Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys
Bioenergetic organelles—mitochondria and plastids—retain their own genomes (mtDNA and ptDNA), and these organelle DNA (oDNA) molecules are vital for eukaryotic life. Like all genomes, oDNA must be able to evolve to suit new environmental challenges. However, mixed oDNA populations in cells can chall...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Genetics |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fgene.2022.974472/full |
| _version_ | 1811336002334097408 |
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| author | Arunas L. Radzvilavicius Arunas L. Radzvilavicius Iain G. Johnston Iain G. Johnston |
| author_facet | Arunas L. Radzvilavicius Arunas L. Radzvilavicius Iain G. Johnston Iain G. Johnston |
| author_sort | Arunas L. Radzvilavicius |
| collection | DOAJ |
| description | Bioenergetic organelles—mitochondria and plastids—retain their own genomes (mtDNA and ptDNA), and these organelle DNA (oDNA) molecules are vital for eukaryotic life. Like all genomes, oDNA must be able to evolve to suit new environmental challenges. However, mixed oDNA populations in cells can challenge cellular bioenergetics, providing a penalty to the appearance and adaptation of new mutations. Here we show that organelle “bottlenecks,” mechanisms increasing cell-to-cell oDNA variability during development, can overcome this mixture penalty and facilitate the adaptation of beneficial mutations. We show that oDNA heteroplasmy and bottlenecks naturally emerge in evolutionary simulations subjected to fluctuating environments, demonstrating that this evolvability is itself evolvable. Usually thought of as a mechanism to clear damaging mutations, organelle bottlenecks therefore also resolve the tension between intracellular selection for pure cellular oDNA populations and the “bet-hedging” need for evolvability and adaptation to new environments. This general theory suggests a reason for the maintenance of organelle heteroplasmy in cells, and may explain some of the observed diversity in organelle maintenance and inheritance across taxa. |
| first_indexed | 2024-04-13T17:33:02Z |
| format | Article |
| id | doaj.art-19c20145ccfd48738b1263276999a20e |
| institution | Directory Open Access Journal |
| issn | 1664-8021 |
| language | English |
| last_indexed | 2024-04-13T17:33:02Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Genetics |
| spelling | doaj.art-19c20145ccfd48738b1263276999a20e2022-12-22T02:37:30ZengFrontiers Media S.A.Frontiers in Genetics1664-80212022-10-011310.3389/fgene.2022.974472974472Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleysArunas L. Radzvilavicius0Arunas L. Radzvilavicius1Iain G. Johnston2Iain G. Johnston3Department of Mathematics, University of Bergen, Bergen, NorwayComputational Biology Unit, University of Bergen, Bergen, NorwayDepartment of Mathematics, University of Bergen, Bergen, NorwayComputational Biology Unit, University of Bergen, Bergen, NorwayBioenergetic organelles—mitochondria and plastids—retain their own genomes (mtDNA and ptDNA), and these organelle DNA (oDNA) molecules are vital for eukaryotic life. Like all genomes, oDNA must be able to evolve to suit new environmental challenges. However, mixed oDNA populations in cells can challenge cellular bioenergetics, providing a penalty to the appearance and adaptation of new mutations. Here we show that organelle “bottlenecks,” mechanisms increasing cell-to-cell oDNA variability during development, can overcome this mixture penalty and facilitate the adaptation of beneficial mutations. We show that oDNA heteroplasmy and bottlenecks naturally emerge in evolutionary simulations subjected to fluctuating environments, demonstrating that this evolvability is itself evolvable. Usually thought of as a mechanism to clear damaging mutations, organelle bottlenecks therefore also resolve the tension between intracellular selection for pure cellular oDNA populations and the “bet-hedging” need for evolvability and adaptation to new environments. This general theory suggests a reason for the maintenance of organelle heteroplasmy in cells, and may explain some of the observed diversity in organelle maintenance and inheritance across taxa.https://www.frontiersin.org/articles/10.3389/fgene.2022.974472/fullmtDNAptDNAevolutionevolvabilityheteroplasmychanging environments |
| spellingShingle | Arunas L. Radzvilavicius Arunas L. Radzvilavicius Iain G. Johnston Iain G. Johnston Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys Frontiers in Genetics mtDNA ptDNA evolution evolvability heteroplasmy changing environments |
| title | Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys |
| title_full | Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys |
| title_fullStr | Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys |
| title_full_unstemmed | Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys |
| title_short | Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys |
| title_sort | organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys |
| topic | mtDNA ptDNA evolution evolvability heteroplasmy changing environments |
| url | https://www.frontiersin.org/articles/10.3389/fgene.2022.974472/full |
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