ATP synthase evolution on a cross-braced dated tree of life

Tara Mahendrarajah; Edmund R R Moody; Dominik Schrempf; Lenard Szantho; Nina Dombrowski; Adrián A. Davín; Davide Pisani; Philip C J Donoghue; Gergely J. Szöllősi; Tom Williams; Anja Spang

doi:10.1038/s41467-023-42924-w

ATP synthase evolution on a cross-braced dated tree of life

Tara Mahendrarajah, Edmund R R Moody, Dominik Schrempf, Lenard Szantho, Nina Dombrowski, Adrián A. Davín, Davide Pisani, Philip C J Donoghue, Gergely J. Szöllősi, Tom Williams^*, Anja Spang^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

23 Citations (Scopus)

Abstract

The timing of early cellular evolution, from the divergence of Archaea and Bacteria to the origin of eukaryotes, is poorly constrained. The ATP synthase complex is thought to have originated prior to the Last Universal Common Ancestor (LUCA) and analyses of ATP synthase genes, together with ribosomes, have played a key role in inferring and rooting the tree of life. We reconstruct the evolutionary history of ATP synthases using an expanded taxon sampling set and develop a phylogenetic cross-bracing approach, constraining equivalent speciation nodes to be contemporaneous, based on the phylogenetic imprint of endosymbioses and ancient gene duplications. This approach results in a highly resolved, dated species tree and establishes an absolute timeline for ATP synthase evolution. Our analyses show that the divergence of ATP synthase into F- and A/V-type lineages was a very early event in cellular evolution dating
35 back to more than 4Ga, potentially predating the diversification of Archaea and Bacteria. Our crossbraced, dated tree of life also provides insight into more recent evolutionary transitions including eukaryogenesis, showing that the eukaryotic nuclear and mitochondrial lineages diverged from their closest archaeal (2.67-2.19Ga) and bacterial (2.58-2.12Ga) relatives at approximately the same time, with a slightly longer nuclear stem-lineage.

Original language	English
Article number	7456
Number of pages	18
Journal	Nature Communications
Volume	14
DOIs	https://doi.org/10.1038/s41467-023-42924-w
Publication status	Published - 17 Nov 2023

Bibliographical note

Funding Information:
This work was supported by the Simons Foundation (735929LPI, to A.S., https://doi.org/10.46714/735929LPI) and the Gordon and Betty Moore Foundation (GBMF9741 to T.A.W., A.S., G.J.S., D.P. and P.C.J.D) and the Gordon and Betty Moore Foundation’s Symbiosis in Aquatic Systems Initiative (GBMF9346, to A.S.). Furthermore, this project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 947317, ASymbEL to A.S. and grant agreement No. 714774, GENECLOCKS to G.J.S.). Further, this work was supported by a Royal Society University Research Fellowship to T.A.W and the John Templeton Foundation (62220, to P.C.J.D., D.P. and T.A.W). Please note that the opinions expressed in this publication are those of the author(s) and do not necessarily reflect the views of the John Templeton Foundation. We are also thankful for financial support from the Swedish Research Council (VR starting grant 2016-03559 to A.S.), the NWO-I foundation of the Netherlands Organisation for Scientific Research (WISE fellowship to A.S.). Finally, we are thankful for financial support from the Leverhulme Trust (RF-2022-167, to P.C.J.D.), the Biotechnology and Biological Sciences Research Council (BB/T012773/1, to P.C.J.D.) and the University of Bristol for a University Research Fellowship (to D.P.). We thank Gertraud Burger, Julius Lukes, Takeshi Nara, and other members of the Diplonema papillatum sequencing consortium for sharing data. We also want to thank Courtney Stairs, Andrew Roger, and Georg Hochberg for helpful discussions and/or feedback regarding eukaryotic metabolism and ancestral sequence reconstructions, respectively.

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© 2023, The Author(s).

