Microbial cooperation
Encyclopedia
Microorganisms engage in a wide variety of social interactions, including cooperation
. A cooperative behavior is one that benefits an individual (the recipient) other than the one performing the behavior (the actor). This article outlines the various forms of cooperative interactions (mutualism and altruism) seen in microbial systems, as well as the benefits that might have driven the evolution of these complex behaviors.
, archaea
, virus
es, and many unicellular eukaryote
s (e.g., some fungi
and protist
s). Typically defined as unicellular life forms that can only be observed with a microscope, microorganisms were the first cellular life forms, and were critical for creating the conditions for the evolution of more complex multicellular forms.
Although microbes are too small to see with the naked eye, they represent the overwhelming majority of biological diversity, and thus serve as an excellent system to study evolutionary questions. One such topic that scientists have examined in microbes is the evolution of social behaviors, including cooperation. A cooperative interaction benefits a recipient, and is selected for on that basis. In microbial systems, cells belonging to the same taxa have been documented partaking in cooperative interactions to perform a wide range of complex multicellular behaviors such as dispersal, foraging, construction of biofilms, reproduction, chemical warfare, and signaling. This article will outline the various forms of cooperative interactions seen in microbial systems, as well as the benefits that might have driven the evolution of these complex behaviors.
From an evolutionary point of view, a behavior is social if it has fitness consequences for both the individual that performs that behavior (the actor) and another individual (the recipient). Hamilton first categorized social behaviors according to whether the consequences they entail for the actor and recipient are beneficial (increase direct fitness) or costly (decrease direct fitness). Based on Hamilton's definition, there are four unique types of social interactions
: mutualism (+/+), selfishness
(+/−), altruism
(−/+), and spite
(−/−) (Table 1). Mutualism and altruism are considered cooperative interactions because they are beneficial to the recipient, and will be the focus of this article.
Explaining cooperation remains one of the greatest challenges for evolutionary biology, regardless of whether the behavior is considered mutually beneficial or altruistic. According to classical evolutionary theory, an organism will only behave in ways that maximize its own fitness
. Therefore, the origin of cooperative interactions, or actions by individuals that result in other individuals receiving fitness benefits, seems counterintuitive.
Theoretical explanations for the evolution of cooperation can be broadly classified into two categories: direct fitness benefits or indirect fitness benefits. This follows from Hamilton's 1964 insight that individuals gain inclusive fitness directly through their impact on their own reproduction (direct fitness effects), as well as through their impact on the reproduction of individuals with related genes (indirect fitness effects).
One very popular example of mutually beneficial microbial interactions involves the production of siderophore
s. Siderophores are iron-scavenging molecules produced by many microbial taxa
, including bacteria and fungi. Iron is a major limiting factor for bacterial growth because most iron in the environment is in the insoluble Fe(III) form. In order for bacteria to access this limiting factor, cells will manufacture these enzymes, and then secrete them into the extracellular space. Once released, the siderophore will sequester the iron, making it metabolically accessible for the bacteria.
There are many explanations in place that justify the evolution of mutually beneficial interactions. Most importantly, in order for the production of public good
s to be evolutionarily beneficial, the behavior must provide a direct benefit to the reproductive performance of the actor that outweighs the cost of performing the behavior. While a siderophore is meant to benefit the cell that secretes it, this is not a guarantee. Rather, any cell that encounters the siderophore can access the iron. Therefore, this strategy will only be evolutionary sound if all cells in a given population secrete siderophores, and thus all cells in that population will share the cost and benefit of siderophore production.
While the production of public goods aims to benefit all individuals, it also leads to the evolution of cheaters, or individuals that do not pay the cost of producing a good, but still receive benefits (Figure 1). In order to minimize fitness costs, natural selection will favor individuals that do not to secrete while taking advantage of the secretions of their neighbors. In a population of siderophore secreting cells, non-secreting mutant cells do not pay the cost of secretion, but still gain the same benefit as the wild-type neighbors. Recently, Griffin et al. (2004) investigated the social nature of the production of siderophores in Pseudomonas aeruginosa
. When cells were grown in pure culture were placed in an iron-limiting environment, populations of cells that secreted siderophores (wild-type) outcompeted a population of mutant
non-secretors. Therefore, siderophore production is beneficial when iron is limiting. However, when the same populations were placed in an iron-rich environment, the mutant population outcompeted wild-type population, demonstrating that siderophore production is metabolically costly. Finally, when both wild type and mutant bacteria were placed in the same mixed population, the mutants can gain the benefit of siderophore production without paying the cost, and hence increase in frequency. This concept is commonly referred to the tragedy of the commons
.
