Changes in an enzyme ensemble during catalysis observed by high-resolution XFEL crystallography

Smith, Nathan; Dasgupta, Medhanjali; Wych, David C.; Dolamore, Cole; Sierra, Raymond G.; Lisova, Stella; Marchany-Rivera, Darya; Cohen, Aina E.; Boutet, Sébastien; Hunter, Mark S.; Kupitz, Christopher; Poitevin, Frédéric; Moss III, Frank R.; Mittan-Moreau, David W.; Brewster, Aaron S.; Sauter, Nicholas K.; Young, Iris D.; Wolff, Alexander M.; Tiwari, Virendra K.; Kumar, Nivesh; Berkowitz, David B.; Hadt, Ryan G.; Thompson, Michael C.; Follmer, Alec H.; Wall, Michael E.; Wilson, Mark A.

doi:10.1126/sciadv.adk7201

Changes in an enzyme ensemble during catalysis observed by high-resolution XFEL crystallography

Journal Article · Wed Mar 27 00:00:00 EDT 2024 · Science Advances

DOI:https://doi.org/10.1126/sciadv.adk7201· OSTI ID:2396810

^[1]; Dasgupta, Medhanjali ^[2]; Wych, David C. ^[3]; Dolamore, Cole ^[2]; ^[4]; Lisova, Stella ^[4]; ^[4]; ^[4]; ^[4]; Hunter, Mark S. ^[4]; ^[4]; ^[4]; ^[4]; ^[5]; ^[5]; ^[5]; ^[5]; ^[6]; Tiwari, Virendra K. ^[2]; Kumar, Nivesh ^[2] more »

Univ. of Nebraska, Lincoln, NE (United States); SLAC
Univ. of Nebraska, Lincoln, NE (United States)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Univ. of California, Merced, CA (United States)
California Institute of Technology (CalTech), Pasadena, CA (United States)
Univ. of California, Irvine, CA (United States)

Enzymes populate ensembles of structures necessary for catalysis that are difficult to experimentally characterize. We use time-resolved mix-and-inject serial crystallography at an x-ray free electron laser to observe catalysis in a designed mutant isocyanide hydratase (ICH) enzyme that enhances sampling of important minor conformations. The active site exists in a mixture of conformations, and formation of the thioimidate intermediate selects for catalytically competent substates. The influence of cysteine ionization on the ICH ensemble is validated by determining structures of the enzyme at multiple pH values. Large molecular dynamics simulations in crystallo and time-resolved electron density maps show that Asp¹⁷ ionizes during catalysis and causes conformational changes that propagate across the dimer, permitting water to enter the active site for intermediate hydrolysis. ICH exhibits a tight coupling between ionization of active site residues and catalysis-activated protein motions, exemplifying a mechanism of electrostatic control of enzyme dynamics.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE National Nuclear Security Administration (NNSA); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 2396810

Alternate ID(s):: OSTI ID: 2426883

Journal Information:: Science Advances, Journal Name: Science Advances Journal Issue: 13 Vol. 10; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

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Mix-and-inject XFEL crystallography reveals gated conformational dynamics during enzyme catalysis

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Changes in an enzyme ensemble during catalysis observed by high-resolution XFEL crystallography

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