Abstract
There is significant contemporary interest in the application of enzymes to replace or augment chemical reagents toward the development of more environmentally sound and sustainable processes. In particular, copper radical oxidases (CRO) from Auxiliary Activity Family 5 Subfamily 2 (AA5_2) are attractive, organic cofactor-free catalysts for the chemoselective oxidation of alcohols to the corresponding aldehydes. These enzymes were first defined by the archetypal galactose-6-oxidase (GalOx, EC 1.1.3.13) from the fungus Fusarium graminearum. The recent discovery of specific alcohol oxidases (EC 1.1.3.7) and aryl alcohol oxidases (EC 1.1.3.47) within AA5_2 has indicated a potentially broad substrate scope among fungal CROs. However, only relatively few AA5_2 members have been characterized to date. Guided by sequence similarity network and phylogenetic analysis, twelve AA5_2 homologs have been recombinantly produced and biochemically characterized in the present study. As defined by their predominant activities, these comprise four galactose 6-oxidases, two raffinose oxidases, four broad-specificity primary alcohol oxidases, and two non-carbohydrate alcohol oxidases. Of particular relevance to applications in biomass valorization, detailed product analysis revealed that two CROs produce the bioplastics monomer furan-2,5-dicarboxylic acid (FDCA) directly from 5-hydroxymethylfurfural (HMF). Furthermore, several CROs could desymmetrize glycerol (a by-product of the biodiesel industry) to d- or l-glyceraldehyde. This study furthers our understanding of CROs by doubling the number of characterized AA5_2 members, which may find future applications as biocatalysts in diverse processes.
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Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files. All nucleotide sequence, protein sequence, and protein structural information used in this work were extracted from existing accessions in public databases, i.e., GenBank, Joint Genome Institute MycoCosm portal, and the Protein Data Bank.
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Acknowledgements
The authors thank Dr. Maria Ezhova and Dr. Zhicheng (Paul) Xia (UBC Department of Chemistry) for support with NMR data acquisition.
Funding
Funding is gratefully acknowledged from: The Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants RGPIN 435223-13 and RGPIN-2018–03892; NSERC Strategic Partnership Grant NETGP 451431-13 for the “NSERC Industrial Biocatalysis Network”; NSERC Strategic Partnership Grant (STPGP 493781–16) and joint Agence Nationale de la Recherche grant (ANR-17-CE07-0047), “FUNTASTIC—Fungal copper radical oxidases as new biocatalysts for the valorization of biomass carbohydrates and alcohols”; and Genome Canada/Genome BC/Ontario Genomics/Genome Quebec for the Large-Scale Applied Research Project (LSARP, project #10405), “SYNBIOMICS—Functional genomics and techno-economic models for advanced biopolymer synthesis”).
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MC performed enzyme cloning, biochemistry, enzyme kinetic and product analysis, all corresponding data analysis, and drafted the manuscript; YM performed sequence analysis, bioinformatics, and enzyme cloning, wrote portions of manuscript, and revised the manuscript; DR and MH performed recombinant protein production and initial kinetic measurements; PM and JH assisted with the glycerol oxidation experiments; ML and JGB assisted with data analysis; and HB coordinated research, analyzed data, and revised the manuscript with input from all the authors.
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Cleveland, M.E., Mathieu, Y., Ribeaucourt, D. et al. A survey of substrate specificity among Auxiliary Activity Family 5 copper radical oxidases . Cell. Mol. Life Sci. 78, 8187–8208 (2021). https://doi.org/10.1007/s00018-021-03981-w
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DOI: https://doi.org/10.1007/s00018-021-03981-w