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title = "ATP synthase evolution on a cross-braced dated tree of life",

abstract = "The timing of early cellular evolution, from the divergence of Archaea and Bacteria to the origin of eukaryotes, is poorly constrained. The ATP synthase complex is thought to have originated prior to the Last Universal Common Ancestor (LUCA) and analyses of ATP synthase genes, together with ribosomes, have played a key role in inferring and rooting the tree of life. We reconstruct the evolutionary history of ATP synthases using an expanded taxon sampling set and develop a phylogenetic cross-bracing approach, constraining equivalent speciation nodes to be contemporaneous, based on the phylogenetic imprint of endosymbioses and ancient gene duplications. This approach results in a highly resolved, dated species tree and establishes an absolute timeline for ATP synthase evolution. Our analyses show that the divergence of ATP synthase into F- and A/V-type lineages was a very early event in cellular evolution dating35 back to more than 4Ga, potentially predating the diversification of Archaea and Bacteria. Our crossbraced, dated tree of life also provides insight into more recent evolutionary transitions including eukaryogenesis, showing that the eukaryotic nuclear and mitochondrial lineages diverged from their closest archaeal (2.67-2.19Ga) and bacterial (2.58-2.12Ga) relatives at approximately the same time, with a slightly longer nuclear stem-lineage.",

author = "Tara Mahendrarajah and Moody, {Edmund R R} and Dominik Schrempf and Lenard Szantho and Nina Dombrowski and Dav{\'i}n, {Adri{\'a}n A.} and Davide Pisani and Donoghue, {Philip C J} and Sz{\"o}ll{\H o}si, {Gergely J.} and Tom Williams and Anja Spang",

note = "Funding Information: This work was supported by the Simons Foundation (735929LPI, to A.S., https://doi.org/10.46714/735929LPI) and the Gordon and Betty Moore Foundation (GBMF9741 to T.A.W., A.S., G.J.S., D.P. and P.C.J.D) and the Gordon and Betty Moore Foundation{\textquoteright}s Symbiosis in Aquatic Systems Initiative (GBMF9346, to A.S.). Furthermore, this project has received funding from the European Research Council (ERC) under the European Union{\textquoteright}s Horizon 2020 research and innovation programme (grant agreement No. 947317, ASymbEL to A.S. and grant agreement No. 714774, GENECLOCKS to G.J.S.). Further, this work was supported by a Royal Society University Research Fellowship to T.A.W and the John Templeton Foundation (62220, to P.C.J.D., D.P. and T.A.W). Please note that the opinions expressed in this publication are those of the author(s) and do not necessarily reflect the views of the John Templeton Foundation. We are also thankful for financial support from the Swedish Research Council (VR starting grant 2016-03559 to A.S.), the NWO-I foundation of the Netherlands Organisation for Scientific Research (WISE fellowship to A.S.). Finally, we are thankful for financial support from the Leverhulme Trust (RF-2022-167, to P.C.J.D.), the Biotechnology and Biological Sciences Research Council (BB/T012773/1, to P.C.J.D.) and the University of Bristol for a University Research Fellowship (to D.P.). We thank Gertraud Burger, Julius Lukes, Takeshi Nara, and other members of the Diplonema papillatum sequencing consortium for sharing data. We also want to thank Courtney Stairs, Andrew Roger, and Georg Hochberg for helpful discussions and/or feedback regarding eukaryotic metabolism and ancestral sequence reconstructions, respectively. Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

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doi = "10.1038/s41467-023-42924-w",

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T1 - ATP synthase evolution on a cross-braced dated tree of life

AU - Mahendrarajah, Tara

AU - Moody, Edmund R R

AU - Schrempf, Dominik

AU - Szantho, Lenard

AU - Dombrowski, Nina

AU - Davín, Adrián A.

AU - Pisani, Davide

AU - Donoghue, Philip C J

AU - Szöllősi, Gergely J.

