In biology, quorum sensing is the ability to detect and to respond to cell population density by gene regulation. As one example, quorum sensing (QS) enables bacteria to restrict the expression of specific genes to the high cell densities at which the resulting phenotypes will be most beneficial. Many species of bacteria use quorum sensing to coordinate gene expression according to the density of their local population. In similar fashion, some social insects use quorum sensing to determine where to nest.
In addition to its function in biological systems, quorum sensing has several useful applications for computing and robotics. In general, quorum sensing can function as a decision-making process in any decentralized system in which the components have: (a) a means of assessing the number of other components they interact with and (b) a standard response once a threshold number of components is detected.
- 1 Bacteria
- 1.1 Mechanism
- 1.2 Examples
- 1.3 Molecules involved
- 1.4 Evolution
- 2 Archaea
- 3 Plants
- 4 Quorum quenching
- 5 Social insects
- 6 Computing and robotics
- 7 See also
- 8 References
- 9 Further reading
- 10 External links
Some of the best-known examples of quorum sensing come from studies of bacteria. Bacteria use quorum sensing to regulate certain phenotype expressions, which in turn, coordinate their behaviours. Some common phenotypes include biofilm formation, virulence factor expression, and motility. Certain bacteria are able to use quorum sensing to regulate bioluminescence, nitrogen fixation and sporulation.
Quorum sensing functions based on the local density of the bacterial population in the immediate environment. It can occur within a single bacterial species, as well as between diverse species. Both Gram-positive and gram-negative bacteria use quorum sensing, but there are some major differences in their mechanisms.
For the bacteria to use quorum sensing constitutively, they must possess three characteristics: to secrete a signaling molecule, an autoinducer, to detect the change in concentration of signaling molecules, and to regulate gene transcription as a response. This process is highly dependent on the diffusion mechanism of the signaling molecules. QS Signaling molecules are usually secreted at a low level by individual bacteria. At low cell density, the molecules may just diffuse away. At high cell density, the local concentration of signaling molecules may exceed its threshold level, and trigger changes in gene expressions.
Gram-positive bacteria use autoinducing peptide (AIP) as their autoinducers.
When gram-positive bacteria detect high concentration of AIP in the environment, AIP bind to a receptor to activate kinase. The kinase phosphorylates a transcription factor, which regulated gene transcription. This is called a two-component system.
Another possible mechanism is that AIP is transported into the cytosol, and binds directly to a transcription factor to initiate or inhibit transcription.
Gram-negative bacteria produce N-acyl homoserine lactones (AHL) as their signaling molecule. Usually AHLs do not need additional processing, and bind directly to transcription factors to regulate gene expression.
Some gram-negative bacteria may use the two-component system as well.
Quorum sensing was first observed in Aliivibrio fischeri, a bioluminescent bacterium that lives as a mutualistic symbiont in the photophore (or light-producing organ) of the Hawaiian bobtail squid. When A. fischeri cells are free-living (or planktonic), the autoinducer is at low concentration, and, thus, cells do not show luminescence. However, when the population reaches the threshold in the photophore (about 1011 cells/ml), transcription of luciferase is induced, leading to bioluminescence.
In the Gram-negative bacterium Escherichia coli (E. coli), cell division may be partially regulated by AI-2-mediated quorum sensing. This species uses AI-2, which is produced and processed by the lsr operon. Part of it encodes an ABC transporter, which imports AI-2 into the cells during the early stationary (latent) phase of growth. AI-2 is then phosphorylated by the LsrK kinase, and the newly produced phospho-AI-2 can be either internalized or used to suppress LsrR, a repressor of the lsr operon (thereby activating the operon). Transcription of the lsr operon is also thought to be inhibited by dihydroxyacetone phosphate (DHAP) through its competitive binding to LsrR. Glyceraldehyde 3-phosphate has also been shown to inhibit the lsr operon through cAMP-CAPK-mediated inhibition. This explains why, when grown with glucose, E. coli will lose the ability to internalize AI-2 (because of catabolite repression). When grown normally, AI-2 presence is transient.
E. coli and Salmonella enterica do not produce AHL signals commonly found in other Gram-negative bacteria. However, they have a receptor that detects AHLs from other bacteria and change their gene expression in accordance with the presence of other "quorate" populations of Gram-negative bacteria.
Salmonella encodes a LuxR homolog, SdiA, but does not encode an AHL synthase. SdiA detects AHLs produced by other species of bacteria including Aeromonas hydrophila, Hafnia alvei, and Yersinia enterocolitica. When AHL is detected, SdiA regulates the rck operon on the Salmonella virulence plasmid (pefI-srgD-srgA-srgB-rck-srgC) and a single gene horizontal acquisition in the chromosome srgE. Salmonella does not detect AHL when passing through the gastrointestinal tracts of several animal species, suggesting that the normal microbiota does not produce AHLs. However, SdiA does become activated when Salmonella transits through turtles colonized with Aeromonas hydrophila or mice infected with Yersinia enterocolitica. Therefore, Salmonella appears to use SdiA to detect the AHL production of other pathogens rather than the normal gut flora.
