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A Biochemical Mechanism for Nonrandom Mutations and Evolution University of Montana ScholarWorks at University of Montana Biological Sciences Faculty Publications Biological Sciences 6-2000 A Biochemical Mechanism for Nonrandom Mutations and Evolution Barbara E. Wright University of Montana - Missoula, [email protected] Follow this and additional works at: https://scholarworks.umt.edu/biosci_pubs Part of the Biology Commons Let us know how access to this document benefits ou.y Recommended Citation Wright, Barbara E., "A Biochemical Mechanism for Nonrandom Mutations and Evolution" (2000). Biological Sciences Faculty Publications. 263. https://scholarworks.umt.edu/biosci_pubs/263 This Article is brought to you for free and open access by the Biological Sciences at ScholarWorks at University of Montana. It has been accepted for inclusion in Biological Sciences Faculty Publications by an authorized administrator of ScholarWorks at University of Montana. For more information, please contact [email protected]. JOURNAL OF BACTERIOLOGY, June 2000, p. 2993–3001 Vol. 182, No. 11 0021-9193/00/$04.00ϩ0 Copyright © 2000, American Society for Microbiology. All Rights Reserved. MINIREVIEW A Biochemical Mechanism for Nonrandom Mutations and Evolution BARBARA E. WRIGHT* Division of Biological Sciences, The University of Montana, Missoula, Montana Downloaded from As this minireview is concerned with the importance of the nario begins with the starvation of a self-replicating unit for its environment in directing evolution, it is appropriate to remem- precursor, metabolite A, utilized by enzyme 1 encoded by gene ber that Lamarck was the first to clearly articulate a consistent 1. When metabolite A is depleted, a mutation in a copy of gene theory of gradual evolution from the simplest of species to the 1 gives rise to gene 2 and allows enzyme 2 to use metabolite B most complex, culminating in the origin of mankind (71). He by converting it to metabolite A. Then metabolite B is de- published his remarkable and courageous theory in 1809, the pleted, obtained from metabolite C, and so on, as an increas- year of Darwin’s birth. Unfortunately, Lamarck’s major con- ingly complex biochemical pathway evolves. In fact, there are http://jb.asm.org/ tributions have been overshadowed by his views on the inher- examples in which a similar series of events can actually be itance of acquired characters. In fact, Darwin shared some of observed in the laboratory, for example, involving enzymes these same views, and even Weismann (106), the father of that are “borrowed” from existing pathways, via regulatory neo-Darwinism, decided late in his career that directed variation mutations, to establish new pathways (75). must be invoked to understand some phenomena, as random The starvation conditions that may initiate a series of events variation and selection alone are not a sufficient explanation such as those described above target the most relevant genes (71). This minireview will describe mechanisms of mutation for increased rates of transcription, which in turn increase rates that are not random and can accelerate the process of evolu- of mutation (111). Transcriptional activation can result from on May 29, 2013 by UNIV OF MONTANA tion in specific directions. The existence of such mechanisms the addition of a substrate or from the removal of a repressor has been predicted by mathematicians (6) who argue that, if or an end product inhibitor. The latter mechanism, called every mutation were really random and had to be tested derepression, occurs in response to starvation for an essential against the environment for selection or rejection, there would substrate or for an end product that represses its own synthesis not have been enough time to evolve the extremely complex by feedback inhibition. Since evolution usually occurs in re- biochemical networks and regulatory mechanisms found in sponse to stress (41), transcriptional activation via derepres- organisms today. Dobzhansky (21) expressed similar views by sion is the main focus of this minireview. stating “The most serious objection to the modern theory of evolution is that since mutations occur by ‘chance’ and are undirected, it is difficult to see how mutation and selection can EVOLUTION OF BIOCHEMICAL PATHWAYS add up to the formation of such beautifully balanced organs as, A number of events initiated by carbon source starvation can for example, the human eye.” facilitate the evolution of a new catabolic pathway. Under The most primitive kinds of cells, called progenotes by these circumstances, cells with gene duplication and higher Woese (108), were undoubtedly very simple biochemically with enzyme levels have a selective advantage (87, 95). In some only a few central anabolic and catabolic pathways. Wa¨chter- systems, duplicated