- Adaptive mutation
Evolutionary theory describes that mutagenesis occurs randomly, regardless of the utility of a genetic mutation to the organism. If it is beneficial or neutral, the organism will survive to reproduce and pass on the mutation. However, molecular biologist John Cairns has proposed that "when populations of single cells are subject to certain forms of strong selection pressure, variants emerge bearing changes in DNA sequence that bring about an appropriate change in phenotype." This suggests that there exists a particular physiological pathway that responds to a specific selective pressure to produce a mutation conferring the correct phenotype that will alleviate this pressure.
Such evidence was first produced by Cairns et al. in 1988. The original experiments involved a strain of E. coli that has a frameshift mutation in the lactose (LacZ) operon, inactivating the proteins needed for utilization of this sugar. The bacteria were then spread on an agar medium in which the only carbon source was lactose. This meant that a cell could grow only if a second mutation occurred in the lactose operon, reversing the effects of the mutation and therefore allowing the enzymes to be synthesized. Mutations with this effect appeared to occur significantly more frequently than expected, and at a rate that was greater than mutations in other parts of the genomes of these E. coli cells.
There is however a serious flaw in this experiment, as Cairns does not distinguish between selection and detection of LacZ revertants. If he is testing to see if the presence of lactose as the selective agent causes mutations that confer the ability to eat lactose, then he should not detect this mutation with lactose present (i.e. looking for cells that grow with lactose as the only carbon source.) He will never know, in this case, if cells have acquired this ability without the presence of lactose - a possibility that his theory cannot reconcile. In fact, the acknowledgment of fundamental limitations on our ability to separate between mutation selection and detection has lead Vasily Ogryzko to suggest that for the proper description of the Cairns' experiments, the formalism of quantum theory would be required, with the phenomenon of adaptive mutations naturally following from such an approach.
Furthermore, when looking for additional mutations only in cells that have already reverted to Lac+, it would certainly be the case that other, unnecessary mutations would be less numerous - especially since most are deleterious. However, Barry Hall has provided evidence that the mutation rate in bacteria under environmental stress increases across the board, most likely indiscriminately. When testing for tryptophan revertants (trp− → trp+, i.e. cells that have regained the ability to make tryptophan), he found that occurrence of auxotrophic mutants increased as well. Tryptophan revertants, which had been exposed to the environmental stress of lacking the amino acid, saw a 1.8% rate of auxotrophy for any other amino acid. When testing for auxotrophy in cells in non-stressed colonies, he found a rate below 0.01%. From these data, Hall hypothesized that cells under stress enter a "hyper-mutable state," where cells increase their general rate of mutation, increasing the overall probability that they will acquire a mutation conferring a phenotype that aids their survival. Hall later determined that his mutants were the result of transposon activity, and concluded that his results were in fact about transposon biology, and not mutagenesis.
Similar results have been observed in other experiments. These experiments suggested that mutations in bacteria are influenced by the selective pressures that the bacteria are placed under.
Another explanation stems from a similarity in cellular mechanisms underlying the acquisition of adaptive mutations in the bacterial stationary phase cells and in the mammalian tumor cells. In both cases the adaptive mutations arise in response to a sustained stress environment and are promoted by high rate of genomic mutations. Cellular processes leading to the mutations are also surprisingly similar between both organisms and include silencing of differentiation, cellular senescence, programmed cell death, and DNA repair on the one hand, and activation of the error-prone replication and transposons on the other. The similarity suggests that the adaptive mutations may be an output of activation in the stressed cell of a special survival strategy for quick adaptation to the stressful environment. This strategy that is also referred as the mutator phenotype is an alternative to other stress-induced strategies, such as senescence and programmed cell death, activated in majority of stressed cells. Continuing stress-induced proliferative and survival signaling may be an important prerequisite for epigenetic reprogramming of some cells to activate the mutator phenotype.
- Genomes, T.A Brown, Second Edition ISBN 1-85996-029-4, Chapter 14.1.3 Hypermutation and the possibility of programmed mutations
- The Origin of Mutants, Cairns et al. 1988 Nature. 1988 Sep 8;335(6186):142-5.
- Evolving responsively: adaptive mutation, Rosenberg, Nature Reviews: Genetics: 2: 504-515 (2001)
- Human cancers express a mutator phenotype. Bielas JH, Loeb KR, Rubin BP, True LD, Loeb LA.: Proc Natl Acad Sci U S A.: 103(48): 18238-42 (2006)
- Mutation as a stress response and the regulation of evolvability. Galhardo RS, Hastings PJ, Rosenberg SM.: Crit Rev Biochem Mol Biol.:42(5):399-435 (2007)
- Bacterial Stationary-State Mutagenesis and Mammalian Tumorigenesis as Stress-Induced Cellular Adaptations and the Role of Epigenetics
- Adaptive Amplification and Point Mutation Are Independent Mechanisms: Evidence for Various Stress-Inducible Mutation Mechanisms
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