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10.1: Microbial communities

The organisms within a particular community are often critically dependent upon one another. Some organisms will secrete nutrients that are needed by others for their survival. Our own need for vitamins, molecules obtained from our diet, reflects this interdependence. Some organisms secrete toxins to control the growth of others. Some secrete molecules that influence the behaviors of other organisms (including themselves). There are complex molecular level conversations going on between the organisms within an ecosystem and the cells within an organism. Organisms are not independent, their behaviors are altered by their environment and they in turn, alter their environment.

An example of how even the simplest organisms can cooperate is an effect known as quorum sensing (which we have mentioned previously.) A bacterium of a particular species can secrete factors that are useful, for example, in the digestion of food into soluble nutrient molecules that it can ingest. But when growing in sparse situations (few organisms per unit volume or area), such a strategy is not efficient. If organisms at low density in a aqueous environment the expensive to produce secreted molecules are more likely to diffuse away and so be effectively useless to the organism that produced them. However if organisms are present at high local densities, then the process becomes more efficient, the concentration of the secreted molecules increases reaching useful levels. By cooperating with their neighbors to produce a mutually beneficial behavior, each individual benefits.

How might this type of cooperation work? In bacteria a common strategy is for individuals to produce and secrete small (relatively energetically inexpensive) molecules known as auto-inducers. They also produce a cellular receptor specific for this auto-inducer. The auto-inducer-receptor system enables organisms of the same type to recognize each other’s presence. The system works because the level of auto-inducer produced by a single bacterium is not sufficient to activate its receptors; only when the density of auto-inducer-secreting bacteria reaches a threshold level does the concentration of auto-inducer increase to a level high enough to activate the receptors. Activation of the auto-inducer- receptor generates a signal that in turn influences the bacterium’s behavior (including gene expression)303. One obvious behavior could be the secretion of digestive enzymes, but there are a number of others. For example, some types of bacteria (including E. coli) use quorum sensing to control cell migration. Over time individual cells migrate using their swimming system. One such system relies on flagellar (rotary) motors driven by electrochemical gradients to move the cell forward. In the absence of such a gradient, the motor reverse causing the cell to tumble and change direction. When moving up a gradient of attractant, or down a gradient of repulsant, tumbling is suppressed; the end result is directed movement.

This type of behavior has been illustrated dramatically by using E. coli that contains a plasmid that encodes the Green Fluorescent Protein (GFP), a protein thatwhen illuminated with blue light glows green304! When GFP-expressing E. coli are cultured in a maze-like environment with a central “chamber” with a single opening, the secreted attractant accumulates to high concentrations within this space. Over a three hour period the bacteria swim in a directed manner up the attractant concentration gradient into the chamber305. At this point quorum sensing-controlled behaviors are activated. For example in situations where nutrients become scarce a quorum sensing controlled behavior can lead some of the cells in the population to die, a process known as programmed cell death, releasing their nutrients for their neighbors to use. This can be seen as a type of altruism, since it helps the neighbors, who are likely to be relatives of the sacrificing cell306. Another type of behavior that can occur under condition of stress is that a subpopulation of cells, known as quiescent or “persister” cells, grow slowly or not at all, while the rest of the population continues to grow307. If the environment turns seriously hostile the persisters have a much higher probability of survival than do the actively growing cells. If conditions improve the persisters can reverse their behavior and reestablish an actively growing population. On the other hand, if the conditions never get hostile, the growing cells have an evolutionary advantage over cells that go quiescent. This implies the presence of a system can produce persisters when they might be useful, and surpress their formation when not. The ability of an organism to produce quiescent persister state helps insure the survival of the population within a wider range of environments than would be expected for a population that cannot produce persisters. This is a example of group selection. A similar behavior has been found to occur within populations of cancer cells308. Persister cells can survive therapeutic treatments and re-emerge later. We have already seen, in the context of the lac operon, how an initially uniform population of organisms can produce distinct phenotypes through stochastic processes; similar random events play an important role in the determination of cell fates in many social situations.

Social cooperation between cells can provide benefits, but also opens up the system to selfish behaviors, essentially cheating309. This raises the evolutionary question what can be done to surpress the emergence of social cheaters? First, what exactly do we mean by a social cheater? In the context of quorum sensing, suppose an individual does not make the auto-inducer, but continues to make its receptor. The cheater gains the benefits of communicating with other bacteria, but minimizes its contribution to the process (it does not use energy to synthesize the autoinducer). It might well gain an advantage in that the energy used to make the auto-inducer could instead be used for growth and reproduction. There are inherent limits to cheating, however. If enough members of a group (population) become cheaters the quorum sensing system will fail because not enough members of the community secrete the auto-inducer. Assuming that the social behavior is critical for the survival of the population, a group with too many cheaters may die out (become extinct).

There are other more pro-active strategies that can be used to suppress cheaters. It may be that the production of the auto-inducer is a by-product of an essential reaction. In this case, loss of the ability to produce the auto-inducer could itself lead to death (the organisms become addicted to the autoinducer). Many bacterial species synthesize toxins to which they themselves are immune, but which kill cells of related species. It can be that toxin immunity is coupled to auto-inducer expression. In higher organisms there can be the development of the ability to recognize cheaters by their behavior in certain situations. We can think of cancer (tumor formation) as a form of social cheating with a multicellular organism, and their are mechanisms that are to suppress it (although we will not have to time to explore them to any significant extent).

References

303 Bacterial quorum-sensing network architectures: http://www.ncbi.nlm.nih.gov/pubmed/19686078

304The original green fluorescent protein evolved in jelly fish Aequorea victori a, it is one of a multigene family of fluorescent proteins: see GFP-like Proteins as Ubiquitous Metazoan Superfamily: Evolution of Functional Features and Structural Complexity: http://www.ncbi.nlm.nih.gov/pubmed/14963095.

305 Motion to Form a Quorum: http://www.ncbi.nlm.nih.gov/pubmed/12855801

306 Programmed cell death in bacteria and implications for antibiotic therapy: http://www.ncbi.nlm.nih.gov/pubmed/23684151

307 “Persisters”: Survival at the Cellular Level: http://www.ncbi.nlm.nih.gov/pubmed/21829345

308 Evolution of cooperation among tumor cells: http://www.ncbi.nlm.nih.gov/pubmed/16938860

309 Safeguards for cell cooperation in mouse embryogenesis shown by genome-wide cheater screen:http://www.ncbi.nlm.nih.gov/pubmed/24030493

Contributors

  • Michael W. Klymkowsky (University of Colorado Boulder) and Melanie M. Cooper (Michigan State University) with significant contributions by Emina Begovic & some editorial assistance of Rebecca Klymkowsky.