The origin and distribution of the main oxygen sensing mechanism across metazoans
Oxygen sensing mechanisms are essential for metazoans, their origin and evolution in the context of oxygen in Earth history are of interest. To trace the evolution of a main oxygen sensing mechanism among metazoans, the hypoxia induced factor, HIF, we investigated the phylogenetic distribution and p...
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| Format: | Article |
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2022.977391/full |
| _version_ | 1798031304978071552 |
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| author | Bing Song Luca David Modjewski Nils Kapust Itzhak Mizrahi William F. Martin |
| author_facet | Bing Song Luca David Modjewski Nils Kapust Itzhak Mizrahi William F. Martin |
| author_sort | Bing Song |
| collection | DOAJ |
| description | Oxygen sensing mechanisms are essential for metazoans, their origin and evolution in the context of oxygen in Earth history are of interest. To trace the evolution of a main oxygen sensing mechanism among metazoans, the hypoxia induced factor, HIF, we investigated the phylogenetic distribution and phylogeny of 11 of its components across 566 eukaryote genomes. The HIF based oxygen sensing machinery in eukaryotes can be traced as far back as 800 million years (Ma) ago, likely to the last metazoan common ancestor (LMCA), and arose at a time when the atmospheric oxygen content corresponded roughly to the Pasteur point, or roughly 1% of present atmospheric level (PAL). By the time of the Cambrian explosion (541–485 Ma) as oxygen levels started to approach those of the modern atmosphere, the HIF system with its key components HIF1α, HIF1β, PHD1, PHD4, FIH and VHL was well established across metazoan lineages. HIF1α is more widely distributed and therefore may have evolved earlier than HIF2α and HIF3α, and HIF1β and is more widely distributed than HIF2β in invertebrates. PHD1, PHD4, FIH, and VHL appear in all 13 metazoan phyla. The O2 consuming enzymes of the pathway, PHDs and FIH, have a lower substrate affinity, Km, for O2 than terminal oxidases in the mitochondrial respiratory chain, in line with their function as an environmental signal to switch to anaerobic energy metabolic pathways. The ancient HIF system has been conserved and widespread during the period when metazoans evolved and diversified together with O2 during Earth history. |
| first_indexed | 2024-04-11T19:54:14Z |
| format | Article |
| id | doaj.art-e3dbc112bdef48b98cb0ecf528734b05 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-04-11T19:54:14Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-e3dbc112bdef48b98cb0ecf528734b052022-12-22T04:06:12ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-10-011310.3389/fphys.2022.977391977391The origin and distribution of the main oxygen sensing mechanism across metazoansBing Song0Luca David Modjewski1Nils Kapust2Itzhak Mizrahi3William F. Martin4Department of Biology, Institute for Molecular Evolution, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, GermanyDepartment of Biology, Institute for Molecular Evolution, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, GermanyDepartment of Biology, Institute for Molecular Evolution, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, GermanyDepartment of Life Sciences, Ben-Gurion University of the Negev and the National Institute for Biotechnology in the Negev, Marcus Family Campus, Be’er-Sheva, IsraelDepartment of Biology, Institute for Molecular Evolution, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, GermanyOxygen sensing mechanisms are essential for metazoans, their origin and evolution in the context of oxygen in Earth history are of interest. To trace the evolution of a main oxygen sensing mechanism among metazoans, the hypoxia induced factor, HIF, we investigated the phylogenetic distribution and phylogeny of 11 of its components across 566 eukaryote genomes. The HIF based oxygen sensing machinery in eukaryotes can be traced as far back as 800 million years (Ma) ago, likely to the last metazoan common ancestor (LMCA), and arose at a time when the atmospheric oxygen content corresponded roughly to the Pasteur point, or roughly 1% of present atmospheric level (PAL). By the time of the Cambrian explosion (541–485 Ma) as oxygen levels started to approach those of the modern atmosphere, the HIF system with its key components HIF1α, HIF1β, PHD1, PHD4, FIH and VHL was well established across metazoan lineages. HIF1α is more widely distributed and therefore may have evolved earlier than HIF2α and HIF3α, and HIF1β and is more widely distributed than HIF2β in invertebrates. PHD1, PHD4, FIH, and VHL appear in all 13 metazoan phyla. The O2 consuming enzymes of the pathway, PHDs and FIH, have a lower substrate affinity, Km, for O2 than terminal oxidases in the mitochondrial respiratory chain, in line with their function as an environmental signal to switch to anaerobic energy metabolic pathways. The ancient HIF system has been conserved and widespread during the period when metazoans evolved and diversified together with O2 during Earth history.https://www.frontiersin.org/articles/10.3389/fphys.2022.977391/fullanaerobesmetazoanoriginoxygen sensing mechanismterminal oxidase |
| spellingShingle | Bing Song Luca David Modjewski Nils Kapust Itzhak Mizrahi William F. Martin The origin and distribution of the main oxygen sensing mechanism across metazoans Frontiers in Physiology anaerobes metazoan origin oxygen sensing mechanism terminal oxidase |
| title | The origin and distribution of the main oxygen sensing mechanism across metazoans |
| title_full | The origin and distribution of the main oxygen sensing mechanism across metazoans |
| title_fullStr | The origin and distribution of the main oxygen sensing mechanism across metazoans |
| title_full_unstemmed | The origin and distribution of the main oxygen sensing mechanism across metazoans |
| title_short | The origin and distribution of the main oxygen sensing mechanism across metazoans |
| title_sort | origin and distribution of the main oxygen sensing mechanism across metazoans |
| topic | anaerobes metazoan origin oxygen sensing mechanism terminal oxidase |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2022.977391/full |
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