AU - Williams, Tom

AU - Spang, Anja

N1 - Funding Information: This work was supported by the Simons Foundation (735929LPI, to A.S., https://doi.org/10.46714/735929LPI) and the Gordon and Betty Moore Foundation (GBMF9741 to T.A.W., A.S., G.J.S., D.P. and P.C.J.D) and the Gordon and Betty Moore Foundation’s Symbiosis in Aquatic Systems Initiative (GBMF9346, to A.S.). Furthermore, this project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 947317, ASymbEL to A.S. and grant agreement No. 714774, GENECLOCKS to G.J.S.). Further, this work was supported by a Royal Society University Research Fellowship to T.A.W and the John Templeton Foundation (62220, to P.C.J.D., D.P. and T.A.W). Please note that the opinions expressed in this publication are those of the author(s) and do not necessarily reflect the views of the John Templeton Foundation. We are also thankful for financial support from the Swedish Research Council (VR starting grant 2016-03559 to A.S.), the NWO-I foundation of the Netherlands Organisation for Scientific Research (WISE fellowship to A.S.). Finally, we are thankful for financial support from the Leverhulme Trust (RF-2022-167, to P.C.J.D.), the Biotechnology and Biological Sciences Research Council (BB/T012773/1, to P.C.J.D.) and the University of Bristol for a University Research Fellowship (to D.P.). We thank Gertraud Burger, Julius Lukes, Takeshi Nara, and other members of the Diplonema papillatum sequencing consortium for sharing data. We also want to thank Courtney Stairs, Andrew Roger, and Georg Hochberg for helpful discussions and/or feedback regarding eukaryotic metabolism and ancestral sequence reconstructions, respectively. Publisher Copyright: © 2023, The Author(s).

PY - 2023/11/17

Y1 - 2023/11/17

N2 - The timing of early cellular evolution, from the divergence of Archaea and Bacteria to the origin of eukaryotes, is poorly constrained. The ATP synthase complex is thought to have originated prior to the Last Universal Common Ancestor (LUCA) and analyses of ATP synthase genes, together with ribosomes, have played a key role in inferring and rooting the tree of life. We reconstruct the evolutionary history of ATP synthases using an expanded taxon sampling set and develop a phylogenetic cross-bracing approach, constraining equivalent speciation nodes to be contemporaneous, based on the phylogenetic imprint of endosymbioses and ancient gene duplications. This approach results in a highly resolved, dated species tree and establishes an absolute timeline for ATP synthase evolution. Our analyses show that the divergence of ATP synthase into F- and A/V-type lineages was a very early event in cellular evolution dating35 back to more than 4Ga, potentially predating the diversification of Archaea and Bacteria. Our crossbraced, dated tree of life also provides insight into more recent evolutionary transitions including eukaryogenesis, showing that the eukaryotic nuclear and mitochondrial lineages diverged from their closest archaeal (2.67-2.19Ga) and bacterial (2.58-2.12Ga) relatives at approximately the same time, with a slightly longer nuclear stem-lineage.

AB - The timing of early cellular evolution, from the divergence of Archaea and Bacteria to the origin of eukaryotes, is poorly constrained. The ATP synthase complex is thought to have originated prior to the Last Universal Common Ancestor (LUCA) and analyses of ATP synthase genes, together with ribosomes, have played a key role in inferring and rooting the tree of life. We reconstruct the evolutionary history of ATP synthases using an expanded taxon sampling set and develop a phylogenetic cross-bracing approach, constraining equivalent speciation nodes to be contemporaneous, based on the phylogenetic imprint of endosymbioses and ancient gene duplications. This approach results in a highly resolved, dated species tree and establishes an absolute timeline for ATP synthase evolution. Our analyses show that the divergence of ATP synthase into F- and A/V-type lineages was a very early event in cellular evolution dating35 back to more than 4Ga, potentially predating the diversification of Archaea and Bacteria. Our crossbraced, dated tree of life also provides insight into more recent evolutionary transitions including eukaryogenesis, showing that the eukaryotic nuclear and mitochondrial lineages diverged from their closest archaeal (2.67-2.19Ga) and bacterial (2.58-2.12Ga) relatives at approximately the same time, with a slightly longer nuclear stem-lineage.

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DO - 10.1038/s41467-023-42924-w

M3 - Article (Academic Journal)

C2 - 37978174

SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

M1 - 7456

ER -

ATP synthase evolution on a cross-braced dated tree of life

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