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MBE Advance Access originally published online on September 19, 2007
Molecular Biology and Evolution 2007 24(12):2716-2722; doi:10.1093/molbev/msm204
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Multicopy Suppression Underpins Metabolic Evolvability

Wayne M. Patrick1, Erik M. Quandt, Dan B. Swartzlander and Ichiro Matsumura

Department of Biochemistry, Center for Fundamental and Applied Molecular Evolution, Emory University, Atlanta, Georgia

E-mail: imatsum{at}emory.edu.

Accepted for publication September 16, 2007.

Our understanding of the origins of new metabolic functions is based upon anecdotal genetic and biochemical evidence. Some auxotrophies can be suppressed by overexpressing substrate-ambiguous enzymes (i.e., those that catalyze the same chemical transformation on different substrates). Other enzymes exhibit weak but detectable catalytic promiscuity in vitro (i.e., they catalyze different transformations on similar substrates). Cells adapt to novel environments through the evolution of these secondary activities, but neither their chemical natures nor their frequencies of occurrence have been characterized en bloc. Here, we systematically identified multifunctional genes within the Escherichia coli genome. We screened 104 single-gene knockout strains and discovered that many (20%) of these auxotrophs were rescued by the overexpression of at least one noncognate E. coli gene. The deleted gene and its suppressor were generally unrelated, suggesting that promiscuity is a product of contingency. This genome-wide survey demonstrates that multifunctional genes are common and illustrates the mechanistic diversity by which their products enhance metabolic robustness and evolvability.

Key Words: catalytic promiscuity • directed evolution • multicopy suppression • substrate ambiguity

1 Present address: Institute of Molecular Biosciences, Massey University, Auckland 0745, New Zealand.

Laura Katz, Associate Editor


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