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Survival of the simplest in microbial evolution.

ABSTRACT: The evolution of microbial and viral organisms often generates clonal interference, a mode of competition between genetic clades within a population. Here we show how interference impacts systems biology by constraining genetic and phenotypic complexity. Our analysis uses biophysically grounded evolutionary models for molecular phenotypes, such as fold stability and enzymatic activity of genes. We find a generic mode of phenotypic interference that couples the function of individual genes and the population's global evolutionary dynamics. Biological implications of phenotypic interference include rapid collateral system degradation in adaptation experiments and long-term selection against genome complexity: each additional gene carries a cost proportional to the total number of genes. Recombination above a threshold rate can eliminate this cost, which establishes a universal, biophysically grounded scenario for the evolution of sex. In a broader context, our analysis suggests that the systems biology of microbes is strongly intertwined with their mode of evolution.

SUBMITTER: Held T

PROVIDER: S-EPMC6554311 | biostudies-other | 2019 Jun

REPOSITORIES: biostudies-other

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Survival of the simplest in microbial evolution.

Held Torsten T Klemmer Daniel D Lässig Michael M

Nature communications 20190606 1

The evolution of microbial and viral organisms often generates clonal interference, a mode of competition between genetic clades within a population. Here we show how interference impacts systems biology by constraining genetic and phenotypic complexity. Our analysis uses biophysically grounded evolutionary models for molecular phenotypes, such as fold stability and enzymatic activity of genes. We find a generic mode of phenotypic interference that couples the function of individual genes and th ...[more]

PMID: 31171781

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Project description:1. Evolutionary changes in the structure of an enzyme that provide an increase in its K(m) value are considered. Provided that K(m) increases as a result of increases in the forward rate constants of the catalysis relative to the reverse rate constants, the enzyme catalyses the conversion of a fixed concentration of its substrate more rapidly when its structure provides that K(m)>[S] than when K(m)<[S]. 2. Catalytic efficiency of enzymes is discussed in terms of the simplest plausible model, the Haldane [(1930) Enzymes, Longmans, London] reversible three-step model: [Formula: see text] The rate equation for the forward reaction of this model (formation of P) may be written in the simple form: [Formula: see text] K(eq.) is the equilibrium constant (=[P](eq.)/[S](eq.)), and k(cat.)=V/[E](T), where [E](T) is the total enzyme concentration. 3. To assess the effectiveness of an enzyme, it is necessary only to determine the extent to which the constraints of a particular kinetic mechanism permit v(2) (v when K(m)>>[S]) to approach v(d) (the diffusion-limited rate). 4. The value of the optimal rate of catalysis (v(opt.), the maximal value of v(2)) is dictated by the equilibrium constant for the reaction, K(eq.); v(2)=v(d)/a, where [Formula: see text] when k(+1) is assumed equal to k(-3), and v(opt.)=v(d)/a(min.). When K(eq.)>/=1, it is necessary that k(+2)>>k(-1) for a to take its minimum value, a(min.); when K(eq.)<<1, it is necessary only that k(+2)>>K(eq.).k(-1), i.e. a can equal a(min.) even if k(+2)<k(-1). When K(eq.)>>1, v(opt.)=v(d); when K(eq.)=1, v(opt.)=v(d)/2, and when K(eq.)<<1, v(opt.)=K(eq.).v(d). 5. The analysis, together with predicted effects of evolutionary pressure, suggests that in practice the rates of the fastest enzyme-catalysed freely reversible reactions might be expected to be lower than the value of k(+1)[E](T)[S] by about an order of magnitude, particularly if K(eq.)<1. 6. The existing literature suggests that, in general, appropriate values of K(m) have evolved for the provision of high rates of catalysis but that many values of k(cat.) are not large enough to provide optimal rates of catalysis unless the value of k(+1)in vivo is lower than its value in free solution.

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Survival of the simplest in microbial evolution.

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Survival of the simplest in microbial evolution.

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