Fatty-acid oxygenation by fungal peroxygenases: From computational simulations to preparative regio- and stereoselective epoxidation

Epoxidation of unsaturated fatty acids by unspecific peroxygenases (UPOs) of the best-known long-UPO subfamily, including the Agrocybe aegerita (AaeUPO) and Coprinopsis cinerea enzymes, is reported here. To understand the different oxygenation patterns by members of the long-UPO and short-UPO subfam...

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Detalles Bibliográficos
Autores: Municoy Terol, Martí, González Benjumea, Alejandro, Carro Aramburu, Juan, Aranda Oliden, Carmen, Linde López, Dolores, Renau Mínguez, Chantal, Ullrich, René, Hofrichter, Martin, Guallar Tasies, Victor, Gutiérrez Suárez, Ana, Martínez Ferrer, Angel Tomás
Tipo de recurso: artículo
Fecha de publicación:2020
País:España
Institución:Universitat Politècnica de Catalunya (UPC)
Repositorio:UPCommons. Portal del coneixement obert de la UPC
Idioma:inglés
OAI Identifier:oai:upcommons.upc.edu:2117/345962
Acceso en línea:https://hdl.handle.net/2117/345962
https://dx.doi.org/10.1021/acscatal.0c03165
Access Level:acceso abierto
Palabra clave:Monte Carlo method
Chemistry, Analytic
Computational chemistry
Unsaturated fatty acids
Oxygenation patterns
Regioselective epoxidation
Stereoselective epoxidation
Monte Carlo molecular simulations
Adaptive-PELE
Fungal unspecific peroxygenases
Montecarlo, Mètode de
Química analítica
Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica
Àrees temàtiques de la UPC::Física
Descripción
Sumario:Epoxidation of unsaturated fatty acids by unspecific peroxygenases (UPOs) of the best-known long-UPO subfamily, including the Agrocybe aegerita (AaeUPO) and Coprinopsis cinerea enzymes, is reported here. To understand the different oxygenation patterns by members of the long-UPO and short-UPO subfamilies, the latter represented by the Marasmius rotula enzyme (MroUPO), fatty-acid diffusion into their heme pockets was simulated with the adaptive PELE software. Computational results shed light on the inability of AaeUPO to epoxidize oleic acid (C18:1), opposed to MroUPO, due to steric hindrances to harbor (with a good interaction energy) the substrate with the ¿9 C10 atom at a catalytically relevant distance (<3.5 Å) from the oxo group in simulated heme compound-I. However, effective a-linolenic acid epoxidation is anticipated because the ¿15 C16 atom would attain such a distance in AaeUPO thanks to its more terminal position. The above hypothesis was verified using an engineered MroUPO variant (I153F/S156F) with a narrowed heme access channel mimicking that of AaeUPO. Experimental oxygenation of unsaturated fatty acids by this variant thus resembles that of AaeUPO, including regioselective (from 95% to >99%) formation of cis,cis-15,16-epoxyoctadeca-9,12-dienoic acid. The nearly complete conversion of a-linolenic acid by the two enzymes was transferred to a small preparative scale, the yield of purified product was estimated, its chemical structure analyzed by NMR, and more interestingly, stereoselective production of the 15(R),16(S) enantiomer (80–83% ee) assessed by chiral HPLC. This enzymatic synthesis overcomes the unspecificity of chemical epoxidation where the reaction cannot be restricted to the formation of monoepoxides as found during m-perchlorobenzoic acid oxidation of a-linolenic acid. Moreover, the variant was able to produce the unsaturated dicarboxylic fatty acid, together with subterminal oxygenation products, during partial conversion of oleic acid. These two noteworthy reactions had not been reported for any UPO described to date.