Structure, mechanism, and evolution of the last step in vitamin C biosynthesis

Autores
Boverio, Alessandro; Jamil, Neelam; Mannucci, Barbara; Mascotti, María Laura; Fraaije, Marco W.; Mattevi, Andrea
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Photosynthetic organisms, fungi, and animals comprise distinct pathways forvitamin C biosynthesis. Besides this diversity, the final biosynthetic step con-sistently involves an oxidation reaction carried out by the aldonolactone oxi-doreductases. Here, we study the origin and evolution of the diversifiedactivities and substrate preferences featured by these flavoenzymes usingmolecular phylogeny, kinetics, mutagenesis, and crystallographic experi-ments. We find clear evidence that they share a common ancestor. A flavin-interacting amino acid modulates the reactivity with the electron acceptors,including oxygen, and determines whether an enzyme functions as an oxidaseor a dehydrogenase. We show that a few side chains in the catalytic cavityimpart the reaction stereoselectivity. Ancestral sequence reconstruction out-lines how these critical positions were affixed to specific amino acids along theevolution of the major eukaryotic clades. During Eukarya evolution, thealdonolactone oxidoreductases adapted to the varying metabolic demandswhile retaining their overarching vitamin C-generating function.
Fil: Boverio, Alessandro. University of Groningen; Países Bajos. Universita degli Studi di Pavia; Italia
Fil: Jamil, Neelam. Universita degli Studi di Pavia; Italia
Fil: Mannucci, Barbara. Universita degli Studi di Pavia; Italia
Fil: Mascotti, María Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis. Universidad Nacional de San Luis. Facultad de Ciencias Físico Matemáticas y Naturales. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis; Argentina
Fil: Fraaije, Marco W.. University of Groningen; Países Bajos
Fil: Mattevi, Andrea. Universita degli Studi di Pavia; Italia
Materia
VITAMIN C
GULO
ANCESTRAL SEQUENCE RECONSTRUCTION
GALDH
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/264850
Acceder
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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Structure, mechanism, and evolution of the last step in vitamin C biosynthesisBoverio, AlessandroJamil, NeelamMannucci, BarbaraMascotti, María LauraFraaije, Marco W.Mattevi, AndreaVITAMIN CGULOANCESTRAL SEQUENCE RECONSTRUCTIONGALDHhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1https://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Photosynthetic organisms, fungi, and animals comprise distinct pathways forvitamin C biosynthesis. Besides this diversity, the final biosynthetic step con-sistently involves an oxidation reaction carried out by the aldonolactone oxi-doreductases. Here, we study the origin and evolution of the diversifiedactivities and substrate preferences featured by these flavoenzymes usingmolecular phylogeny, kinetics, mutagenesis, and crystallographic experi-ments. We find clear evidence that they share a common ancestor. A flavin-interacting amino acid modulates the reactivity with the electron acceptors,including oxygen, and determines whether an enzyme functions as an oxidaseor a dehydrogenase. We show that a few side chains in the catalytic cavityimpart the reaction stereoselectivity. Ancestral sequence reconstruction out-lines how these critical positions were affixed to specific amino acids along theevolution of the major eukaryotic clades. During Eukarya evolution, thealdonolactone oxidoreductases adapted to the varying metabolic demandswhile retaining their overarching vitamin C-generating function.Fil: Boverio, Alessandro. University of Groningen; Países Bajos. Universita degli Studi di Pavia; ItaliaFil: Jamil, Neelam. Universita degli Studi di Pavia; ItaliaFil: Mannucci, Barbara. Universita degli Studi di Pavia; ItaliaFil: Mascotti, María Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis. Universidad Nacional de San Luis. Facultad de Ciencias Físico Matemáticas y Naturales. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis; ArgentinaFil: Fraaije, Marco W.. University of Groningen; Países BajosFil: Mattevi, Andrea. Universita degli Studi di Pavia; ItaliaSpringer2024-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/264850Boverio, Alessandro; Jamil, Neelam; Mannucci, Barbara; Mascotti, María Laura; Fraaije, Marco W.; et al.; Structure, mechanism, and evolution of the last step in vitamin C biosynthesis; Springer; Nature Communications; 15; 1; 5-2024; 1-102041-1723CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41467-024-48410-1info:eu-repo/semantics/altIdentifier/doi/10.1038/s41467-024-48410-1info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:54:01Zoai:ri.conicet.gov.ar:11336/264850instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:54:02.042CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Structure, mechanism, and evolution of the last step in vitamin C biosynthesis
title Structure, mechanism, and evolution of the last step in vitamin C biosynthesis
spellingShingle Structure, mechanism, and evolution of the last step in vitamin C biosynthesis
Boverio, Alessandro
VITAMIN C
GULO
ANCESTRAL SEQUENCE RECONSTRUCTION
GALDH
title_short Structure, mechanism, and evolution of the last step in vitamin C biosynthesis
title_full Structure, mechanism, and evolution of the last step in vitamin C biosynthesis
title_fullStr Structure, mechanism, and evolution of the last step in vitamin C biosynthesis
title_full_unstemmed Structure, mechanism, and evolution of the last step in vitamin C biosynthesis
title_sort Structure, mechanism, and evolution of the last step in vitamin C biosynthesis
dc.creator.none.fl_str_mv Boverio, Alessandro
Jamil, Neelam
Mannucci, Barbara
Mascotti, María Laura
Fraaije, Marco W.
