is called thearchaellum to note its difference from the bacterial flagellum.[7][8]
Eukaryotic flagella andcilia are identical in structure but have different lengths and functions.[9]Prokaryoticfimbriae andpili are smaller, and thinner appendages, with different functions. Cilia are attached to the surface of flagella and are used to swim or move fluid from one region to another.[10]
Prokaryotic (bacterial and archaeal) flagella run in a rotary movement, while eukaryotic flagella run in a bending movement. The prokaryotic flagellum uses arotary motor, and the eukaryotic flagellum uses a complex sliding filament system. Eukaryotic flagella are ATP-driven, while prokaryotic flagella can be ATP-driven (Archaea) or proton-driven (Bacteria).[11]
The three types of flagella are bacterial, archaeal, and eukaryotic.
The flagella in eukaryotes havedynein andmicrotubules that move with a bending mechanism. Bacteria and archaea do not have dynein or microtubules in their flagella, and they move using a rotary mechanism.[12]
Archaeal flagella (archaella) are superficially similar to bacterial flagella in that it also has a rotary motor, but are different in many details and considered non-homologous.[18][19][20]
Eukaryotic flagella—those of animal, plant, and protist cells—are complex cellular projections that lash back and forth. Eukaryotic flagella andmotile cilia are identical in structure, but have different lengths, waveforms, and functions.Primary cilia are immotile, and have astructurally different9+0 axoneme rather than the9+2 axoneme found in both flagella and motile cilia.
The bacterial flagellum is made up ofprotein subunits offlagellin.[12] Its shape is a 20-nanometer-thick hollow tube. It ishelical and has a sharp bend just outside the outer membrane; this "hook" allows the axis of the helix to point directly away from the cell. A shaft runs between the hook and thebasal body, passing through protein rings in the cell's membrane that act as bearings.Gram-positive organisms have two of these basal body rings, one in thepeptidoglycan layer and one in theplasma membrane.Gram-negative organisms have four such rings: theL ring associates with thelipopolysaccharides, theP ring associates withpeptidoglycan layer, the M ring is embedded in theplasma membrane, and the S ring is directly attached to thecytoplasm. The filament ends with a capping protein.[21][22]
The flagellar filament is the long, helical screw that propels the bacterium when rotated by the motor, through the hook. In most bacteria that have been studied, including the gram-negativeEscherichia coli,Salmonella typhimurium,Caulobacter crescentus, andVibrio alginolyticus, the filament is made up of 11 protofilaments approximately parallel to the filament axis. Each protofilament is a series of tandem protein chains. However,Campylobacter jejuni has seven protofilaments.[23]
The basal body has several traits in common with some types ofsecretory pores, such as the hollow, rod-like "plug" in their centers extending out through the plasma membrane. The similarities between bacterial flagella and bacterial secretory system structures and proteins provide scientific evidence supporting the theory that bacterial flagella evolved from thetype-three secretion system (TTSS).
