Differential catalytic promiscuity of the alkaline phosphatase superfamily bimetallo core reveals mechanistic features underlying enzyme evolution

Sunden, Fanny; AlSadhan, Ishraq; Lyubimov, Artem; Doukov, Tzanko; Swan, Jeffrey; Herschlag, Daniel

doi:10.1074/jbc.m117.788240

Title: Differential catalytic promiscuity of the alkaline phosphatase superfamily bimetallo core reveals mechanistic features underlying enzyme evolution

Journal Article · Wed Oct 25 00:00:00 EDT 2017 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.m117.788240· OSTI ID:1425345

Sunden, Fanny ^[1]; AlSadhan, Ishraq ^[1]; Lyubimov, Artem ^[2]; Doukov, Tzanko ^[3]; Swan, Jeffrey ^[1]; Herschlag, Daniel ^[4]

Stanford Univ., CA (United States). Dept. of Biochemistry, Beckman Center
Stanford Univ., CA (United States). Dept. of Molecular and Cellular Physiology, Dept. of Neurology and Neurological Science, Structural Biology, and Photon Science, and Howard Hughes Medical Inst.
SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL), Macromolecular Crystallographic Group
Stanford Univ., CA (United States). Dept. of Biochemistry, Dept. of Neurology and Neurological Science, and Beckman Center; Stanford Univ., CA (United States). Stanford Chemistry, Engineering, and Medicine for Human Health (ChEM-H)

Members of enzyme superfamilies specialize in different reactions but often exhibit catalytic promiscuity for one another's reactions, consistent with catalytic promiscuity as an important driver in the evolution of new enzymes. Wanting to understand how catalytic promiscuity and other factors may influence evolution across a superfamily, we turned to the well-studied alkaline phosphatase (AP) superfamily, comparing three of its members, two evolutionarily distinct phosphatases and a phosphodiesterase. Here, we mutated distinguishing active-site residues to generate enzymes that had a common Zn²⁺ bimetallo core but little sequence similarity and different auxiliary domains. We then tested the catalytic capabilities of these pruned enzymes with a series of substrates. A substantial rate enhancement of ~1011-fold for both phosphate mono- and diester hydrolysis by each enzyme indicated that the Zn²⁺ bimetallo core is an effective mono/di-esterase generalist and that the bimetallo cores were not evolutionarily tuned to prefer their cognate reactions. In contrast, our pruned enzymes were ineffective sulfatases, and this limited promiscuity may have provided a driving force for founding the distinct one-metal-ion branch that contains all known AP superfamily sulfatases. Finally, our pruned enzymes exhibited 10⁷–10⁸-fold phosphotriesterase rate enhancements, despite absence of such enzymes within the AP superfamily. We speculate that the superfamily active-site architecture involved in nucleophile positioning prevents accommodation of the additional triester substituent. Overall, we suggest that catalytic promiscuity, and the ease or difficulty of remodeling and building onto existing protein scaffolds, have greatly influenced the course of enzyme evolution. Uncovering principles and properties of enzyme function, promiscuity, and repurposing provides lessons for engineering new enzymes.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515; GM64798; GM049243

OSTI ID:: 1425345

Journal Information:: Journal of Biological Chemistry, Vol. 292, Issue 51; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 18 works

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Title: Differential catalytic promiscuity of the alkaline phosphatase superfamily bimetallo core reveals mechanistic features underlying enzyme evolution

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