Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum
The origin of eukaryotes was marked by the emergence of several novel subcellular systems. One such is the calcium (Ca2+)-stores system of the endoplasmic reticulum, which profoundly influences diverse aspects of cellular function including signal transduction, motility, division, and biomineralizat...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-02-01
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| Series: | Frontiers in Genetics |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fgene.2020.00034/full |
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| author | Daniel E. Schäffer Daniel E. Schäffer Lakshminarayan M. Iyer A. Maxwell Burroughs L. Aravind |
| author_facet | Daniel E. Schäffer Daniel E. Schäffer Lakshminarayan M. Iyer A. Maxwell Burroughs L. Aravind |
| author_sort | Daniel E. Schäffer |
| collection | DOAJ |
| description | The origin of eukaryotes was marked by the emergence of several novel subcellular systems. One such is the calcium (Ca2+)-stores system of the endoplasmic reticulum, which profoundly influences diverse aspects of cellular function including signal transduction, motility, division, and biomineralization. We use comparative genomics and sensitive sequence and structure analyses to investigate the evolution of this system. Our findings reconstruct the core form of the Ca2+-stores system in the last eukaryotic common ancestor as having at least 15 proteins that constituted a basic system for facilitating both Ca2+ flux across endomembranes and Ca2+-dependent signaling. We present evidence that the key EF-hand Ca2+-binding components had their origins in a likely bacterial symbiont other than the mitochondrial progenitor, whereas the protein phosphatase subunit of the ancestral calcineurin complex was likely inherited from the asgard archaeal progenitor of the stem eukaryote. This further points to the potential origin of the eukaryotes in a Ca2+-rich biomineralized environment such as stromatolites. We further show that throughout eukaryotic evolution there were several acquisitions from bacteria of key components of the Ca2+-stores system, even though no prokaryotic lineage possesses a comparable system. Further, using quantitative measures derived from comparative genomics we show that there were several rounds of lineage-specific gene expansions, innovations of novel gene families, and gene losses correlated with biological innovation such as the biomineralized molluscan shells, coccolithophores, and animal motility. The burst of innovation of new genes in animals included the wolframin protein associated with Wolfram syndrome in humans. We show for the first time that it contains previously unidentified Sel1, EF-hand, and OB-fold domains, which might have key roles in its biochemistry. |
| first_indexed | 2024-12-11T14:18:25Z |
| format | Article |
| id | doaj.art-8740205a119049539d304753d89460d9 |
| institution | Directory Open Access Journal |
| issn | 1664-8021 |
| language | English |
| last_indexed | 2024-12-11T14:18:25Z |
| publishDate | 2020-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Genetics |
| spelling | doaj.art-8740205a119049539d304753d89460d92022-12-22T01:03:02ZengFrontiers Media S.A.Frontiers in Genetics1664-80212020-02-011110.3389/fgene.2020.00034487335Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic ReticulumDaniel E. Schäffer0Daniel E. Schäffer1Lakshminarayan M. Iyer2A. Maxwell Burroughs3L. Aravind4National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, United StatesScience, Mathematics, and Computer Science Magnet Program, Montgomery Blair High School, Silver Spring, MD, United StatesNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, United StatesNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, United StatesNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, United StatesThe origin of eukaryotes was marked by the emergence of several novel subcellular systems. One such is the calcium (Ca2+)-stores system of the endoplasmic reticulum, which profoundly influences diverse aspects of cellular function including signal transduction, motility, division, and biomineralization. We use comparative genomics and sensitive sequence and structure analyses to investigate the evolution of this system. Our findings reconstruct the core form of the Ca2+-stores system in the last eukaryotic common ancestor as having at least 15 proteins that constituted a basic system for facilitating both Ca2+ flux across endomembranes and Ca2+-dependent signaling. We present evidence that the key EF-hand Ca2+-binding components had their origins in a likely bacterial symbiont other than the mitochondrial progenitor, whereas the protein phosphatase subunit of the ancestral calcineurin complex was likely inherited from the asgard archaeal progenitor of the stem eukaryote. This further points to the potential origin of the eukaryotes in a Ca2+-rich biomineralized environment such as stromatolites. We further show that throughout eukaryotic evolution there were several acquisitions from bacteria of key components of the Ca2+-stores system, even though no prokaryotic lineage possesses a comparable system. Further, using quantitative measures derived from comparative genomics we show that there were several rounds of lineage-specific gene expansions, innovations of novel gene families, and gene losses correlated with biological innovation such as the biomineralized molluscan shells, coccolithophores, and animal motility. The burst of innovation of new genes in animals included the wolframin protein associated with Wolfram syndrome in humans. We show for the first time that it contains previously unidentified Sel1, EF-hand, and OB-fold domains, which might have key roles in its biochemistry.https://www.frontiersin.org/article/10.3389/fgene.2020.00034/fullcalcium bindingcalcium storescalmodulinchannelseukaryote originsendomembranes |
| spellingShingle | Daniel E. Schäffer Daniel E. Schäffer Lakshminarayan M. Iyer A. Maxwell Burroughs L. Aravind Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum Frontiers in Genetics calcium binding calcium stores calmodulin channels eukaryote origins endomembranes |
| title | Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum |
| title_full | Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum |
| title_fullStr | Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum |
| title_full_unstemmed | Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum |
| title_short | Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum |
| title_sort | functional innovation in the evolution of the calcium dependent system of the eukaryotic endoplasmic reticulum |
| topic | calcium binding calcium stores calmodulin channels eukaryote origins endomembranes |
| url | https://www.frontiersin.org/article/10.3389/fgene.2020.00034/full |
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