The prisoner's dilemma
game is another way that evolutionary biologists explain the presence of cheating in cooperative microbial systems. Originally framed by Merrill Flood and Melvin Dresher
in 1950, the Prisoner's Dilemma is a fundamental problem in game theory
, and demonstrates that two individuals might not cooperate even if it is in both their best interests to do so. In the dilemma, two individuals each choose whether to cooperate with the other individual or to cheat. Cooperation by both individuals gives the greatest average advantage. However, if one individual decides to cheat, they will obtain a greater individual advantage. If the game is played only once cheating is the superior strategy since it is the superior strategy. However, in biologically realistic situations, with repeated interactions (games), mutations, and heterogeneous environments, there is often no single stable solution and the success of individual strategies can vary in endless periodic or chaotic cycles.
Greig & Travisano (2004) addressed these ideas with an experimental study on Saccharomyces cerevisiae
. S. cerevisiae possesses multiple genes that each produce invertase
, an enzyme that is secreted to digest sucrose outside of the cell. As discussed above, this public good production creates the potential for individual cells to cheat by stealing the sugar digested by their neighbors without contributing the enzyme themselves. Greig & Travisano (2004) measured the fitness of a cheater type (who possessed a reduced number of invertase genes) relative to a cooperator (who contained all possible invertase genes). By manipulating the level of social interaction within the community by varying the population density, they found that the cheater is less fit than the cooperator at low levels of sociality, but more fit in dense communities. Therefore, they propose that selection for "cheating" causes natural variation in the amount of invertase genes an individual may possess, and that variation in invertase genes reflects constant adaptation to an ever changing biotic environment that is a consequence of the instability of cooperative interactions.
. According to Hamilton, an altruistic act is evolutionarily beneficial if the relatedness of the individual that profits from the altruistic act is higher than the cost/benefit ratio this act imposes. This rationale is referred to as Hamilton's rule.
Natural selection
normally favors a gene if it increases reproduction, because the offspring share copies of that gene. However, a gene can also be favored if it aids other relatives, who also share copies. Therefore, by helping a close relative reproduce, an individual is still passing on its own genes to the next generation, albeit indirectly. Hamilton pointed out that kin selection could occur via two mechanisms: (a) kin discrimination, when cooperation is preferentially directed toward relatives, and (b) limited dispersal (population viscosity), which keeps relatives in spatial proximity to one another, allowing cooperation to be directed indiscriminately toward all neighbors (who tend to be relatives). In microbial systems, these two mechanisms are equally important. For example, most microbial populations often begin from a small number of colonizers. Because most microbes reproduce asexually
, close genetic relatives will surround cells as the population grows. These clonal populations often result in an extremely high density, especially in terrestrial systems. Therefore, the probability that a cells altruistic behavior will benefit a close relative is extremely high.
While altruistic behaviors are most common between individuals with high genetic relatedness, it is not completely necessary. Altruistic behaviors can also be evolutionarily beneficial if the cooperation is directed towards individuals who share the gene of interest, regardless of whether this is due to coancestry or some other mechanism. An example of this is known as the "green beard
" mechanism, and requires a single gene (or a number of tightly linked genes) that both causes the cooperative behavior and can be recognized by other individuals due to a distinctive phenotypic marker, such as a green beard.
The most studied slime mold from this perspective is Dictyostelium discoideum
, a predator of bacteria that is common in the soil. When starving, the usually solitary single-celled amoebae aggregate and form a multicellullar slug that can contain 104–106 cells. This slug migrates to the soil surface, where it transforms into a fruiting body composed of a spherical tip of spores and a stalk consisting of nonviable stalk cells that hold the spores aloft (Figure 2). Roughly 20% of the cells develop into the non-reproductive stalk, elevating the spores and aiding their dispersal.
Programmed cell death (PCD) is another suggested form of microbial altruistic behavior. Although programmed cell death (also known as apoptosis
or autolysis
) clearly provides no direct fitness benefit, it can be evolutionary adaptive if it provides indirect benefits to individuals with high genetic relatedness (kin selection
). Several altruistic possibilities have been suggested for PCD, such as providing resources that could be used by other cells for growth and survival in Saccharomyces cerevisiae
. While using kin selection to explain the evolutionary benefits of PCD is common, the reasoning contains some inherent problems. Charlesworth (1978) noted that it is extremely hard for a gene causing suicide to spread because only relatives that do NOT share the gene would ultimately benefit. Therefore, the possible solution to this problem in microbes is that selection could favor a low probability of PCD among a large population of cells, possibly depending upon individual condition, environmental conditions, or signaling.
