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Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals

Bruno Santos Bezerra, Flavia Ariany Belato, Beatriz Mello, Federico Brown, Christopher Coates, Juliana de Moraes Leme, Ricardo I. F. Trindade, Elisa Maria Costa-Paiva

Scientific Reports, Volume: 11, Issue: 1

Swansea University Author: Christopher Coates

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DOI (Published version): 10.1038/s41598-021-95094-4

Abstract

The biological toolkits for aerobic respiration were critical for the rise and diversification of early animals. Aerobic life forms generate ATP through the oxidation of organic molecules in a process known as Krebs’ Cycle, where the enzyme isocitrate dehydrogenase (IDH) regulates the cycle's t...

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Published in: Scientific Reports
ISSN: 2045-2322
Published: Springer Science and Business Media LLC 2021
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URI: https://cronfa.swan.ac.uk/Record/cronfa57414
first_indexed 2021-07-19T07:38:22Z
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spelling 2022-07-07T14:25:10.3682945 v2 57414 2021-07-19 Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals af160934b75bea5b8ba83d68b3d1a003 Christopher Coates Christopher Coates true false 2021-07-19 BGPS The biological toolkits for aerobic respiration were critical for the rise and diversification of early animals. Aerobic life forms generate ATP through the oxidation of organic molecules in a process known as Krebs’ Cycle, where the enzyme isocitrate dehydrogenase (IDH) regulates the cycle's turnover rate. Evolutionary reconstructions and molecular dating of proteins related to oxidative metabolism, such as IDH, can therefore provide an estimate of when the diversification of major taxa occurred, and their coevolution with the oxidative state of oceans and atmosphere. To establish the evolutionary history and divergence time of NAD-dependent IDH, we examined transcriptomic data from 195 eukaryotes (mostly animals). We demonstrate that two duplication events occurred in the evolutionary history of NAD-IDH, one in the ancestor of eukaryotes approximately at 1967 Ma, and another at 1629 Ma, both in the Paleoproterozoic Era. Moreover, NAD-IDH regulatory subunits β and γ are exclusive to metazoans, arising in the Mesoproterozoic. Our results therefore support the concept of an ‘‘earlier-than-Tonian’’ diversification of eukaryotes and the pre-Cryogenian emergence of a metazoan IDH enzyme. Journal Article Scientific Reports 11 1 Springer Science and Business Media LLC 2045-2322 3 8 2021 2021-08-03 10.1038/s41598-021-95094-4 COLLEGE NANME Biosciences Geography and Physics School COLLEGE CODE BGPS Swansea University Another institution paid the OA fee The study was supported by FAPESP, by thematic project (Proc. 2016/06114-6), coordinated by R.I.T. A fellowship to E.M.C-P. was provided by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil—2018/20268-1). F.A.B. was supported by CNPq and FAPESP (Proc. 2019/18051-7). C.J.C.’s contributions are facilitated by start-up funds from the College of Science, Swansea University. 2022-07-07T14:25:10.3682945 2021-07-19T08:36:13.9414543 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Bruno Santos Bezerra 1 Flavia Ariany Belato 2 Beatriz Mello 3 Federico Brown 4 Christopher Coates 5 Juliana de Moraes Leme 6 Ricardo I. F. Trindade 7 Elisa Maria Costa-Paiva 8 57414__20687__f8b4fa5f54254e66a7a8f6832b472ab1.pdf 57414.pdf 2021-08-19T17:17:01.8318225 Output 2283099 application/pdf Version of Record true © The Author(s) 2021. Tis article is licensed under a Creative Commons Attribution 4.0 International License true eng http://creativecommons.org/licenses/by/4.0/
title Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals
spellingShingle Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals
Christopher Coates
title_short Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals
title_full Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals
title_fullStr Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals
title_full_unstemmed Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals
title_sort Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals
author_id_str_mv af160934b75bea5b8ba83d68b3d1a003
author_id_fullname_str_mv af160934b75bea5b8ba83d68b3d1a003_***_Christopher Coates
author Christopher Coates
author2 Bruno Santos Bezerra
Flavia Ariany Belato
Beatriz Mello
Federico Brown
Christopher Coates
Juliana de Moraes Leme
Ricardo I. F. Trindade
Elisa Maria Costa-Paiva
format Journal article
container_title Scientific Reports
container_volume 11
container_issue 1
publishDate 2021
institution Swansea University
issn 2045-2322
doi_str_mv 10.1038/s41598-021-95094-4
publisher Springer Science and Business Media LLC
college_str Faculty of Science and Engineering
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hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
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description The biological toolkits for aerobic respiration were critical for the rise and diversification of early animals. Aerobic life forms generate ATP through the oxidation of organic molecules in a process known as Krebs’ Cycle, where the enzyme isocitrate dehydrogenase (IDH) regulates the cycle's turnover rate. Evolutionary reconstructions and molecular dating of proteins related to oxidative metabolism, such as IDH, can therefore provide an estimate of when the diversification of major taxa occurred, and their coevolution with the oxidative state of oceans and atmosphere. To establish the evolutionary history and divergence time of NAD-dependent IDH, we examined transcriptomic data from 195 eukaryotes (mostly animals). We demonstrate that two duplication events occurred in the evolutionary history of NAD-IDH, one in the ancestor of eukaryotes approximately at 1967 Ma, and another at 1629 Ma, both in the Paleoproterozoic Era. Moreover, NAD-IDH regulatory subunits β and γ are exclusive to metazoans, arising in the Mesoproterozoic. Our results therefore support the concept of an ‘‘earlier-than-Tonian’’ diversification of eukaryotes and the pre-Cryogenian emergence of a metazoan IDH enzyme.
published_date 2021-08-03T02:22:15Z
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