Twitching motility

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Twitching motility is a form of crawling bacterial motility used to move over surfaces. Twitching is mediated by the activity of hair-like filaments called type IV pili which extend from the cell's exterior, bind to surrounding solid substrates, and retract, pulling the cell forwards in a manner similar to the action of a grappling hook. [1] [2] [3] The name twitching motility is derived from the characteristic jerky and irregular motions of individual cells when viewed under the microscope. [4] It has been observed in many bacterial species, but is most well studied in Pseudomonas aeruginosa , Neisseria gonorrhoeae and Myxococcus xanthus . Active movement mediated by the twitching system has been shown to be an important component of the pathogenic mechanisms of several species. [2]

Contents

Mechanisms

Pilus structure

Twitching motility. Type IV pili are extended from the surface of twitching-capable cells and attach to a nearby surface. Pilus retraction results in the forwards movement of the cell. Arrows indicate direction of pilus retraction/extension. Inset: Structure of the type IV pilus machinery. The four composing subcomplexes (the motor subcomplex (red), alignment subcomplex (blue and violet), secretion subcomplex (yellow) and pilus (green)) are highlighted. Twitching Motility Summary.svg
Twitching motility. Type IV pili are extended from the surface of twitching-capable cells and attach to a nearby surface. Pilus retraction results in the forwards movement of the cell. Arrows indicate direction of pilus retraction/extension. Inset: Structure of the type IV pilus machinery. The four composing subcomplexes (the motor subcomplex (red), alignment subcomplex (blue and violet), secretion subcomplex (yellow) and pilus (green)) are highlighted.

The type IV pilus complex consists of both the pilus itself and the machinery required for its construction and motor activity. The pilus filament is largely composed of the PilA protein, with more uncommon minor pilins at the tip. These are thought to play a role in initiation of pilus construction. [5] Under normal conditions, the pilin subunits are arranged as a helix with five subunits in each turn, [5] [6] but pili under tension are able to stretch and rearrange their subunits into a second configuration with around 1+2⁄3 subunits per turn. [7]

Three subcomplexes form the apparatus responsible for assembling and retracting the type IV pili. [8] The core of this machinery is the motor subcomplex, consisting of the PilC protein and the cytosolic ATPases PilB and PilT. These ATPases drive pilus extension or retraction respectively, depending on which of the two is currently bound to the pilus complex. Surrounding the motor complex is the alignment subcomplex, formed from the PilM, PilN, PilO and PilP proteins. These proteins form a bridge between the inner and outer membranes and create a link between the inner membrane motor subcomplex and the outer membrane secretion subcomplex. This consists of a pore formed from the PilQ protein, through which the assembled pilus can exit the cell. [9]

Regulation

Regulatory proteins associated with the twitching motility system have strong sequence and structural similarity to those that regulate bacterial chemotaxis using flagellae. [2] [10] In P. aeruginosa for example, a total of four homologous chemosensory pathways are present, three regulating swimming motility and one regulating twitching motility. [11] These chemotactic systems allow cells to regulate twitching so as to move towards chemoattractants such as phospholipids and fatty acids. [12] In contrast to the run-and-tumble model of chemotaxis associated with flagellated cells however, movement towards chemoattractants in twitching cells appears to be mediated via regulation of the timing of directional reversals. [13]

Motility patterns

The tug-of-war model of twitching motility. Cells (such as the shown N. gonorrhoeae diplococcus) extend pili (green) that attach themselves to locations in the surrounding environment (blue circles). Pili experience tension due to activation of the retraction machinery. Upon detachment or rupture of a pilus (red), the cell quickly jerks into a new position based on the resulting balance of forces acting through the remaining pili. Twitching tug-of-war.svg
The tug-of-war model of twitching motility. Cells (such as the shown N. gonorrhoeae diplococcus) extend pili (green) that attach themselves to locations in the surrounding environment (blue circles). Pili experience tension due to activation of the retraction machinery. Upon detachment or rupture of a pilus (red), the cell quickly jerks into a new position based on the resulting balance of forces acting through the remaining pili.

