Ruma Banerjee Introduction to the Thematic Minireview Series on Enzyme Evolution

Minireviews:
Introduction to the Thematic Minireview
Series on Enzyme Evolution
Ruma Banerjee
J. Biol. Chem. 2014, 289:30196-30197.
doi: 10.1074/jbc.R114.610766 originally published online September 10, 2014
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MINIREVIEW PROLOGUE
THE JOURNAL OF BIOLOGICAL CHEMISTRY VOL. 289, NO. 44, pp. 30196 –30197, October 31, 2014
© 2014 by The American Society for Biochemistry and Molecular Biology, Inc. Published in the U.S.A.
Introduction to the Thematic Minireview Series on Enzyme
Evolution*
Published, JBC Papers in Press, September 10, 2014, DOI 10.1074/jbc.R114.610766
Ruma Banerjee1
From the Department of Biological Chemistry, University of Michigan Medical School, Ann Arbor, Michigan 48109-0600
How did enzymes evolve to speed up reactions moving them
from geological to biological timescales that required lowering
of formidable kinetic barriers? In the first article in the series
(1), Wolfenden explains that Arrhenius analyses indicate that
the temperature sensitivity of a reaction increases with its sluggishness to an extent not previously suspected. A corollary is
that the emergence of life at high temperatures would have
provided substantial acceleration of chemical reactions, hastening evolution. Also, if primordial catalysts, like modern
enzymes, operated primarily by decreasing the enthalpic barrier (⌬H‡) rather than by increasing T⌬S‡, a selective advantage
would have been conferred as the earth cooled. Enhanced
mutation rates at high temperatures would have further accelerated the pace of evolution during earth’s early history.
In the second article in the series (2), Klinman and Kohen
discuss the role of protein dynamics on hydride transfer catalysis. The prototype selected to illustrate the principle of coevolution of catalytically important amino acid networks is dihydrofolate reductase, and the prototype selected to illustrate the
principle of preserving catalytic fitness during adaptation to
different environmental niches is alcohol dehydrogenase. Residues in coevolving networks in dihydrofolate reductase identified by computational and genetic approaches, and evaluated
by biochemical approaches, can couple protein dynamics to the
reaction coordinate, suggesting that evolutionary pressure has
played a role in preserving conformational fluctuations important for catalyzing the chemical step. Similarly, adaptation of
thermophilic alcohol dehydrogenase to cooler climes in psy-
* This work was supported, in whole or in part, by National Institutes of Health
1
Grants DK45776, HL58984, and GM112455 (to R. B.)
To whom correspondence should be addressed: 4220C MSRB III, 1150 W.
Medical Center Dr., University of Michigan, Ann Arbor, MI 48109-0600. Tel.:
734-615-5238; E-mail: rbanerje@umich.edu.
30196 JOURNAL OF BIOLOGICAL CHEMISTRY
chrophilic and mesophilic organisms appears to have been
accompanied by preservation of an optimal conformational
landscape for catalyzing hydride transfer.
In the third article in the series (3), Carter discusses Urzymes,
models of primordial catalysts constructed from the invariant
cores of enzyme superfamilies. The class I and II aminoacyl
tRNA synthetase Urzymes tested the hypothesis that ancestral
members of each class were derived from opposite strands of
the same gene. Significant catalytic activity and reduced specificity make these Urzymes novel experimental systems for
understanding the evolution of modern enzymes and for examining how the addition of modules might influence catalytic and
allosteric functionalities related to catalytic efficiency and
specificity.
In the fourth article in the series (4), Brown and Babbitt
describe insights derived from large scale studies on sequencestructure relationships into the evolution of enzyme superfamilies. The review examines how a relatively small number of
architectural scaffolds have been repurposed to expand the repertoire of catalytic functions across diverse superfamilies.
The review also discusses the challenges associated with making functional assignments because the number of newly
sequenced family members grows at an ever-increasing pace
and because a significant proportion of these sequences encode
domains of unknown function. The authors suggest that protein similarity network analysis will be an important approach
for generating hypotheses about structure-function relationships, which can be tested experimentally and perhaps even
exploited to guide natural evolution of new functions in a laboratory setting.
In the fifth article in the series (5), Dunaway-Mariano, Allen,
and coworkers discuss catalytic promiscuity and substrate
ambiguity as engines of evolutionary innovation. The potential advantages of substrate ambiguity, estimated to be a
property of some 37% of metabolic enzymes in Escherichia
coli, include disposing antimetabolites and xenobiotics,
engendering redundancy, and balancing metabolite pools.
Using as examples the phosphatases in the haloalkanoate
dehalogenase and thioesterases in the hotdog fold superfamilies, the authors illustrate how promiscuity can be
achieved via domain insertion or by varying the volume and
accessibility of the active site pocket.
This collection of reviews is a sequel to an earlier set of minireviews on Enzyme Evolution in the Post-genomic Era (6).
REFERENCES
1. Wolfenden, R. (2014) Massive thermal acceleration of the emergence of
primordial chemistry, the evolution of enzymes, and the tempo of spontaneous mutation. J. Biol. Chem. 289, 30198 –30204
VOLUME 289 • NUMBER 44 • OCTOBER 31, 2014
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In this thematic minireview series, the JBC presents five provocative articles on Enzyme Evolution. The reviews discuss
stimulating concepts that include the emergence of primordial
catalysts at temperatures that were considerably warmer than
present day ones and the impact of the cooling environment on
the evolution of catalytic fitness and the preservation of catalysis-promoting conformational dynamics. They also discuss the
use of Urzymes or invariant modules in enzyme superfamilies as
paradigms for understanding the evolution of catalytic efficiency and specificity, the use of bioinformatics approaches to
understand the roles of substrate ambiguity and catalytic promiscuity as drivers of evolution, and the challenges associated with
assigning catalytic function as the number of superfamily members grows rapidly.
MINIREVIEW: Thematic Minireview Series on Enzyme Evolution
2. Klinman, J. P., and Kohen, A. (2014) Evolutionary aspects of enzyme dynamics. J. Biol. Chem. 289, 30205–30212
3. Carter, C. W. (2014) Urzymology: experimental access to a key transition
in the appearance of enzymes. J. Biol. Chem. 289, 30213–30220
4. Brown, S. D., and Babbitt, P. C. (2014) New insights about enzyme evolution from large-scale studies of sequence and structure relationships.
J. Biol. Chem. 289, 30221–30228
5. Pandya, C., Farelli, J. D., Dunaway-Mariano, D., and Allen, K. N. (2014)
Enzyme promiscuity: engine of evolutionary innovation. J. Biol. Chem.
289, 30229 –30236
6. Allewell, N. (2012) Thematic minireview series on enzyme evolution in
the post-genomic era. J. Biol. Chem. 287, 1–2
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OCTOBER 31, 2014 • VOLUME 289 • NUMBER 44
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