The atomic structure of both bacterial flagella as well as the TTSSinjectisome have been elucidated in great detail, especially with the development ofcryo-electron microscopy. The best understood parts are the parts between the inner and outermembrane, that is, the scaffolding rings of the inner membrane (IM), the scaffolding pairs of the outer membrane (OM), and the rod/needle (injectisome) or rod/hook (flagellum) sections.[24]
Bacterial flagellar motor assembly: Shown here is the C-ring at the base with FliG in red, FliM in yellow, and FliN in shades of purple; the MS-ring in blue; the MotAB in brown; the LP-ring in pink; and the rod in gray.[25]
The bacterial flagellum is driven by a rotary engine (Mot complex) made up of protein, located at the flagellum's anchor point on the inner cell membrane. The engine is powered byproton-motive force, i.e., by the flow of protons (hydrogen ions) across the bacterial cell membrane due to aconcentration gradient set up by the cell's metabolism (Vibrio species have two kinds of flagella, lateral and polar, and some are driven by a sodiumion pump rather than aproton pump[26]). The rotor transports protons across the membrane, and is turned in the process. The rotor alone can operate at 6,000 to 100,000rpm,[27] but with the flagellar filament attached usually only reaches 200 to 1000 rpm. The direction of rotation can be changed by theflagellar motor switch almost instantaneously, caused by a slight change in the position of a protein,FliG, in the rotor.[28] The torque is transferred from the MotAB to the torque helix on FliG's D5 domain and with the increase in the requirement of the torque or speed more MotAB are employed.[25] Because the flagellar motor has no on-off switch, the protein epsE is used as a mechanical clutch to disengage the motor from the rotor, thus stopping the flagellum and allowing the bacterium to remain in one place.[29]
The production and rotation of a flagellum can take up to 10% of anEscherichia coli cell's energy budget and has been described as an "energy-guzzling machine".[30] Its operation generatesreactive oxygen species that elevate mutation rates.[30]
The cylindrical shape of flagella is suited to locomotion of microscopic organisms; these organisms operate at a lowReynolds number, where the viscosity of the surrounding water is much more important than its mass or inertia.[31]
The rotational speed of flagella varies in response to the intensity of the proton-motive force, thereby permitting certain forms of speed control, and also permitting some types of bacteria to attain remarkable speeds in proportion to their size; some achieve roughly 60 cell lengths per second. At such a speed, a bacterium would take about 245 days to cover 1 km; although that may seem slow, the perspective changes when the concept of scale is introduced. In comparison to macroscopic life forms, it is very fast indeed when expressed in terms of number of body lengths per second. A cheetah, for example, only achieves about 25 body lengths per second.[32]
Through use of their flagella, bacteria are able to move rapidly towards attractants and away from repellents, by means of abiased random walk, withruns and tumbles brought about by rotating its flagellumcounterclockwise andclockwise, respectively. The two directions of rotation are not identical (with respect to flagellum movement) and are selected by a molecular switch.[33] Clockwise rotation is called thetraction mode with the body following the flagella. Counterclockwise rotation is called thethruster mode with the flagella lagging behind the body.[34]
During flagellar assembly, components of the flagellum pass through the hollow cores of the basal body and the nascent filament. During assembly, protein components are added at the flagellar tip rather than at the base.[35]In vitro, flagellar filaments assemble spontaneously in a solution containing purified flagellin as the sole protein.[36]
At least 10 protein components of the bacterial flagellum share homologous proteins with thetype three secretion system (T3SS) found in many gram-negative bacteria,[37] hence one likely evolved from the other. Because the T3SS has a similar number of components as a flagellar apparatus (about 25 proteins), which one evolved first is difficult to determine. However, the flagellar system appears to involve more proteins overall, including various regulators and chaperones, hence it has been argued that flagella evolved from a T3SS. However, it has also been suggested[38] that the flagellum may have evolved first or the two structures evolved in parallel. Early single-cell organisms' need formotility (mobility) support that the more mobile flagella would be selected by evolution first,[38] but the T3SS evolving from the flagellum can be seen as 'reductive evolution', and receives no topological support from thephylogenetic trees.[39] The hypothesis that the two structures evolved separately from a common ancestor accounts for the protein similarities between the two structures, as well as their functional diversity.[40]
Some authors have argued that flagella cannot have evolved, assuming that they can only function properly when all proteins are in place. In other words, the flagellar apparatus is "irreducibly complex".[41] However, many proteins can be deleted or mutated and the flagellum still works, though sometimes at reduced efficiency.[42] Moreover, with many proteins unique to some number across species, diversity of bacterial flagella composition was higher than expected.[43] Hence, the flagellar apparatus is clearly very flexible in evolutionary terms and perfectly able to lose or gain protein components. For instance, a number of mutations have been found thatincrease the motility ofE. coli.[44] Additional evidence for the evolution of bacterial flagella includes the existence of vestigial flagella, intermediate forms of flagella and patterns of similarities among flagellar protein sequences, including the observation that almost all of the core flagellar proteins have known homologies with non-flagellar proteins.[37] Furthermore, several processes have been identified as playing important roles in flagellar evolution, including self-assembly of simple repeating subunits, gene duplication with subsequent divergence, recruitment of elements from other systems ('molecular bricolage') and recombination.[45]
Different species of bacteria have different numbers and arrangements of flagella,[46][47] named using the termtricho, from the Greektrichos meaninghair.[48]
Monotrichous bacteria such asVibrio cholerae have a singlepolar flagellum.[49]
Amphitrichous bacteria have a single flagellum on each of two opposite ends (e.g.,Campylobacter jejuni orAlcaligenes faecalis)—both flagella rotate but coordinate to produce coherent thrust.