Twitching motility is capable of driving the movement of individual cells. [1] [13] The pattern of motility that results is highly dependent upon cell shape and the distribution of pili over the cell surface. [14] In N. gonorrhoeae for example, the roughly spherical cell shape and uniform distribution of pili results in cells adopting a 2D random walk over the surface they are attached to. [15] In contrast, species such as P. aeruginosa and M. xanthus exist as elongated rods with pili localised at their poles, and show much greater directional persistence during crawling due to the resulting bias in force generation direction. [16] P. aeruginosa and M. xanthus are also able to reverse direction during crawling by switching the pole of pilus localization. [13] [14] Type IV pili also mediate a form of walking motility in P. aeruginosa, where pili are used to pull the cell rod into a vertical orientation and move it at much higher speeds than during horizontal crawling motility. [16] [17]

The existence of many pili pulling simultaneously on the cell body results in a balance of forces determining the movement of the cell body. This is known as the tug-of-war model of twitching motility. [14] [15] Sudden changes in the balance of forces caused by detachment or release of individual pili results in a fast jerk (or 'slingshot') that combines fast rotational and lateral movements, in contrast to the slower lateral movements seen during the longer periods between slingshots. [18]

Roles

Pathogenesis

Both presence of type IV pili and active pilar movement appear to be important contributors to the pathogenicity of several species. [8] In P. aeruginosa, loss of pilus retraction results in a reduction of bacterial virulence in pneumonia [19] and reduces colonisation of the cornea. [20] Some bacteria are also able to twitch along vessel walls against the direction of fluid flow within them, [21] which is thought to permit colonisation of otherwise inaccessible sites in the vasculatures of plants and animals.

Bacterial cells can also be targeted by twitching: during the cell invasion phase of the lifecycle of Bdellovibrio , type IV pili are used by cells to pull themselves through gaps formed in the cell wall of prey bacteria. [22] Once inside, the Bdellovibrio are able to use the host cell's resources to grow and reproduce, eventually lysing the cell wall of the prey bacterium and escaping to invade other cells.

Biofilms

Twitching motility is also important during the formation of biofilms. [8] During biofilm establishment and growth, motile bacteria are able to interact with secreted extracellular polymeric substances (EPSs) such as Psl, alginate and extracellular DNA. [23] As they encounter sites of high EPS deposition, P. aeruginosa cells slow down, accumulate and deposit further EPS components. This positive feedback is an important initiating factor for the establishment of microcolonies, the precursors to fully fledged biofilms. [24] In addition, once biofilms have become established, their twitching-mediated spread is facilitated and organised by components of the EPS. [25]

Twitching can also influence the structure of biofilms. During their establishment, twitching-capable cells are able to crawl on top of cells lacking twitching motility and dominate the fast-growing external surface of the biofilm. [23] [26]

Taxonomic distribution and evolution

Type IV pili and related structures can be found across almost all phyla of Bacteria and Archaea, [27] however definitive twitching motility has been shown in a more limited range of prokaryotes. Most well studied and wide spread are the twitching Pseudomonadota, such as Neisseria gonorrhoeae , Myxococcus xanthus and Pseudomonas aeruginosa . [14] [8] Nevertheless, twitching has been observed in other phyla as well. For example, twitching motility has been observed in the cyanobacterium Synechocystis , [28] as well as the gram-positive Bacillota Streptococcus sanguinis . [29]

Other structures and systems closely related to type IV pili have also been observed in prokaryotes. In Archea, for example, bundles of type IV-like filaments have been observed to form helical structures similar in both form and function to the bacterial flagellum. These swimming associated structures have been termed archaella. [30] Also closely related to the type IV pilus is the type II secretion system, [31] itself widely distributed amongst gram-negative bacteria. In this secretion system, cargo destined for export is associated with tips of type IV-like pseudopili in the periplasm. Extension of the pseudopili through secretin proteins similar to PilQ permits these cargo proteins to cross the outer membrane and enter the extracellular environment.