The opportunistic pathogen Pseudomonas aeruginosa uses quorum sensing to coordinate the formation of biofilm, swarming motility, exopolysaccharide production, virulence, and cell aggregation. These bacteria can grow within a host without harming it, until they reach a threshold concentration. Then they become aggressive, developing to the point at which their numbers are sufficient to overcome the host's immune system, and form a biofilm, leading to disease within the host as the biofilm is a protective layer encasing the bacteria population. Another form of gene regulation that allows the bacteria to rapidly adapt to surrounding changes is through environmental signaling. Recent studies have discovered that anaerobiosis can significantly impact the major regulatory circuit of quorum sensing. This important link between quorum sensing and anaerobiosis has a significant impact on production of virulence factors of this organism. Garlic and ginseng experimentally block quorum sensing in Pseudomonas aeruginosa. It is hoped that the therapeutic enzymatic degradation of the signaling molecules will prevent the formation of such biofilms and possibly weaken established biofilms. Disrupting the signalling process in this way is called quorum sensing inhibition.
It has recently been found that Acinetobacter sp. also show quorum sensing activity. This bacterium, an emerging pathogen, produces AHLs. Acinetobacter sp. shows both quorum sensing and quorum quenching activity. It produces AHLs and also, it can degrade the AHL molecules as well.
This bacterium was previously considered a fish pathogen, but it has recently emerged as a human pathogen. Aeromonas sp. have been isolated from various infected sites from patients (bile, blood, peritoneal fluid, pus, stool and urine). All isolates produced the two principal AHLs, N-butanoylhomoserine lactone (C4-HSL) and N-hexanoyl homoserine lactone (C6-HSL). It has been documented that Aeromonas sobria has produced C6-HSL and two additional AHLs with N-acyl side chain longer than C6.
The YenR and YenI proteins produced by the gammaproteobacterium Yersinia enterocolitica are similar to Aliivibrio fischeri LuxR and LuxI. YenR activates the expression of a small non-coding RNA, YenS. YenS inhibits YenI expression and acylhomoserine lactone production. YenR/YenI/YenS are involved in the control of swimming and swarming motility.
Three-dimensional structures of proteins involved in quorum sensing were first published in 2001, when the crystal structures of three LuxS orthologs were determined by X-ray crystallography. In 2002, the crystal structure of the receptor LuxP of Vibrio harveyi with its inducer AI-2 (which is one of the few biomolecules containing boron) bound to it was also determined. Many bacterial species, including E. coli, an enteric bacterium and model organism for Gram-negative bacteria, produce AI-2. A comparative genomic and phylogenetic analysis of 138 genomes of bacteria, archaea, and eukaryotes found that "the LuxS enzyme required for AI-2 synthesis is widespread in bacteria, while the periplasmic binding protein LuxP is present only in Vibrio strains," leading to the conclusion that either "other organisms may use components different from the AI-2 signal transduction system of Vibrio strains to sense the signal of AI-2 or they do not have such a quorum sensing system at all." Farnesol is used by the fungus Candida albicans as a quorum sensing molecule that inhibits filamentation.
Certain bacteria can produce enzymes called lactonases that can target and inactivate AHLs. Researchers have developed novel molecules which block the signalling receptors of bacteria (Quorum quenching). mBTL is a compound that has been shown to inhibit quorum sensing and decrease the amount of cell death by a significant amount. Additionally, researchers are also examining the role of natural compounds (such as caffeine) as potential quorum sensing inhibitors. Research in this area has been promising and could lead to the development of natural compounds as effective therapeutics.
The majority of quorum sensing systems that fall under the "two-gene" (an autoinducer synthase coupled with a receptor molecule) paradigm as defined by the Vibrio fischeri system occur in the Gram-negative Proteobacteria. A comparison between the Proteobacteria phylogeny as generated by 16S ribosomal RNA sequences and phylogenies of LuxI-, LuxR-, or LuxS-homologs shows a notably high level of global similarity. Overall, the quorum sensing genes seem to have diverged along with the Proteobacteria phylum as a whole. This indicates that these quorum sensing systems are quite ancient, and arose very early in the Proteobacteria lineage.
Although examples of horizontal gene transfer are apparent in LuxI, LuxR, and LuxS phylogenies, they are relatively rare. This result is in line with the observation that quorum sensing genes tend to control the expression of a wide array of genes scattered throughout the bacterial chromosome. A recent acquisition by horizontal gene transfer would be unlikely to have integrated itself to this degree. Given that the majority of autoinducer–synthase/receptor occurs in tandem in bacterial genomes, it is also rare that they switch partners and so pairs tend to co-evolve.