segments are specifically subject to higher ha¨user (103) theorizes that the earliest metabolic pathway was mutation rates (93), providing ideal and expendable material a reductive citric acid cycle by which carbon fixation occurred for mutations representing minor modifications of existing (64). At that point in time, some four billion years ago, how did genes (58). These new genes can encode modified enzymes the additional, more complex metabolic pathways found in catalyzing reactions closely related and/or complementary to even the simplest prokaryotes evolve? For that matter, how are those in existence (56). An additional consequence of starva- they evolving today? As pointed out by Oparin (79), it is in- tion is the removal of feedback controls, resulting in the dere- conceivable that a self-reproducing unit as complicated as a pression of genes previously inhibited by the now absent me- nucleoprotein could suddenly arise by chance; a period of tabolite. Increased rates of mutation in these derepressed evolution through the natural selection of organic substances genes increase the probability of creating a new gene-enzyme of ever-increasing degrees of complexity must intervene. system. A number of examples exist in which derepression of a Horowitz (40) suggests a plausible scheme by which biosyn- gene has enabled an enzyme to use a new substrate. For ex- thetic pathways can evolve from the successive depletion and ample, altros-galactoside can be used by ␤-galactosidase after interconversion of related metabolites in a primitive environ- it is derepressed (53); other examples are ␤-glycerolphosphate ment, as the rich supply of organic molecules is consumed by a via alkaline phosphatase (100), putrescine via diamine-␣-keto- burgeoning population of heterotrophs. Thus, a possible sce- glutarate transaminase (44), and D-mannitol via D-arabitol de- hydrogenase (55). An excellent example of the evolution of biochemical path- * Mailing address: Division of Biological Sciences, The University of ways involves the modification of two genes to serve the new Montana, Missoula, MT 59812. Phone: (406) 243-6676. Fax: (406) demands imposed by carbon source starvation (56, 112). Rib- 243-4184. E-mail: [email protected]. itol dehydrogenase, which is induced by ribitol in wild-type 2993 2994 MINIREVIEW J. BACTERIOL. TABLE 1. Evolution of a catabolic pathwaya ities by coordinating these activities with the presence or ab- sence of nutrients in the environment. High mutation rates in Generation Km (mM) [14C]xylitol uptake Strain derepressed genes prepare cells to respond rapidly to new time (h) Xylitol Ribitol (cpm) challenges should the stress become more severe. As will be- b come apparent, genetic derepression may be the only mecha- X 4.1 0 3 104 X1c 4.1 290 3 104 nism by which particular environmental conditions of stress X2 1.7 120 2 185 target specific regions of the genome for higher mutation rates X3 0.9 130 2 685 (hypermutation). Although this direct avenue for increasing variability is probably not available to multicellular organisms a Data taken from reference 112. in which germ cells and somatic cells are separated, the dere- b Wild-type strain with inducible ribitol dehydrogenase. c Mutant strain with constitutive ribitol dehydrogenase. pression of biosynthetic pathways is essential to increased lon- gevity in mammals subjected to caloric restriction (54), and amino acid limitation in rats can also induce gene expression (9). Downloaded from Enterobacter arogenes (strain X in Table 1), is unable to use xylitol. Starvation for ribitol in the presence of xylitol results in a mutation to strain X1, in which ribitol dehydrogenase is MECHANISMS OF MUTATIONS VERSUS constitutive and able to use xylitol, which is a poor substrate for MECHANISMS OF EVOLUTION the enzyme but not its inducer. By repeated growth cycling on In a scientific context, the word spontaneous is meaningless. xylitol, derivative mutants X2 and X3 are obtained with lower Every event is preceded by, and dependent upon, innumerable Km for xylitol. The enhanced uptake of labeled xylitol in the known and unknown prior events and circumstances. There- final mutant, X3, is due to the acquisition of a constitutively fore, the work background will be used when referring to the expressed active transport system for xylitol, originating from many environmental conditions, cellular events, and repair http://jb.asm.org/ the modification of an inducible transport system for D-arabi- processes that affect mutation rates in nature. Although back- tol. Thus, two preexistent gene-enzyme systems evolve to ini- ground mutations, such as deamination, alkylation, and depuri- tiate a new catabolic pathway in response to the stress of nation, occur with low frequencies, they have characteristic,
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