Because of this wide but patchy distribution of type IV pilus-like machinery, it has been suggested that the genetic material encoding it has been transferred between species via horizontal gene transfer following its initial development in a single species of Pseudomonadota. [6]

See also

Related Research Articles

<span class="mw-page-title-main">Pilus</span> A proteinaceous hair-like appendage on the surface of bacteria

A pilus is a hair-like appendage found on the surface of many bacteria and archaea. The terms pilus and fimbria can be used interchangeably, although some researchers reserve the term pilus for the appendage required for bacterial conjugation. All conjugative pili are primarily composed of pilin – fibrous proteins, which are oligomeric.

<span class="mw-page-title-main">Biofilm</span> Aggregation of bacteria or cells on a surface

A biofilm comprises any syntrophic consortium of microorganisms in which cells stick to each other and often also to a surface. These adherent cells become embedded within a slimy extracellular matrix that is composed of extracellular polymeric substances (EPSs). The cells within the biofilm produce the EPS components, which are typically a polymeric conglomeration of extracellular polysaccharides, proteins, lipids and DNA. Because they have three-dimensional structure and represent a community lifestyle for microorganisms, they have been metaphorically described as "cities for microbes".

<i>Neisseria gonorrhoeae</i> Species of bacterium

Neisseria gonorrhoeae, also known as gonococcus (singular), or gonococci (plural), is a species of Gram-negative diplococci bacteria isolated by Albert Neisser in 1879. It causes the sexually transmitted genitourinary infection gonorrhea as well as other forms of gonococcal disease including disseminated gonococcemia, septic arthritis, and gonococcal ophthalmia neonatorum.

<span class="mw-page-title-main">Secretion</span> Controlled release of substances by cells or tissues

Secretion is the movement of material from one point to another, such as a secreted chemical substance from a cell or gland. In contrast, excretion is the removal of certain substances or waste products from a cell or organism. The classical mechanism of cell secretion is via secretory portals at the plasma membrane called porosomes. Porosomes are permanent cup-shaped lipoprotein structures embedded in the cell membrane, where secretory vesicles transiently dock and fuse to release intra-vesicular contents from the cell.

<i>Pseudomonas aeruginosa</i> Species of bacterium

Pseudomonas aeruginosa is a common encapsulated, Gram-negative, aerobic–facultatively anaerobic, rod-shaped bacterium that can cause disease in plants and animals, including humans. A species of considerable medical importance, P. aeruginosa is a multidrug resistant pathogen recognized for its ubiquity, its intrinsically advanced antibiotic resistance mechanisms, and its association with serious illnesses – hospital-acquired infections such as ventilator-associated pneumonia and various sepsis syndromes.

Pilin refers to a class of fibrous proteins that are found in pilus structures in bacteria. These structures can be used for the exchange of genetic material, or as a cell adhesion mechanism. Although not all bacteria have pili or fimbriae, bacterial pathogens often use their fimbriae to attach to host cells. In Gram-negative bacteria, where pili are more common, individual pilin molecules are linked by noncovalent protein-protein interactions, while Gram-positive bacteria often have polymerized LPXTG pilin.

<span class="mw-page-title-main">Bacteria</span> Domain of microorganisms

Bacteria are ubiquitous, mostly free-living organisms often consisting of one biological cell. They constitute a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria were among the first life forms to appear on Earth, and are present in most of its habitats. Bacteria inhabit soil, water, acidic hot springs, radioactive waste, and the deep biosphere of Earth's crust. Bacteria play a vital role in many stages of the nutrient cycle by recycling nutrients and the fixation of nitrogen from the atmosphere. The nutrient cycle includes the decomposition of dead bodies; bacteria are responsible for the putrefaction stage in this process. In the biological communities surrounding hydrothermal vents and cold seeps, extremophile bacteria provide the nutrients needed to sustain life by converting dissolved compounds, such as hydrogen sulphide and methane, to energy. Bacteria also live in symbiotic and parasitic relationships with plants and animals. Most bacteria have not been characterised and there are many species that cannot be grown in the laboratory. The study of bacteria is known as bacteriology, a branch of microbiology.