Lophotrichous bacteria (lopho Greek combining term meaningcrest ortuft)[50] have multiple flagella located at the same spot on the bacterial surface such asHelicobacter pylori, which act in concert to drive the bacteria in a single direction. In many cases, the bases of multiple flagella are surrounded by a specialized region of the cell membrane, called thepolar organelle.[citation needed]
Peritrichous bacteria have flagella projecting in all directions (e.g.,E. coli).
Counterclockwise rotation of a monotrichous polar flagellum pushes the cell forward with the flagellum trailing behind, much like a corkscrew moving inside cork. Water on the microscopic scale is highlyviscous, unlike usualwater.
Spirochetes, in contrast, have flagella calledendoflagella arising from opposite poles of the cell, and are located within theperiplasmic space as shown by breaking the outer-membrane and also byelectron cryotomography microscopy.[51] The rotation of the filaments relative to the cell body causes the entire bacterium to move forward in a corkscrew-like motion, even through material viscous enough to prevent the passage of normally flagellated bacteria.
In certain large forms ofSelenomonas, more than 30 individual flagella are organized outside the cell body, helically twining about each other to form a thick structure (easily visible with the light microscope) called a "fascicle".
In someVibrio spp. (particularlyVibrio parahaemolyticus[52]) and relatedbacteria such asAeromonas, two flagellar systems co-exist, using different sets of genes and different ion gradients for energy. The polar flagella are constitutively expressed and provide motility in bulk fluid, while the lateral flagella are expressed when the polar flagella meet too much resistance to turn.[53][54][55][56][57][58] These provide swarming motility on surfaces or in viscous fluids.
Bundling is an event that can happen in multi-flagellated cells, bundling the flagella together and causing them to rotate in a coordinated manner.
Flagella are left-handed helices, and when rotated counter-clockwise by their rotors, they can bundle and rotate together. When the rotors reverse direction, thus rotating clockwise, the flagellum unwinds from the bundle. This may cause the cell to stop its forward motion and instead start twitching in place, referred to astumbling. Tumbling results in a stochastic reorientation of the cell, causing it to change the direction of its forward swimming.
It is not known which stimuli drive the switch between bundling and tumbling, but the motor is highly adaptive to different signals. In the model describingchemotaxis ("movement on purpose") the clockwise rotation of a flagellum is suppressed by chemical compounds favorable to the cell (e.g. food). When moving in a favorable direction, the concentration of such chemical attractants increases and therefore tumbles are continually suppressed, allowing forward motion; likewise, when the cell's direction of motion is unfavorable (e.g., away from a chemical attractant), tumbles are no longer suppressed and occur much more often, with the chance that the cell will be thus reoriented in the correct direction.
Even if all flagella would rotate clockwise, however, they often cannot form a bundle due to geometrical and hydrodynamic reasons.[59][60]
Eukaryotic flagella. 1–axoneme, 2–cell membrane, 3–IFT (IntraFlagellar Transport), 4–Basal body, 5–Cross section of flagella, 6–Triplets of microtubules of basal bodyCross section of anaxonemeLongitudinal section through the flagella area inChlamydomonas reinhardtii. In the cell apex is the basal body that is the anchoring site for a flagellum. Basal bodies originate from and have a substructure similar to that of centrioles, with nine peripheral microtubule triplets (see structure at bottom center of image).The "9+2" structure is visible in this cross-section micrograph of an axoneme.