are controlled by cell-cell signaling systems. One way that microbes communicate and organize with each other in order to partake in more advanced cooperative interactions is through quorum sensing
. Quorum sensing describes the phenomenon in which the accumulation of signaling molecules in the surrounding environment enables a single cell to assess the number of individuals (cell density) so that the population as a whole can make a coordinated response. This interaction is fairly common among bacterial taxa, and involves the secretion by individual cells of 'signaling' molecules. called autoinducer
s or pheromone
s.These bacteria also have a receptor
that can specifically detect the signaling molecule. When the inducer binds the receptor, it activates transcription
of certain genes, including those for inducer synthesis. There is a low likelihood of a bacterium detecting its own secreted inducer. Thus, in order for gene transcription to be activated, the cell must encounter signaling molecules secreted by other cells in its environment. When only a few other bacteria of the same kind are in the vicinity, diffusion
reduces the concentration of the inducer in the surrounding medium to almost zero, so the bacteria produce little inducer. However, as the population grows the concentration of the inducer passes a threshold, causing more inducer to be synthesized. This forms a positive feedback loop, and the receptor becomes fully activated. Activation of the receptor induces the up regulation of other specific genes, causing all of the cells to begin transcription at approximately the same time. In other words, when the local concentration of these molecules has reached a threshold, the cells respond by switching on particular genes. In this way individual cells can sense the local density of bacteria, so that the population as a whole can make a coordinated response.
In many situations, the cost bacterial cells pay in order to coordinate behaviors outweighs the benefits unless there is a sufficient number of collaborators. For instance, the bioluminescent luciferase
produced by Vibrio fischeri
would not be visible if it was produced by a single cell. By using quorum sensing to limit the production of luciferase to situations when cell populations are large, V. fischeri cells are able to avoid wasting energy on the production of useless product. In many situations bacterial activities, such as the production of the mentioned public goods, are only worthwhile as a joint activity by a sufficient number of collaborators. Regulation by quorum sensing would allow the cells to express appropriate behavior only when it is effective, thus saving resources under low density conditions. Therefore, quorum sensing has been interpreted as a bacterial communication system to coordinate behaviors at the population level.
The opportunistic bacteria Pseudomonas aeruginosa
also uses quorum sensing to coordinate the formation of biofilms, swarming motility
, exopolysaccharide
production, and cell aggregation. These bacteria can grow within a host without harming it, until they reach a certain concentration. Then they become aggressive, their numbers sufficient to overcome the host's immune system, and form a biofilm, leading to disease within the host. 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. 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 inhibition.
, including the evolution of multicellularity
. This idea, often referred to as the Colonial Theory, was first proposed by Haeckel in 1874, and claims that the symbiosis of many organisms of the same species (unlike the symbiotic theory, which suggests the symbiosis of different species) led to a multicellular organism. In a few instances, multicellularity occurs by cells separating and then rejoining (e.g., cellular slime molds) whereas for the majority of multicellular types, multicellularity occurs as a consequence of cells failing to separate following division. The mechanism of this latter colony formation can be as simple as incomplete cytokinesis, though multicellularity is also typically considered to involve cellular differentiation.
The advantage of the Colonial Theory hypothesis is that it has been seen to occur independently numerous times (in 16 different protoctistan phyla). For instance, during food shortages Dictyostelium discoideum
cells group together in a colony that moves as one to a new location. Some of these cells then slightly differentiate from each other. Other examples of colonial organisation in protozoa are Volvocaceae
, such as Eudorina
and Volvox
. However, it can often be hard to separate colonial protists from true multicellular organisms, as the two concepts are not distinct. This problem plagues most hypotheses of how multicellularisation could have occurred. However, most scientists accept that multicellular organisms, from all phyla, evolved by the colonial mechanism.
Co-operation (evolution)
Co-operation or co-operative behaviours are terms used to describe behaviours by organisms which are beneficial to other organisms, and are selected for on that basis. Under this definition, altruism is a form of co-operation in which there is no direct benefit to the actor...
. A cooperative behavior is one that benefits an individual (the recipient) other than the one performing the behavior (the actor). This article outlines the various forms of cooperative interactions (mutualism and altruism) seen in microbial systems, as well as the benefits that might have driven the evolution of these complex behaviors.
Introduction
Microorganisms, or microbes, span all three domains of life, including bacteriaBacteria
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...
, archaea
Archaea
The Archaea are a group of single-celled microorganisms. A single individual or species from this domain is called an archaeon...
, virus
Virus
A virus is a small infectious agent that can replicate only inside the living cells of organisms. Viruses infect all types of organisms, from animals and plants to bacteria and archaea...
es, and many unicellular eukaryote
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...
s (e.g., some fungi
Fungus
A fungus is a member of a large group of eukaryotic organisms that includes microorganisms such as yeasts and molds , as well as the more familiar mushrooms. These organisms are classified as a kingdom, Fungi, which is separate from plants, animals, and bacteria...
and protist
Protist
Protists are a diverse group of eukaryotic microorganisms. Historically, protists were treated as the kingdom Protista, which includes mostly unicellular organisms that do not fit into the other kingdoms, but this group is contested in modern taxonomy...
s). Typically defined as unicellular life forms that can only be observed with a microscope, microorganisms were the first cellular life forms, and were critical for creating the conditions for the evolution of more complex multicellular forms.
