Mechanism and dynamics of fatty acid photodecarboxylase

Sorigué, D.; Hadjidemetriou, K.; Blangy, S.; Gotthard, G.; Bonvalet, A.; Coquelle, N.; Samire, P.; Aleksandrov, A.; Antonucci, L.; Benachir, A.; Boutet, S.; Byrdin, M.; Cammarata, M.; Carbajo, S.; Cuiné, S.; Doak, R. B.; Foucar, L.; Gorel, A.; Grünbein, M.; Hartmann, E.; Hienerwadel, R.; Hilpert, M.; Kloos, M.; Lane, T. J.; Légeret, B.; Legrand, P.; Li-Beisson, Y.; Moulin, S. Y.; Nurizzo, D.; Peltier, G.; Schirò, G.; Shoeman, R. L.; Sliwa, M.; Solinas, X.; Zhuang, B.; Barends, T. M.; Colletier, J. -P.; Joffre, M.; Royant, A.; Berthomieu, C.; Weik, M.; Domratcheva, T.; Brettel, K.; Vos, M. H.; Schlichting, I.; Arnoux, P.; Müller, P.; Beisson, F.

doi:10.1126/science.abd5687

Title: Mechanism and dynamics of fatty acid photodecarboxylase

Journal Article · Fri Apr 09 00:00:00 EDT 2021 · Science

DOI:https://doi.org/10.1126/science.abd5687· OSTI ID:1810562

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Aix-Marseille Univ., Saint-Paul-lez-Durance, (France)
Univ. Grenoble Alpes (France)
European Synchrotron Radiation Facility, Grenoble (France)
Ecole Polytechnique, Palaiseau (France)
Inst. Laue Langevin, Grenoble (France)
Aix-Marseille Univ., Saint-Paul-lez-Durance, (France); Univ. Paris-Saclay, Gif-sur-Yvette (France)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Univ. of Rennes (France); European Synchrotron Radiation Facility (ESRF), Grenoble (France)
Max-Planck-Institut für medizinische Forschung, Heidelberg (Germany)
Max-Planck-Institut für medizinische Forschung, Heidelberg (Germany); Sample Environment and Characterization European XFEL, Schenefeld (Germany)
Synchrotron SOLEIL, Gif-sur-Yvette (France)
Univ. Lille (France)
Ecole Polytechnique, Palaiseau (France); Univ. Paris-Saclay, Gif-sur-Yvette (France)
Univ. Grenoble Alpes (France); European Synchrotron Radiation Facility, Grenoble (France)
Max-Planck-Institut für medizinische Forschung, Heidelberg (Germany); Lomonosov Moscow States Univ. (Russia)
Univ. Paris-Saclay, Gif-sur-Yvette (France)

Photoenzymes are rare biocatalysts driven by absorption of a photon at each catalytic cycle; they inspire development of artificial photoenzymes with valuable activities. Fatty acid photodecarboxylase (FAP) is a natural photoenzyme that has potential applications in the bio-based production of hydrocarbons, yet its mechanism is far from fully understood. RATIONALE To elucidate the mechanism of FAP, we studied the wild-type (WT) enzyme from Chlorella variabilis (CvFAP) and variants with altered active-site residues using a wealth of techniques, including static and time-resolved crystallography and spectroscopy, as well as biochemical and computational approaches. RESULTS A 1.8-Å-resolution CvFAP x-ray crystal structure revealed a dense hydrogen-bonding network positioning the fatty acid carboxyl group in the vicinity of the flavin adenine dinucleotide (FAD) cofactor. Structures solved from free electron laser and low-dose synchrotron x-ray crystal data further highlighted an unusual bent shape of the oxidized flavin chromophore, and showed that the bending angle (14°) did not change upon photon absorption (step 1) or throughout the photocycle. Calculations showed that bending substantially affected the energy levels of the flavin. Structural and spectroscopic analysis of WT and mutant proteins targeting two conserved active-site residues, R451 and C432, demonstrated that both residues were crucial for proper positioning of the substrate and water molecules and for oxidation of the fatty acid carboxylate by ¹FAD* (~300 ps in WT FAP) to form FAD^∙– (step 2). Time-resolved infrared spectroscopy demonstrated that decarboxylation occured quasi-instantaneously upon this forward electron transfer, consistent with barrierless bond cleavage predicted by quantum chemistry calculations and with snapshots obtained by time-resolved crystallography. Transient absorption spectroscopy in H₂O and D₂O buffers indicated that back electron transfer from FAD^∙– was coupled to and limited by transfer of an exchangeable proton or hydrogen atom (step 3). Unexpectedly, concomitant with FAD^∙– reoxidation (to a red-shifted form FAD_RS) in 100 ns, most of the CO₂ product was converted, most likely into bicarbonate (as inferred from FTIR spectra of the cryotrapped FAD_RS intermediate). Calculations indicated that this catalytic transformation involved an active-site water molecule. Cryo-Fourier transform infrared spectroscopy studies suggested that bicarbonate formation (step 4) was preceded by deprotonation of an arginine residue (step 3). At room temperature, the remaining CO₂ left the protein in 1.5 μs (step 4'). The observation of residual electron density close to C432 in electron density maps derived from time-resolved and cryocrystallography data suggests that this residue may play a role in stabilizing CO₂ and/or bicarbonate. Three routes for alkane formation were identified by quantum chemistry calculations; the one shown in the figure is favored by the ensemble of experimental data. CONCLUSION Finally, we provide a detailed and comprehensive characterization of light-driven hydrocarbon formation by FAP, which uses a remarkably complex mechanism including unique catalytic steps. We anticipate that our results will help to expand the green chemistry toolkit.

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515; P41GM103393

OSTI ID:: 1810562

Journal Information:: Science, Vol. 372, Issue 6538; ISSN 0036-8075

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

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