<span class="mw-page-title-main">Swarming motility</span>

Swarming motility is a rapid and coordinated translocation of a bacterial population across solid or semi-solid surfaces, and is an example of bacterial multicellularity and swarm behaviour. Swarming motility was first reported by Jorgen Henrichsen and has been mostly studied in genus Serratia, Salmonella, Aeromonas, Bacillus, Yersinia, Pseudomonas, Proteus, Vibrio and Escherichia.

<span class="mw-page-title-main">Extracellular polymeric substance</span> Gluey polymers secreted by microorganisms to form biofilms

Extracellular polymeric substances (EPSs) are natural polymers of high molecular weight secreted by microorganisms into their environment. EPSs establish the functional and structural integrity of biofilms, and are considered the fundamental component that determines the physicochemical properties of a biofilm. EPS in the matrix of biofilms provides compositional support and protection of microbial communities from the harsh environments. Components of EPS can be of different classes of polysaccharides, lipids, nucleic acids, proteins, lipopolysaccharides, and minerals.

<span class="mw-page-title-main">Bacterial motility</span> Ability of bacteria to move independently using metabolic energy

Bacterial motility is the ability of bacteria to move independently using metabolic energy. Most motility mechanisms which evolved among bacteria also evolved in parallel among the archaea. Most rod-shaped bacteria can move using their own power, which allows colonization of new environments and discovery of new resources for survival. Bacterial movement depends not only on the characteristics of the medium, but also on the use of different appendages to propel. Swarming and swimming movements are both powered by rotating flagella. Whereas swarming is a multicellular 2D movement over a surface and requires the presence of surfactants, swimming is movement of individual cells in liquid environments.

<span class="mw-page-title-main">Cyclic di-GMP</span> Chemical compound

Cyclic di-GMP is a second messenger used in signal transduction in a wide variety of bacteria. Cyclic di-GMP is not known to be used by archaea, and has only been observed in eukaryotes in Dictyostelium. The biological role of cyclic di-GMP was first uncovered when it was identified as an allosteric activator of a cellulose synthase found in Gluconacetobacter xylinus in order to produce microbial cellulose.

<span class="mw-page-title-main">Gliding motility</span>

Gliding motility is a type of translocation used by microorganisms that is independent of propulsive structures such as flagella, pili, and fimbriae. Gliding allows microorganisms to travel along the surface of low aqueous films. The mechanisms of this motility are only partially known.

<span class="mw-page-title-main">Sortase</span> Group of prokaryotic enzymes

Sortase refers to a group of prokaryotic enzymes that modify surface proteins by recognizing and cleaving a carboxyl-terminal sorting signal. For most substrates of sortase enzymes, the recognition signal consists of the motif LPXTG (Leu-Pro-any-Thr-Gly), then a highly hydrophobic transmembrane sequence, followed by a cluster of basic residues such as arginine. Cleavage occurs between the Thr and Gly, with transient attachment through the Thr residue to the active site Cys residue, followed by transpeptidation that attaches the protein covalently to cell wall components. Sortases occur in almost all Gram-positive bacteria and the occasional Gram-negative bacterium or Archaea, where cell wall LPXTG-mediated decoration has not been reported. Although sortase A, the "housekeeping" sortase, typically acts on many protein targets, other forms of sortase recognize variant forms of the cleavage motif, or catalyze the assembly of pilins into pili.

Roberto Kolter is Professor of Microbiology, Emeritus at Harvard Medical School, an author, and past president of the American Society for Microbiology. Kolter has been a professor at Harvard Medical School since 1983 and was Co-director of Harvard's Microbial Sciences Initiative from 2003-2018. During the 35-year term of the Kolter laboratory from 1983 to 2018, more than 130 graduate student and postdoctoral trainees explored an eclectic mix of topics gravitating around the study of microbes. Kolter is a fellow of the American Association for the Advancement of Science and of the American Academy of Microbiology.