Although microbes are too small to see with the naked eye, they represent the overwhelming majority of biological diversity, and thus serve as an excellent system to study evolutionary questions. One such topic that scientists have examined in microbes is the evolution of social behaviors, including cooperation. A cooperative interaction benefits a recipient, and is selected for on that basis. In microbial systems, cells belonging to the same taxa have been documented partaking in cooperative interactions to perform a wide range of complex multicellular behaviors such as dispersal, foraging, construction of biofilms, reproduction, chemical warfare, and signaling. This article will outline the various forms of cooperative interactions seen in microbial systems, as well as the benefits that might have driven the evolution of these complex behaviors.
History
| Effect on recipient | |||
| + | − | ||
| Effect on actor |
+ | Mutual benefit | Selfishness |
| − | Altruism | Spite | |
From an evolutionary point of view, a behavior is social if it has fitness consequences for both the individual that performs that behavior (the actor) and another individual (the recipient). Hamilton first categorized social behaviors according to whether the consequences they entail for the actor and recipient are beneficial (increase direct fitness) or costly (decrease direct fitness). Based on Hamilton's definition, there are four unique types of social interactions
Social evolution
Social evolution is a subdiscipline of evolutionary biology that is concerned with social behaviors that have fitness consequences for individuals other than the actor...
: mutualism (+/+), selfishness
Selfishness
Selfishness denotes an excessive or exclusive concern with oneself, and as such it exceeds mere self interest or self concern. Insofar as a decision maker knowingly burdens or harms others for personal gain, the decision is selfish. In contrast, self-interest is more general...
(+/−), altruism
Altruism
Altruism is a concern for the welfare of others. It is a traditional virtue in many cultures, and a core aspect of various religious traditions, though the concept of 'others' toward whom concern should be directed can vary among cultures and religions. Altruism is the opposite of...
(−/+), and spite
Spite
In fair division problems, spite is a phenomenon that occurs when a player's value of an allocation decreases when one or more other players' valuation increases...
(−/−) (Table 1). Mutualism and altruism are considered cooperative interactions because they are beneficial to the recipient, and will be the focus of this article.
Explaining cooperation remains one of the greatest challenges for evolutionary biology, regardless of whether the behavior is considered mutually beneficial or altruistic. According to classical evolutionary theory, an organism will only behave in ways that maximize its own fitness
Fitness (biology)
Fitness is a central idea in evolutionary theory. It can be defined either with respect to a genotype or to a phenotype in a given environment...
. Therefore, the origin of cooperative interactions, or actions by individuals that result in other individuals receiving fitness benefits, seems counterintuitive.
Theoretical explanations for the evolution of cooperation can be broadly classified into two categories: direct fitness benefits or indirect fitness benefits. This follows from Hamilton's 1964 insight that individuals gain inclusive fitness directly through their impact on their own reproduction (direct fitness effects), as well as through their impact on the reproduction of individuals with related genes (indirect fitness effects).
Mutualism
Perhaps the most common cooperative interactions seen in microbial systems are mutually beneficial (+/+). Mutually beneficial social interactions provide a direct fitness benefit to the individual that performs the behavior, which outweighs the cost of performing the behavior. Most of the time, individuals partaking in the behaviors have a shared interest in cooperation. In microbial systems, this is most often seen as the production of public goods. Many microbes, especially bacteria, produce numerous factors that are released into the environment beyond the cell membrane.One very popular example of mutually beneficial microbial interactions involves the production of siderophore
Siderophore
Siderophores are small, high-affinity iron chelating compounds secreted by grasses and microorganisms such as bacteria and fungi...
s. Siderophores are iron-scavenging molecules produced by many microbial taxa
Taxon
|thumb|270px|[[African elephants]] form a widely-accepted taxon, the [[genus]] LoxodontaA taxon is a group of organisms, which a taxonomist adjudges to be a unit. Usually a taxon is given a name and a rank, although neither is a requirement...
, including bacteria and fungi. Iron is a major limiting factor for bacterial growth because most iron in the environment is in the insoluble Fe(III) form. In order for bacteria to access this limiting factor, cells will manufacture these enzymes, and then secrete them into the extracellular space. Once released, the siderophore will sequester the iron, making it metabolically accessible for the bacteria.
