The evolution of vitamin C biosynthesis and transport in animals.


Journal

BMC ecology and evolution
ISSN: 2730-7182
Titre abrégé: BMC Ecol Evol
Pays: England
ID NLM: 101775613

Informations de publication

Date de publication:
25 06 2022
Historique:
received: 08 10 2021
accepted: 17 06 2022
entrez: 25 6 2022
pubmed: 26 6 2022
medline: 29 6 2022
Statut: epublish

Résumé

Vitamin C (VC) is an indispensable antioxidant and co-factor for optimal function and development of eukaryotic cells. In animals, VC can be synthesized by the organism, acquired through the diet, or both. In the single VC synthesis pathway described in animals, the penultimate step is catalysed by Regucalcin, and the last step by L-gulonolactone oxidase (GULO). The GULO gene has been implicated in VC synthesis only, while Regucalcin has been shown to have multiple functions in mammals. Both GULO and Regucalcin can be found in non-bilaterian, protostome and deuterostome species. Regucalcin, as here shown, is involved in multiple functions such as VC synthesis, calcium homeostasis, and the oxidative stress response in both Deuterostomes and Protostomes, and in insects in receptor-mediated uptake of hexamerin storage proteins from haemolymph. In Insecta and Nematoda, however, there is no GULO gene, and in the latter no Regucalcin gene, but species from these lineages are still able to synthesize VC, implying at least one novel synthesis pathway. In vertebrates, SVCT1, a gene that belongs to a family with up to five members, as here shown, is the only gene involved in the uptake of VC in the gut. This specificity is likely the result of a subfunctionalization event that happened at the base of the Craniata subphylum. SVCT-like genes present in non-Vertebrate animals are likely involved in both VC and nucleobase transport. It is also shown that in lineages where GULO has been lost, SVCT1 is now an essential gene, while in lineages where SVCT1 gene has been lost, GULO is now an essential gene. The simultaneous study, for the first time, of GULO, Regucalcin and SVCTs evolution provides a clear picture of VC synthesis/acquisition and reveals very different selective pressures in different animal taxonomic groups.

Sections du résumé

BACKGROUND
Vitamin C (VC) is an indispensable antioxidant and co-factor for optimal function and development of eukaryotic cells. In animals, VC can be synthesized by the organism, acquired through the diet, or both. In the single VC synthesis pathway described in animals, the penultimate step is catalysed by Regucalcin, and the last step by L-gulonolactone oxidase (GULO). The GULO gene has been implicated in VC synthesis only, while Regucalcin has been shown to have multiple functions in mammals.
RESULTS
Both GULO and Regucalcin can be found in non-bilaterian, protostome and deuterostome species. Regucalcin, as here shown, is involved in multiple functions such as VC synthesis, calcium homeostasis, and the oxidative stress response in both Deuterostomes and Protostomes, and in insects in receptor-mediated uptake of hexamerin storage proteins from haemolymph. In Insecta and Nematoda, however, there is no GULO gene, and in the latter no Regucalcin gene, but species from these lineages are still able to synthesize VC, implying at least one novel synthesis pathway. In vertebrates, SVCT1, a gene that belongs to a family with up to five members, as here shown, is the only gene involved in the uptake of VC in the gut. This specificity is likely the result of a subfunctionalization event that happened at the base of the Craniata subphylum. SVCT-like genes present in non-Vertebrate animals are likely involved in both VC and nucleobase transport. It is also shown that in lineages where GULO has been lost, SVCT1 is now an essential gene, while in lineages where SVCT1 gene has been lost, GULO is now an essential gene.
CONCLUSIONS
The simultaneous study, for the first time, of GULO, Regucalcin and SVCTs evolution provides a clear picture of VC synthesis/acquisition and reveals very different selective pressures in different animal taxonomic groups.

Identifiants

pubmed: 35752765
doi: 10.1186/s12862-022-02040-7
pii: 10.1186/s12862-022-02040-7
pmc: PMC9233358
doi:

Substances chimiques

Antioxidants 0
L-Gulonolactone Oxidase EC 1.1.3.8
Ascorbic Acid PQ6CK8PD0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

84

Informations de copyright

© 2022. The Author(s).

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Auteurs

Pedro Duque (P)

Instituto de Ciências Biomédicas Abel Salazar (ICBAS), Universidade do Porto, Rua de Jorge Viterbo Ferreira, 228, 4050-313, Porto, Portugal.
Faculdade de Ciências da Universidade do Porto (FCUP), Rua do Campo Alegre, s/n, 4169-007, Porto, Portugal.
Instituto de Investigação e Inovação em Saúde (I3S), Universidade do Porto, Rua Alfredo Allen, 208, 4200-135, Porto, Portugal.
Instituto de Biologia Molecular e Celular (IBMC), Rua Alfredo Allen, 208, 4200-135, Porto, Portugal.

Cristina P Vieira (CP)

Instituto de Investigação e Inovação em Saúde (I3S), Universidade do Porto, Rua Alfredo Allen, 208, 4200-135, Porto, Portugal.
Instituto de Biologia Molecular e Celular (IBMC), Rua Alfredo Allen, 208, 4200-135, Porto, Portugal.

Bárbara Bastos (B)

Instituto de Investigação e Inovação em Saúde (I3S), Universidade do Porto, Rua Alfredo Allen, 208, 4200-135, Porto, Portugal.
Instituto de Biologia Molecular e Celular (IBMC), Rua Alfredo Allen, 208, 4200-135, Porto, Portugal.

Jorge Vieira (J)

Instituto de Investigação e Inovação em Saúde (I3S), Universidade do Porto, Rua Alfredo Allen, 208, 4200-135, Porto, Portugal. jbvieira@ibmc.up.pt.
Instituto de Biologia Molecular e Celular (IBMC), Rua Alfredo Allen, 208, 4200-135, Porto, Portugal. jbvieira@ibmc.up.pt.

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