Aiming to emphasize the distinction between the bacterial flagella and the eukaryotic cilia and flagella, some authors attempted to replace the name of these two eukaryotic structures with "undulipodia" (e.g., all papers byMargulis since the 1970s)[61] or "cilia" for both (e.g., Hülsmann, 1992;[62] Adl et al., 2012;[63] most papers ofCavalier-Smith), preserving "flagella" for the bacterial structure. However, the discriminative usage of the terms "cilia" and "flagella" for eukaryotes adopted in this article (see§ Flagella versus cilia below) is still common (e.g., Andersen et al., 1991;[64] Leadbeater et al., 2000).[65]
The core of a eukaryotic flagellum, known as theaxoneme is a bundle of nine fused pairs ofmicrotubules known asdoublets surrounding two central single microtubules (singlets). This9+2 axoneme is characteristic of the eukaryotic flagellum. At the base of a eukaryotic flagellum is abasal body, "blepharoplast" or kinetosome, which is themicrotubule organizing center for flagellar microtubules and is about 500 nanometers long. Basal bodies are structurally identical tocentrioles. The flagellum is encased within the cell'splasma membrane, so that the interior of the flagellum is accessible to the cell'scytoplasm.
Besides the axoneme and basal body, relatively constant in morphology, other internal structures of the flagellar apparatus are the transition zone (where the axoneme and basal body meet) and the root system (microtubular or fibrilar structures that extend from the basal bodies into the cytoplasm), more variable and useful as indicators of phylogenetic relationships of eukaryotes. Other structures, more uncommon, are the paraflagellar (or paraxial, paraxonemal) rod, the R fiber, and the S fiber.[66]: 63–84 For surface structures, see below.
Each of the outer 9 doublet microtubules extends a pair ofdynein arms (an "inner" and an "outer" arm) to the adjacent microtubule; these produce force through ATP hydrolysis. The flagellar axoneme also containsradial spokes, polypeptide complexes extending from each of the outer nine microtubule doublets towards the central pair, with the "head" of the spoke facing inwards. The radial spoke is thought to be involved in the regulation of flagellar motion, although its exact function and method of action are not yet understood.[67]
Beating pattern of eukaryotic "flagellum" and "cillum", a traditional distinction before the structures of the two are known.
The regular beat patterns of eukaryoticcilia and flagella generate motion on a cellular level. Examples range from the propulsion of single cells such as the swimming ofspermatozoa to the transport of fluid along a stationary layer of cells such as in therespiratory tract.[68]
Although eukaryoticcilia and flagella are ultimately the same, they are sometimes classed by their pattern of movement, a tradition from before their structures have been known. In the case of flagella, the motion is often planar and wave-like, whereas the motile cilia often perform a more complicated three-dimensional motion with a power and recovery stroke.[68] Yet another traditional form of distinction is by the number of 9+2 organelles on the cell.[67]
Intraflagellar transport, the process by which axonemal subunits,transmembrane receptors, and other proteins are moved up and down the length of the flagellum, is essential for proper functioning of the flagellum, in both motility and signal transduction.[69]
Eukaryotic flagella or cilia, probably an ancestral characteristic,[70] are widespread in almost all groups of eukaryotes, as a relatively perennial condition, or as a flagellated life cycle stage (e.g.,zoids,gametes,zoospores, which may be produced continually or not).[71][72][63]
A number of terms related to flagella or cilia are used to characterize eukaryotes.[72][75][66]: 60–63 [76][77] According to surface structures present, flagella may be:
whiplash flagella (= smooth, acronematic flagella): without hairs, e.g., inOpisthokonta
According to the place of insertion of the flagella:[81]
opisthokont: cells with flagella inserted posteriorly, e.g., inOpisthokonta (Vischer, 1945). InHaptophyceae, flagella are laterally to terminally inserted, but are directed posteriorly during rapid swimming.[82]