There are many explanations in place that justify the evolution of mutually beneficial interactions. Most importantly, in order for the production of public good
Public good
In economics, a public good is a good that is non-rival and non-excludable. Non-rivalry means that consumption of the good by one individual does not reduce availability of the good for consumption by others; and non-excludability means that no one can be effectively excluded from using the good...
s to be evolutionarily beneficial, the behavior must provide a direct benefit to the reproductive performance of the actor that outweighs the cost of performing the behavior. While a siderophore is meant to benefit the cell that secretes it, this is not a guarantee. Rather, any cell that encounters the siderophore can access the iron. Therefore, this strategy will only be evolutionary sound if all cells in a given population secrete siderophores, and thus all cells in that population will share the cost and benefit of siderophore production.
While the production of public goods aims to benefit all individuals, it also leads to the evolution of cheaters, or individuals that do not pay the cost of producing a good, but still receive benefits (Figure 1). In order to minimize fitness costs, natural selection will favor individuals that do not to secrete while taking advantage of the secretions of their neighbors. In a population of siderophore secreting cells, non-secreting mutant cells do not pay the cost of secretion, but still gain the same benefit as the wild-type neighbors. Recently, Griffin et al. (2004) investigated the social nature of the production of siderophores in Pseudomonas aeruginosa
Pseudomonas aeruginosa
Pseudomonas aeruginosa is a common bacterium that can cause disease in animals, including humans. It is found in soil, water, skin flora, and most man-made environments throughout the world. It thrives not only in normal atmospheres, but also in hypoxic atmospheres, and has, thus, colonized many...
. When cells were grown in pure culture were placed in an iron-limiting environment, populations of cells that secreted siderophores (wild-type) outcompeted a population of mutant
Mutant
In biology and especially genetics, a mutant is an individual, organism, or new genetic character, arising or resulting from an instance of mutation, which is a base-pair sequence change within the DNA of a gene or chromosome of an organism resulting in the creation of a new character or trait not...
non-secretors. Therefore, siderophore production is beneficial when iron is limiting. However, when the same populations were placed in an iron-rich environment, the mutant population outcompeted wild-type population, demonstrating that siderophore production is metabolically costly. Finally, when both wild type and mutant bacteria were placed in the same mixed population, the mutants can gain the benefit of siderophore production without paying the cost, and hence increase in frequency. This concept is commonly referred to the tragedy of the commons
Tragedy of the commons
The tragedy of the commons is a dilemma arising from the situation in which multiple individuals, acting independently and rationally consulting their own self-interest, will ultimately deplete a shared limited resource, even when it is clear that it is not in anyone's long-term interest for this...
.
The prisoner's dilemma
Prisoner's dilemma
The prisoner’s dilemma is a canonical example of a game, analyzed in game theory that shows why two individuals might not cooperate, even if it appears that it is in their best interest to do so. It was originally framed by Merrill Flood and Melvin Dresher working at RAND in 1950. Albert W...
game is another way that evolutionary biologists explain the presence of cheating in cooperative microbial systems. Originally framed by Merrill Flood and Melvin Dresher
Melvin Dresher
Melvin Dresher was a Polish-born American mathematician, notable for developing, with Merrill Flood, the game theoretical model of cooperation and conflict known as the Prisoner's Dilemma while at RAND in 1950 .Dresher came to the United States in 1923...
in 1950, the Prisoner's Dilemma is a fundamental problem in game theory
Game theory
Game theory is a mathematical method for analyzing calculated circumstances, such as in games, where a person’s success is based upon the choices of others...
, and demonstrates that two individuals might not cooperate even if it is in both their best interests to do so. In the dilemma, two individuals each choose whether to cooperate with the other individual or to cheat. Cooperation by both individuals gives the greatest average advantage. However, if one individual decides to cheat, they will obtain a greater individual advantage. If the game is played only once cheating is the superior strategy since it is the superior strategy. However, in biologically realistic situations, with repeated interactions (games), mutations, and heterogeneous environments, there is often no single stable solution and the success of individual strategies can vary in endless periodic or chaotic cycles.
Greig & Travisano (2004) addressed these ideas with an experimental study on Saccharomyces cerevisiae
Saccharomyces cerevisiae
Saccharomyces cerevisiae is a species of yeast. It is perhaps the most useful yeast, having been instrumental to baking and brewing since ancient times. It is believed that it was originally isolated from the skin of grapes...
. S. cerevisiae possesses multiple genes that each produce invertase
Invertase
Invertase is an enzyme that catalyzes the hydrolysis of sucrose . The resulting mixture of fructose and glucose is called inverted sugar syrup. Related to invertases are sucrases. Invertases and sucrases hydrolyze sucrose to give the same mixture of glucose and fructose...