In quorum sensing genes of Gammaproteobacteria, which includes Pseudomonas aeruginosa and Escherichia coli, the LuxI/LuxR genes form a functional pair, with LuxI as the auto-inducer synthase and LuxR as the receptor. Gamma Proteobacteria are unique in possessing quorum sensing genes, which, although functionally similar to the LuxI/LuxR genes, have a markedly divergent sequence. This family of quorum-sensing homologs may have arisen in the gamma Proteobacteria ancestor, although the cause of their extreme sequence divergence yet maintenance of functional similarity has yet to be explained. In addition, species that employ multiple discrete quorum sensing systems are almost all members of the gamma Proteobacteria, and evidence of horizontal transfer of quorum sensing genes is most evident in this class.
As quorum sensing implies a cooperative behavior, this concept has been challenged by the evolutionary implication of cooperative cheaters. This is circumvented by the concept of diffusion sensing, which has been an alternative and complementary model to quorum sensing. However, both explanations face the problems of signalling in either complex (multiple species sharing the same space) or simple (one single cell confined to a limited volume) environments where the spatial distribution of the cells can be more important for sensing than the cell population density. A new model, efficiency sensing, which takes into account both problematics, population density and spatial confinement, has been proposed as an alternative. One of the probable reasons for controversy is that current terminologies (quorum sensing, diffusion sensing, efficiency sensing) arise from different models of how natural selection has acted to shape and maintain the process. Since each of the various models does apply under some circumstances but not others, a sensible resolution to these controversies could be to return the terminology of the process to autoinduction, as originally described by Hastings and coworkers, as this term does not imply understanding of the function of the process.
Interaction of quorum-sensing molecules with mammalian cells and its medical applications
Next to the potential antimicrobial functionality, quorum-sensing derived molecules, especially the peptides, are being investigated for their use in other therapeutic domains as well, including immunology, central nervous system disorders and oncology. Quorum-sensing peptides have been demonstrated to interact with cancer cells, as well as to permeate the blood-brain barrier permeation reaching the brain parenchyma
Methanosaeta harundinacea 6Ac
Methanosaeta harundinacea 6Ac, a methanogenic archaeon, produces carboxylated acyl homoserine lactone compounds that facilitate the transition from growth as short cells to growth as filaments.
Quorum sensing could be described when it was known that bacteria possess the ability to communicate. In the last few years, interactions between bacteria and eukaryotic hosts, such as plants, have been shown. These interactions are facilitated by quorum-sensing molecules and play a major role in maintaining the pathogenicity of bacteria towards other hosts, such as humans. This mechanism can be understood by looking at the effects of N-Acyl homoserine lactone (AHL), one of the quorum sensing-signalling molecules in gram-negative bacteria, on plants. The model organism used is Arabidopsis thaliana.
The role of AHLs having long carbon-chains (C12, C14), which have an unknown receptor mechanism, is less well understood than AHLs having short carbon-chains (C4, C6, C8), which are perceived by the G protein-coupled receptor. A phenomenon called "AHL priming", which is a dependent signalling pathway, enhanced our knowledge of long-chain AHLs. The role of quorum-sensing molecules was better explained according to three categories: host physiology–based impact of quorum sensing molecules; ecological effects; and cellular signaling. Calcium signalling and calmodulin have a large role in short-chain AHLs response in Arabidopsis. Research was also conducted on barley and crop yam bean that reveals the AHLs determining the detoxification enzymes called GST were found less in yam bean.
Quorum sensing-based regulatory systems are necessary to plant-disease-causing bacteria. Looking towards developing new strategies based on plant-associated microbiomes, the aim of further study is to improve the quantity and quality of the food supply. Further research into this inter-kingdom communication also enhances the possibility of learning about quorum sensing in humans.
Quorum quenching is the process of preventing quorum sensing by disrupting signalling. This is achieved by inactivating signalling enzymes, by introducing molecules that mimic signalling molecules and block their receptors, or by degrading signalling molecules themselves.
Closantel and triclosan are known inhibitors of quorum sensing enzymes. Closantel induces aggregation of the histamine kinase sensor in two-component signalling. The latter disrupts the synthesis of a class of signalling molecules known as N-acyl homoserine lactones (AHLs) by blocking the enoyl-acyl carrier protein (ACP) reductase.
Two groups of well-known mimicking molecules include halogenated furanones, which mimic AHL molecules, and synthetic Al peptides (AIPs), which mimic naturally occurring AIPs. These groups inhibit receptors from binding substrate or decrease the concentration of receptors in the cell. Furanones have also been found to act on AHL-dependant transcriptional activity, whereby the half life of the autoinducer-binding LuxR protein is significantly shortened.
