A metagenomic ‘dark matter’ enzyme catalyses oxidative cellulose conversion

Clelton A. Santos, Mariana A. B. Morais, Fernanda Mandelli, Evandro A. Lima, Renan Y. Miyamoto, Paula M. R. Higasi, Evandro A. Araujo, Douglas A. A. Paixão, Joaquim M. Junior, Maria L. Motta, Rodrigo S. A. Streit, Luana G. Morão, Claudio B. C. Silva, Lucia D. Wolf, Cesar R. F. Terrasan, Nathalia R. Bulka, Jose A. Diogo, Felipe J. Fuzita, Felippe M. Colombari, Camila R. Santos, Priscila T. Rodrigues, Daiane B. Silva, Sacha Grisel, Juliana S. Bernardes, Nicolas Terrapon, Vincent Lombard, Antonio J. C. Filho, Bernard Henrissat, Bastien Bissaro, Jean-Guy Berrin, Gabriela F. Persinoti and Mario T. Murakami ()
Additional contact information
Clelton A. Santos: Brazilian Center for Research in Energy and Materials (CNPEM)
Mariana A. B. Morais: Brazilian Center for Research in Energy and Materials (CNPEM)
Fernanda Mandelli: Brazilian Center for Research in Energy and Materials (CNPEM)
Evandro A. Lima: Brazilian Center for Research in Energy and Materials (CNPEM)
Renan Y. Miyamoto: Brazilian Center for Research in Energy and Materials (CNPEM)
Paula M. R. Higasi: Brazilian Center for Research in Energy and Materials (CNPEM)
Evandro A. Araujo: Brazilian Center for Research in Energy and Materials (CNPEM)
Douglas A. A. Paixão: Brazilian Center for Research in Energy and Materials (CNPEM)
Joaquim M. Junior: Brazilian Center for Research in Energy and Materials (CNPEM)
Maria L. Motta: Brazilian Center for Research in Energy and Materials (CNPEM)
Rodrigo S. A. Streit: Brazilian Center for Research in Energy and Materials (CNPEM)
Luana G. Morão: Brazilian Center for Research in Energy and Materials (CNPEM)
Claudio B. C. Silva: Brazilian Center for Research in Energy and Materials (CNPEM)
Lucia D. Wolf: Brazilian Center for Research in Energy and Materials (CNPEM)
Cesar R. F. Terrasan: Brazilian Center for Research in Energy and Materials (CNPEM)
Nathalia R. Bulka: Brazilian Center for Research in Energy and Materials (CNPEM)
Jose A. Diogo: Brazilian Center for Research in Energy and Materials (CNPEM)
Felipe J. Fuzita: Brazilian Center for Research in Energy and Materials (CNPEM)
Felippe M. Colombari: Brazilian Center for Research in Energy and Materials (CNPEM)
Camila R. Santos: Brazilian Center for Research in Energy and Materials (CNPEM)
Priscila T. Rodrigues: Brazilian Center for Research in Energy and Materials (CNPEM)
Daiane B. Silva: Brazilian Center for Research in Energy and Materials (CNPEM)
Sacha Grisel: UMR1163, INRAE, Aix Marseille University
Juliana S. Bernardes: Brazilian Center for Research in Energy and Materials (CNPEM)
Nicolas Terrapon: CNRS, Aix-Marseille University
Vincent Lombard: CNRS, Aix-Marseille University
Antonio J. C. Filho: University of São Paulo
Bernard Henrissat: Technical University of Denmark
Bastien Bissaro: UMR1163, INRAE, Aix Marseille University
Jean-Guy Berrin: UMR1163, INRAE, Aix Marseille University
Gabriela F. Persinoti: Brazilian Center for Research in Energy and Materials (CNPEM)
Mario T. Murakami: Brazilian Center for Research in Energy and Materials (CNPEM)

Nature, 2025, vol. 639, issue 8056, 1076-1083

Abstract: Abstract The breakdown of cellulose is one of the most important reactions in nature1,2 and is central to biomass conversion to fuels and chemicals3. However, the microfibrillar organization of cellulose and its complex interactions with other components of the plant cell wall poses a major challenge for enzymatic conversion4. Here, by mining the metagenomic ‘dark matter’ (unclassified DNA with unknown function) of a microbial community specialized in lignocellulose degradation, we discovered a metalloenzyme that oxidatively cleaves cellulose. This metalloenzyme acts on cellulose through an exo-type mechanism with C1 regioselectivity, resulting exclusively in cellobionic acid as a product. The crystal structure reveals a catalytic copper buried in a compact jelly-roll scaffold that features a flattened cellulose binding site. This metalloenzyme exhibits a homodimeric configuration that enables in situ hydrogen peroxide generation by one subunit while the other is productively interacting with cellulose. The secretome of an engineered strain of the fungus Trichoderma reesei expressing this metalloenzyme boosted the glucose release from pretreated lignocellulosic biomass under industrially relevant conditions, demonstrating its biotechnological potential. This discovery modifies the current understanding of bacterial redox enzymatic systems devoted to overcoming biomass recalcitrance5–7. Furthermore, it enables the conversion of agro-industrial residues into value-added bioproducts, thereby contributing to the transition to a sustainable and bio-based economy.

Date: 2025
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DOI: 10.1038/s41586-024-08553-z

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