, an enzyme that is secreted to digest sucrose outside of the cell. As discussed above, this public good production creates the potential for individual cells to cheat by stealing the sugar digested by their neighbors without contributing the enzyme themselves. Greig & Travisano (2004) measured the fitness of a cheater type (who possessed a reduced number of invertase genes) relative to a cooperator (who contained all possible invertase genes). By manipulating the level of social interaction within the community by varying the population density, they found that the cheater is less fit than the cooperator at low levels of sociality, but more fit in dense communities. Therefore, they propose that selection for "cheating" causes natural variation in the amount of invertase genes an individual may possess, and that variation in invertase genes reflects constant adaptation to an ever changing biotic environment that is a consequence of the instability of cooperative interactions.
Altruism
The second type of cooperative interactions is altruistic, or interactions that are beneficial to the recipient but costly to the actor (-/+). Justifying the evolutionary benefit of altruistic behavior is a highly-debated topic. A common justification for the presence of altruistic behaviors is that they provide an indirect benefit because the behavior is directed towards other individuals who carry the cooperative gene. The simplest and most common reason for two individuals to share genes in common is for them to be genealogical relatives (kin), and so this is often termed kin selectionKin selection
Kin selection refers to apparent strategies in evolution that favor the reproductive success of an organism's relatives, even at a cost to the organism's own survival and reproduction. Charles Darwin was the first to discuss the concept of group/kin selection...
. According to Hamilton, an altruistic act is evolutionarily beneficial if the relatedness of the individual that profits from the altruistic act is higher than the cost/benefit ratio this act imposes. This rationale is referred to as Hamilton's rule.
Natural selection
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....
normally favors a gene if it increases reproduction, because the offspring share copies of that gene. However, a gene can also be favored if it aids other relatives, who also share copies. Therefore, by helping a close relative reproduce, an individual is still passing on its own genes to the next generation, albeit indirectly. Hamilton pointed out that kin selection could occur via two mechanisms: (a) kin discrimination, when cooperation is preferentially directed toward relatives, and (b) limited dispersal (population viscosity), which keeps relatives in spatial proximity to one another, allowing cooperation to be directed indiscriminately toward all neighbors (who tend to be relatives). In microbial systems, these two mechanisms are equally important. For example, most microbial populations often begin from a small number of colonizers. Because most microbes reproduce asexually
Asexual reproduction
Asexual reproduction is a mode of reproduction by which offspring arise from a single parent, and inherit the genes of that parent only, it is reproduction which does not involve meiosis, ploidy reduction, or fertilization. A more stringent definition is agamogenesis which is reproduction without...
, close genetic relatives will surround cells as the population grows. These clonal populations often result in an extremely high density, especially in terrestrial systems. Therefore, the probability that a cells altruistic behavior will benefit a close relative is extremely high.
While altruistic behaviors are most common between individuals with high genetic relatedness, it is not completely necessary. Altruistic behaviors can also be evolutionarily beneficial if the cooperation is directed towards individuals who share the gene of interest, regardless of whether this is due to coancestry or some other mechanism. An example of this is known as the "green beard
Green-beard effect
The gene-centered view of evolution postulates that natural selection will increase the frequency of those genes whose phenotypic effects ensure their successful replication...
" mechanism, and requires a single gene (or a number of tightly linked genes) that both causes the cooperative behavior and can be recognized by other individuals due to a distinctive phenotypic marker, such as a green beard.
The most studied slime mold from this perspective is Dictyostelium discoideum
Dictyostelium discoideum
Dictyostelium discoideum is a species of soil-living amoeba belonging to the phylum Mycetozoa. D. discoideum, commonly referred to as slime mold, is a eukaryote that transitions from a collection of unicellular amoebae into a multicellular slug and then into a fruiting body within its lifetime. D...
, a predator of bacteria that is common in the soil. When starving, the usually solitary single-celled amoebae aggregate and form a multicellullar slug that can contain 104–106 cells. This slug migrates to the soil surface, where it transforms into a fruiting body composed of a spherical tip of spores and a stalk consisting of nonviable stalk cells that hold the spores aloft (Figure 2). Roughly 20% of the cells develop into the non-reproductive stalk, elevating the spores and aiding their dispersal.
Programmed cell death (PCD) is another suggested form of microbial altruistic behavior. Although programmed cell death (also known as apoptosis
Apoptosis
Apoptosis is the process of programmed cell death that may occur in multicellular organisms. Biochemical events lead to characteristic cell changes and death. These changes include blebbing, cell shrinkage, nuclear fragmentation, chromatin condensation, and chromosomal DNA fragmentation...
or autolysis
Autolysis (biology)
In biology, autolysis, more commonly known as self-digestion, refers to the destruction of a cell through the action of its own enzymes. It may also refer to the digestion of an enzyme by another molecule of the same enzyme....