akrokont: cells with flagella inserted apically
subakrokont: cells with flagella inserted subapically
pleurokont: cells with flagella inserted laterally
According to the beating pattern:
gliding: a flagellum that trails on the substrate[79]
heterodynamic: flagella with different beating patterns (usually with one flagellum functioning in food capture and the other functioning in gliding, anchorage, propulsion or "steering")[83]
isodynamic: flagella beating with the same patterns
Other terms related to the flagellar type:
isokont: cells with flagella of equal length. It was also formerly used to refer to theChlorophyta
heterokont: term introduced by Luther (1899) to refer to theXanthophyceae, due to the pair of flagella of unequal length. It has taken on a specific meaning in referring to cells with an anterior straminipilous flagellum (with tripartite mastigonemes, in one or two rows) and a posterior usually smooth flagellum. It is also used to refer to the taxonHeterokonta
stephanokont: cells with a crown of flagella near its anterior end, e.g., the gametes and spores ofOedogoniales, the spores of someBryopsidales. Term introduced by Blackman & Tansley (1902) to refer to theOedogoniales
akont: cells without flagella. It was also used to refer to taxonomic groups, as Aconta or Akonta: theZygnematophyceae andBacillariophyceae (Oltmanns, 1904), or theRhodophyceae (Christensen, 1962)
Thearchaellum possessed by some species ofArchaea is superficially similar to the bacterial flagellum; in the 1980s, they were thought to be homologous on the basis of gross morphology and behavior.[84] Both flagella and archaella consist of filaments extending outside the cell, and rotate to propel the cell. Archaeal flagella have a unique structure which lacks a central channel. Similar to bacterialtype IV pilins, the archaeal proteins (archaellins) are made with class 3 signal peptides and they are processed by a type IV prepilin peptidase-like enzyme. The archaellins are typically modified by the addition of N-linkedglycans which are necessary for proper assembly or function.[3]
Discoveries in the 1990s revealed numerous detailed differences between the archaeal and bacterial flagella. These include:
While bacterial cells often have many flagellar filaments, each of which rotates independently, the archaeal flagellum is composed of a bundle of many filaments that rotates as a single assembly.
Bacterial flagella grow by the addition of flagellin subunits at the tip; archaeal flagella grow by the addition of subunits to the base.
Bacterial flagella are thicker than archaella, and the bacterial filament has a large enough hollow "tube" inside that the flagellin subunits can flow up the inside of the filament and get added at the tip; the archaellum is too thin (12-15 nm) to allow this.[86]
Many components of bacterial flagella share sequence similarity to components of thetype III secretion systems, but the components of bacterial flagella and archaella share no sequence similarity. Instead, some components of archaella share sequence and morphological similarity with components oftype IV pili, which are assembled through the action oftype II secretion systems (the nomenclature of pili and protein secretion systems is not consistent).[86]
These differences support the theory that the bacterial flagella and archaella are a classic case of biologicalanalogy, orconvergent evolution, rather thanhomology.[87][88][89] Research into the structure of archaella made significant progress beginning in the early 2010s, with the first atomic resolution structure of an archaella protein, the discovery of additional functions of archaella, and the first reports of archaella in Nanoarchaeota and Thaumarchaeota.[90][91]
The onlyfungi to have a single flagellum on theirspores are thechytrids. InBatrachochytrium dendrobatidis the flagellum is 19–20 μm long.[92] A nonfunctioningcentriole lies adjacent to thekinetosome. Nine interconnected props attach the kinetosome to theplasmalemma, and a terminal plate is present in the transitional zone. An inner ring-like structure attached to the tubules of the flagellar doublets within the transitional zone has been observed in transverse section.[92]
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