Mattevi, Andrea
author Boverio, Alessandro
author_facet Boverio, Alessandro
Jamil, Neelam
Mannucci, Barbara
Mascotti, María Laura
Fraaije, Marco W.
Mattevi, Andrea
author_role author
author2 Jamil, Neelam
Mannucci, Barbara
Mascotti, María Laura
Fraaije, Marco W.
Mattevi, Andrea
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv VITAMIN C
GULO
ANCESTRAL SEQUENCE RECONSTRUCTION
GALDH
topic VITAMIN C
GULO
ANCESTRAL SEQUENCE RECONSTRUCTION
GALDH
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Photosynthetic organisms, fungi, and animals comprise distinct pathways forvitamin C biosynthesis. Besides this diversity, the final biosynthetic step con-sistently involves an oxidation reaction carried out by the aldonolactone oxi-doreductases. Here, we study the origin and evolution of the diversifiedactivities and substrate preferences featured by these flavoenzymes usingmolecular phylogeny, kinetics, mutagenesis, and crystallographic experi-ments. We find clear evidence that they share a common ancestor. A flavin-interacting amino acid modulates the reactivity with the electron acceptors,including oxygen, and determines whether an enzyme functions as an oxidaseor a dehydrogenase. We show that a few side chains in the catalytic cavityimpart the reaction stereoselectivity. Ancestral sequence reconstruction out-lines how these critical positions were affixed to specific amino acids along theevolution of the major eukaryotic clades. During Eukarya evolution, thealdonolactone oxidoreductases adapted to the varying metabolic demandswhile retaining their overarching vitamin C-generating function.
Fil: Boverio, Alessandro. University of Groningen; Países Bajos. Universita degli Studi di Pavia; Italia
Fil: Jamil, Neelam. Universita degli Studi di Pavia; Italia
Fil: Mannucci, Barbara. Universita degli Studi di Pavia; Italia
Fil: Mascotti, María Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis. Universidad Nacional de San Luis. Facultad de Ciencias Físico Matemáticas y Naturales. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis; Argentina
Fil: Fraaije, Marco W.. University of Groningen; Países Bajos
Fil: Mattevi, Andrea. Universita degli Studi di Pavia; Italia
description Photosynthetic organisms, fungi, and animals comprise distinct pathways forvitamin C biosynthesis. Besides this diversity, the final biosynthetic step con-sistently involves an oxidation reaction carried out by the aldonolactone oxi-doreductases. Here, we study the origin and evolution of the diversifiedactivities and substrate preferences featured by these flavoenzymes usingmolecular phylogeny, kinetics, mutagenesis, and crystallographic experi-ments. We find clear evidence that they share a common ancestor. A flavin-interacting amino acid modulates the reactivity with the electron acceptors,including oxygen, and determines whether an enzyme functions as an oxidaseor a dehydrogenase. We show that a few side chains in the catalytic cavityimpart the reaction stereoselectivity. Ancestral sequence reconstruction out-lines how these critical positions were affixed to specific amino acids along theevolution of the major eukaryotic clades. During Eukarya evolution, thealdonolactone oxidoreductases adapted to the varying metabolic demandswhile retaining their overarching vitamin C-generating function.
publishDate 2024
dc.date.none.fl_str_mv 2024-05
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/264850
Boverio, Alessandro; Jamil, Neelam; Mannucci, Barbara; Mascotti, María Laura; Fraaije, Marco W.; et al.; Structure, mechanism, and evolution of the last step in vitamin C biosynthesis; Springer; Nature Communications; 15; 1; 5-2024; 1-10
2041-1723
CONICET Digital
CONICET
url http://hdl.handle.net/11336/264850
identifier_str_mv Boverio, Alessandro; Jamil, Neelam; Mannucci, Barbara; Mascotti, María Laura; Fraaije, Marco W.; et al.; Structure, mechanism, and evolution of the last step in vitamin C biosynthesis; Springer; Nature Communications; 15; 1; 5-2024; 1-10
2041-1723
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41467-024-48410-1
info:eu-repo/semantics/altIdentifier/doi/10.1038/s41467-024-48410-1
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.13397

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