) clearly provides no direct fitness benefit, it can be evolutionary adaptive if it provides indirect benefits to individuals with high genetic relatedness (kin selection
Kin selection
Kin selection refers to apparent strategies in evolution that favor the reproductive success of an organism's relatives, even at a cost to the organism's own survival and reproduction. Charles Darwin was the first to discuss the concept of group/kin selection...
). Several altruistic possibilities have been suggested for PCD, such as providing resources that could be used by other cells for growth and survival in Saccharomyces cerevisiae
Saccharomyces cerevisiae
Saccharomyces cerevisiae is a species of yeast. It is perhaps the most useful yeast, having been instrumental to baking and brewing since ancient times. It is believed that it was originally isolated from the skin of grapes...
. While using kin selection to explain the evolutionary benefits of PCD is common, the reasoning contains some inherent problems. Charlesworth (1978) noted that it is extremely hard for a gene causing suicide to spread because only relatives that do NOT share the gene would ultimately benefit. Therefore, the possible solution to this problem in microbes is that selection could favor a low probability of PCD among a large population of cells, possibly depending upon individual condition, environmental conditions, or signaling.
Quorum sensing
The integration of cooperative and communicative interactions appear to be extremely important to microbes; for example, 6–10% of all genes in the bacterium Pseudomonas aeruginosaPseudomonas aeruginosa
Pseudomonas aeruginosa is a common bacterium that can cause disease in animals, including humans. It is found in soil, water, skin flora, and most man-made environments throughout the world. It thrives not only in normal atmospheres, but also in hypoxic atmospheres, and has, thus, colonized many...
are controlled by cell-cell signaling systems. One way that microbes communicate and organize with each other in order to partake in more advanced cooperative interactions is through quorum sensing
Quorum sensing
Quorum sensing is a system of stimulus and response correlated to population density. 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...
. Quorum sensing describes the phenomenon in which the accumulation of signaling molecules in the surrounding environment enables a single cell to assess the number of individuals (cell density) so that the population as a whole can make a coordinated response. This interaction is fairly common among bacterial taxa, and involves the secretion by individual cells of 'signaling' molecules. called autoinducer
Autoinducer
Autoinducers are chemical signaling molecules that are produced and used by bacteria participating in quorum sensing. Quorum sensing is a phenomenon that allows both Gram-negative and Gram-positive bacteria to sense one another and to regulate a wide variety of physiological activities. Such...
s or pheromone
Pheromone
A pheromone is a secreted or excreted chemical factor that triggers a social response in members of the same species. Pheromones are chemicals capable of acting outside the body of the secreting individual to impact the behavior of the receiving individual...
s.These bacteria also have a receptor
Receptor (biochemistry)
In biochemistry, a receptor is a molecule found on the surface of a cell, which receives specific chemical signals from neighbouring cells or the wider environment within an organism...
that can specifically detect the signaling molecule. When the inducer binds the receptor, it activates transcription
Transcription (genetics)
Transcription is the process of creating a complementary RNA copy of a sequence of DNA. Both RNA and DNA are nucleic acids, which use base pairs of nucleotides as a complementary language that can be converted back and forth from DNA to RNA by the action of the correct enzymes...
of certain genes, including those for inducer synthesis. There is a low likelihood of a bacterium detecting its own secreted inducer. Thus, in order for gene transcription to be activated, the cell must encounter signaling molecules secreted by other cells in its environment. When only a few other bacteria of the same kind are in the vicinity, diffusion
Diffusion
Molecular diffusion, often called simply diffusion, is the thermal motion of all particles at temperatures above absolute zero. The rate of this movement is a function of temperature, viscosity of the fluid and the size of the particles...
reduces the concentration of the inducer in the surrounding medium to almost zero, so the bacteria produce little inducer. However, as the population grows the concentration of the inducer passes a threshold, causing more inducer to be synthesized. This forms a positive feedback loop, and the receptor becomes fully activated. Activation of the receptor induces the up regulation of other specific genes, causing all of the cells to begin transcription at approximately the same time. In other words, when the local concentration of these molecules has reached a threshold, the cells respond by switching on particular genes. In this way individual cells can sense the local density of bacteria, so that the population as a whole can make a coordinated response.