Recently, a well-studied quorum quenching bacterial strain (KM1S) was isolated and its AHL degradation kinetic was studied using rapid resolution liquid chromatography (RRLC). RRLC efficiently separates components of a mixture to a high degree of sensitivity, based on their affinities for different liquid phases. It was found that the genome of this strain encoded an inactivation enzyme with distinct motifs targeting the degradation of AHLs.
Applications of quorum quenching that have been exploited by humans include the use of AHL-degrading bacteria in aquacultures to limit the spread of diseases in aquatic populations of fish, mollusks and crustaceans. This technique has also been translated to agriculture, to restrict the spread of pathogenic bacteria that use quorum sensing in plants. Anti-biofouling is another process that exploits quorum quenching bacteria to mediate the dissociation of unwanted biofilms aggregating on wet surfaces, such as medical devices, transportation infrastructure and water systems.
Social insect colonies are an excellent example of a decentralized system, because no individual is in charge of directing or making decisions for the colony. Several groups of social insects have been shown to use quorum sensing in a process that resembles collective decision-making.
Colonies of the ant Temnothorax albipennis nest in small crevices between rocks. When the rocks shift and the nest is broken up, these ants must quickly choose a new nest to move into. During the first phase of the decision-making process, a small portion of the workers leave the destroyed nest and search for new crevices. When one of these scout ants finds a potential nest, she assesses the quality of the crevice based on a variety of factors including the size of the interior, the number of openings (based on light level), and the presence or absence of dead ants. The worker then returns to the destroyed nest, where she waits for a short period before recruiting other workers to follow her to the nest that she has found, using a process called tandem running. The waiting period is inversely related to the quality of the site; for instance, a worker that has found a poor site will wait longer than a worker that encountered a good site. As the new recruits visit the potential nest site and make their own assessment of its quality, the number of ants visiting the crevice increases. During this stage, ants may be visiting many different potential nests. However, because of the differences in the waiting period, the number of ants in the best nest will tend to increase at the greatest rate. Eventually, the ants in this nest will sense that the rate at which they encounter other ants has exceeded a particular threshold, indicating that the quorum number has been reached. Once the ants sense a quorum, they return to the destroyed nest and begin rapidly carrying the brood, queen, and fellow workers to the new nest. Scouts that are still tandem-running to other potential sites are also recruited to the new nest, and the entire colony moves. Thus, although no single worker may have visited and compared all of the available options, quorum sensing enables the colony as a whole to quickly make good decisions about where to move.
Honey bees (Apis mellifera) also use quorum sensing to make decisions about new nest sites. Large colonies reproduce through a process called swarming, in which the queen leaves the hive with a portion of the workers to form a new nest elsewhere. After leaving the nest, the workers form a swarm that hangs from a branch or overhanging structure. This swarm persists during the decision-making phase until a new nest site is chosen.
The quorum sensing process in honey bees is similar to the method used by Temnothorax ants in several ways. A small portion of the workers leave the swarm to search out new nest sites, and each worker assesses the quality of the cavity it finds. The worker then returns to the swarm and recruits other workers to her cavity using the honey bee waggle dance. However, instead of using a time delay, the number of dance repetitions the worker performs is dependent on the quality of the site. Workers that found poor nests stop dancing sooner, and can therefore be recruited to the better sites. Once the visitors to a new site sense that a quorum number (usually 10–20 bees) has been reached, they return to the swarm and begin using a new recruitment method called piping. This vibration signal causes the swarm to take off and fly to the new nest location. In an experimental test, this decision-making process enabled honey bee swarms to choose the best nest site in four out of five trials.
Computing and robotics
Quorum sensing can be a useful tool for improving the function of self-organizing networks such as the SECOAS (Self-Organizing Collegiate Sensor) environmental monitoring system. In this system, individual nodes sense that there is a population of other nodes with similar data to report. The population then nominates just one node to report the data, resulting in power savings. Ad-hoc wireless networks can also benefit from quorum sensing, by allowing the system to detect and respond to network conditions.
Quorum sensing can also be used to coordinate the behavior of autonomous robot swarms. Using a process similar to that used by Temnothorax ants, robots can make rapid group decisions without the direction of a controller.
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- Dedicated issue of Philosophical Transactions B on quorum sensing (2007). Some articles are freely available.
- The Quorum Sensing Website
- Cell-to-Cell Communication in Bacteria
- The SECOAS project—Development of a Self-Organising, Wireless Sensor Network for Environmental Monitoring
- Measurement of Space: From Ants to Robots
- Instant insight into quorum sensing from the Royal Society of Chemistry
- Bonnie Bassler: Discovering bacteria's amazing communication system
- Bonnie Bassler's seminar: "Cell-Cell Communication in Bacteria"