Divergence time estimates for the hypoxia-inducible factor-1 alpha (HIF1α) reveal an ancient emergence of animals in low-oxygen environments.


Journal

Geobiology
ISSN: 1472-4669
Titre abrégé: Geobiology
Pays: England
ID NLM: 101185472

Informations de publication

Date de publication:
26 Sep 2023
Historique:
revised: 13 07 2023
received: 10 10 2022
accepted: 07 09 2023
medline: 26 9 2023
pubmed: 26 9 2023
entrez: 26 9 2023
Statut: aheadofprint

Résumé

Unveiling the tempo and mode of animal evolution is necessary to understand the links between environmental changes and biological innovation. Although the earliest unambiguous metazoan fossils date to the late Ediacaran period, molecular clock estimates agree that the last common ancestor (LCA) of all extant animals emerged ~850 Ma, in the Tonian period, before the oldest evidence for widespread ocean oxygenation at ~635-560 Ma in the Ediacaran period. Metazoans are aerobic organisms, that is, they are dependent on oxygen to survive. In low-oxygen conditions, most animals have an evolutionarily conserved pathway for maintaining oxygen homeostasis that triggers physiological changes in gene expression via the hypoxia-inducible factor (HIFa). However, here we confirm the absence of the characteristic HIFa protein domain responsible for the oxygen sensing of HIFa in sponges and ctenophores, indicating the LCA of metazoans lacked the functional protein domain as well, and so could have maintained their transcription levels unaltered under the very low-oxygen concentrations of their environments. Using Bayesian relaxed molecular clock dating, we inferred that the ancestral gene lineage responsible for HIFa arose in the Mesoproterozoic Era, ~1273 Ma (Credibility Interval 957-1621 Ma), consistent with the idea that important genetic machinery associated with animals evolved much earlier than the LCA of animals. Our data suggest at least two duplication events in the evolutionary history of HIFa, which generated three vertebrate paralogs, products of the two successive whole-genome duplications that occurred in the vertebrate LCA. Overall, our results support the hypothesis of a pre-Tonian emergence of metazoans under low-oxygen conditions, and an increase in oxygen response elements during animal evolution.

Identifiants

pubmed: 37750460
doi: 10.1111/gbi.12577
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
Organisme : National Science Foundation

Informations de copyright

© 2023 John Wiley & Sons Ltd.

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Auteurs

Flavia A Belato (FA)

Institute of Biosciences, Department of Zoology, University of Sao Paulo, São Paulo - SP, Brazil.

Beatriz Mello (B)

Biology Institute, Genetics Department, Federal University of Rio de Janeiro, Rio de Janeiro - RJ, Brazil.

Christopher J Coates (CJ)

Zoology, Ryan Institute, School of Natural Sciences, University of Galway, Galway, Ireland.

Kenneth M Halanych (KM)

Center for Marine Science, University of North Carolina Wilmington, Wilmington, North Carolina, USA.

Federico D Brown (FD)

Institute of Biosciences, Department of Zoology, University of Sao Paulo, São Paulo - SP, Brazil.

André C Morandini (AC)

Institute of Biosciences, Department of Zoology, University of Sao Paulo, São Paulo - SP, Brazil.

Juliana de Moraes Leme (J)

Geoscience Institute, University of Sao Paulo, São Paulo - SP, Brazil.

Ricardo I F Trindade (RIF)

Institute of Astronomy, Geophysics and Atmospheric Sciences, University of Sao Paulo, São Paulo - SP, Brazil.

Elisa Maria Costa-Paiva (EM)

Institute of Biosciences, Department of Zoology, University of Sao Paulo, São Paulo - SP, Brazil.
Institute of Astronomy, Geophysics and Atmospheric Sciences, University of Sao Paulo, São Paulo - SP, Brazil.

Classifications MeSH