In many situations, the cost bacterial cells pay in order to coordinate behaviors outweighs the benefits unless there is a sufficient number of collaborators. For instance, the bioluminescent luciferase
Luciferase
Luciferase is a generic term for the class of oxidative enzymes used in bioluminescence and is distinct from a photoprotein. One famous example is the firefly luciferase from the firefly Photinus pyralis. "Firefly luciferase" as a laboratory reagent usually refers to P...
produced by Vibrio fischeri
Vibrio fischeri
Vibrio fischeri is a gram-negative rod-shaped bacterium found globally in marine environments. V. fischeri has bioluminescent properties, and is found predominantly in symbiosis with various marine animals, such as the bobtail squid. It is heterotrophic and moves by means of flagella. Free living...
would not be visible if it was produced by a single cell. By using quorum sensing to limit the production of luciferase to situations when cell populations are large, V. fischeri cells are able to avoid wasting energy on the production of useless product. In many situations bacterial activities, such as the production of the mentioned public goods, are only worthwhile as a joint activity by a sufficient number of collaborators. Regulation by quorum sensing would allow the cells to express appropriate behavior only when it is effective, thus saving resources under low density conditions. Therefore, quorum sensing has been interpreted as a bacterial communication system to coordinate behaviors at the population level.
The opportunistic bacteria Pseudomonas aeruginosa
Pseudomonas aeruginosa
Pseudomonas aeruginosa is a common bacterium that can cause disease in animals, including humans. It is found in soil, water, skin flora, and most man-made environments throughout the world. It thrives not only in normal atmospheres, but also in hypoxic atmospheres, and has, thus, colonized many...
also uses quorum sensing to coordinate the formation of biofilms, swarming motility
Swarming motility
Swarming motility is a rapid and coordinated translocation of a bacterial population across solid or semi-solid surfaces. This type of motility is an example of an emerging concept in microbiology : bacterial multicellularity...
, exopolysaccharide
Exopolysaccharide
Exopolysaccharides are high-molecular-weight polymers that are composed of sugar residues and are secreted by a microorganism into the surrounding environment. Microorganisms synthesize a wide spectrum of multifunctional polysaccharides including intracellular polysaccharides, structural...
production, and cell aggregation. These bacteria can grow within a host without harming it, until they reach a certain concentration. Then they become aggressive, their numbers sufficient to overcome the host's immune system, and form a biofilm, leading to disease within the host. 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. 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 inhibition.
Implications
While the evolution of cooperative interactions allowed microbial taxa to increase their fitness, it is hypothesized that cooperation provided a proximate cause to other major evolutionary transitionsThe Major Transitions in Evolution
The Major Transitions in Evolution is a book written by John Maynard Smith and Eörs Szathmáry . This was a seminal publication that continues to contribute to ongoing issues in evolutionary biology....
, including the evolution of multicellularity
Multicellular organism
Multicellular organisms are organisms that consist of more than one cell, in contrast to single-celled organisms. Most life that can be seen with the the naked eye is multicellular, as are all animals and land plants.-Evolutionary history:Multicellularity has evolved independently dozens of times...
. This idea, often referred to as the Colonial Theory, was first proposed by Haeckel in 1874, and claims that the symbiosis of many organisms of the same species (unlike the symbiotic theory, which suggests the symbiosis of different species) led to a multicellular organism. In a few instances, multicellularity occurs by cells separating and then rejoining (e.g., cellular slime molds) whereas for the majority of multicellular types, multicellularity occurs as a consequence of cells failing to separate following division. The mechanism of this latter colony formation can be as simple as incomplete cytokinesis, though multicellularity is also typically considered to involve cellular differentiation.
The advantage of the Colonial Theory hypothesis is that it has been seen to occur independently numerous times (in 16 different protoctistan phyla). For instance, during food shortages Dictyostelium discoideum
Dictyostelium discoideum
Dictyostelium discoideum is a species of soil-living amoeba belonging to the phylum Mycetozoa. D. discoideum, commonly referred to as slime mold, is a eukaryote that transitions from a collection of unicellular amoebae into a multicellular slug and then into a fruiting body within its lifetime. D...
cells group together in a colony that moves as one to a new location. Some of these cells then slightly differentiate from each other. Other examples of colonial organisation in protozoa are Volvocaceae
Volvocaceae
The Volvocaceae are a family of unicellular or colonial biflagellates, including the typical genus Volvox. The family was named by Ehrenberg in 1834, and is known in older classifications as the Volvocidae.- Description :...
, such as Eudorina
Eudorina
In taxonomy, Eudorina is a genus of colonial green algae, specifically of the Volvocaceae. Eudorina colonies consist of 32 individual cells grouped together. Each individual cell contains flagella which allow the colony to move as a whole when the individual cells beat their flagella together...
and Volvox
Volvox
Volvox is a genus of chlorophytes, a type of green algae. It forms spherical colonies of up to 50,000 cells. They live in a variety of freshwater habitats, and were first reported by Antonie van Leeuwenhoek in 1700. Volvox developed its colonial lifestyle .-Description:Volvox is the most developed...
. However, it can often be hard to separate colonial protists from true multicellular organisms, as the two concepts are not distinct. This problem plagues most hypotheses of how multicellularisation could have occurred. However, most scientists accept that multicellular organisms, from all phyla, evolved by the colonial mechanism.