<span class="mw-page-title-main">PilZ domain</span>

The PilZ protein family is named after the type IV pilus control protein first identified in Pseudomonas aeruginosa, expressed as part of the pil operon. It has a cytoplasmic location and is essential for type IV fimbrial, or pilus, biogenesis. PilZ is a c-di-GMP binding domain and PilZ domain-containing proteins represent the best studied class of c-di-GMP effectors. C-di-GMP, cyclic diguanosine monophosphate, the second messenger in cells, is widespread in and unique to the bacterial kingdom. Elevated intracellular levels of c-di-GMP generally cause bacteria to change from a motile single-cell state to a sessile, adhesive surface-attached multicellular state called biofilm.

<span class="mw-page-title-main">Rhamnolipid</span> Chemical compound

Rhamnolipids are a class of glycolipid produced by Pseudomonas aeruginosa, amongst other organisms, frequently cited as bacterial surfactants. They have a glycosyl head group, in this case a rhamnose moiety, and a 3-(hydroxyalkanoyloxy)alkanoic acid (HAA) fatty acid tail, such as 3-hydroxydecanoic acid.

Bacterial morphological plasticity refers to changes in the shape and size that bacterial cells undergo when they encounter stressful environments. Although bacteria have evolved complex molecular strategies to maintain their shape, many are able to alter their shape as a survival strategy in response to protist predators, antibiotics, the immune response, and other threats.

<span class="mw-page-title-main">Bacterial secretion system</span> Protein complexes present on the cell membranes of bacteria for secretion of substances

Bacterial secretion systems are protein complexes present on the cell membranes of bacteria for secretion of substances. Specifically, they are the cellular devices used by pathogenic bacteria to secrete their virulence factors to invade the host cells. They can be classified into different types based on their specific structure, composition and activity. Generally, proteins can be secreted through two different processes. One process is a one-step mechanism in which proteins from the cytoplasm of bacteria are transported and delivered directly through the cell membrane into the host cell. Another involves a two-step activity in which the proteins are first transported out of the inner cell membrane, then deposited in the periplasm, and finally through the outer cell membrane into the host cell.

<span class="mw-page-title-main">Social motility</span>

Social motility describes the motile movement of groups of cells that communicate with each other to coordinate movement based on external stimuli. There are multiple varieties of each kingdom that express social motility that provides a unique evolutionary advantages that other species do not possess. This has made them lethal killers such as African trypanosomiasis, or Myxobacteria. These evolutionary advantages have proven to increase survival rate among socially motile bacteria whether it be the ability to evade predators or communication within a swarm to form spores for long term hibernation in times of low nutrients or toxic environments.

<span class="mw-page-title-main">Cyanobacterial morphology</span> Form and structure of a phylum

Cyanobacterial morphology refers to the form or shape of cyanobacteria. Cyanobacteria are a large and diverse phylum of bacteria defined by their unique combination of pigments and their ability to perform oxygenic photosynthesis.

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  30. ↑ Ng, Sandy Y. M.; Chaban, Bonnie; Jarrell, Ken F. (2006). "Archaeal flagella, bacterial flagella and type IV pili: a comparison of genes and posttranslational modifications". Journal of Molecular Microbiology and Biotechnology. 11 (3–5): 167–191. doi:10.1159/000094053. ISSN   1464-1801. PMID   16983194. S2CID   30386932.
  31. ↑ Peabody, Christopher R.; Chung, Yong Joon; Yen, Ming-Ren; Vidal-Ingigliardi, Dominique; Pugsley, Anthony P.; Saier, Milton H. (November 2003). "Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella". Microbiology. 149 (Pt 11): 3051–3072. doi: 10.1099/mic.0.26364-0 . ISSN   1350-0872. PMID   14600218.
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