Horizontal and endosymbiotic gene transfer in early plastid evolution

AbstractThe endosymbiosis of the bacterial progenitors of mitochondrion and the chloroplast are landmark events in the evolution of life on earth. While both organelles have retained substantial proteomic and biochemical complexity, this complexity is not reflected in the content of their genomes. Instead, the organellar genomes encode fewer than 5% of genes found in living relatives of their ancestors. While some of the 95% of missing organellar genes have been discarded, many have been transferred to the host nuclear genome through a process known as endosymbiotic gene transfer. Here we demonstrate that the energy liberated or consumed by a cell as a result of endosymbiotic gene transfer can be sufficient to provide a selectable advantage for retention or nuclear-transfer of organellar genes in eukaryotic cells. We further demonstrate that for realistic estimates of protein abundances, organellar protein import costs, host cell sizes, and cellular investment in organelles that it is energetically favourable to transfer the majority of organellar genes to the nuclear genome. Moreover, we show that the selective advantage of such transfers is sufficiently large to enable such events to rapidly reach fixation. Thus, endosymbiotic gene transfer can be advantageous in the absence of any additional benefit to the host cell, providing new insight into the processes that have shaped eukaryotic genome evolution.One sentence summaryThe high copy number of organellar genomes renders endosymbiotic gene transfer energetically favourable for the vast majority of organellar genes.

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The economics of organellar gene loss and endosymbiotic gene transfer

Genome Biology ◽

10.1186/s13059-021-02567-w ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Steven Kelly

Keyword(s):

Gene Transfer ◽

Nuclear Genome ◽

Energy Budgets ◽

Net Energy ◽

Endosymbiotic Gene Transfer ◽

Organellar Genomes ◽

Chloroplast Genomes ◽

Evolution Of Life ◽

The Difference ◽

Life On Earth

Abstract Background The endosymbiosis of the bacterial progenitors of the mitochondrion and the chloroplast are landmark events in the evolution of life on Earth. While both organelles have retained substantial proteomic and biochemical complexity, this complexity is not reflected in the content of their genomes. Instead, the organellar genomes encode fewer than 5% of the genes found in living relatives of their ancestors. While many of the 95% of missing organellar genes have been discarded, others have been transferred to the host nuclear genome through a process known as endosymbiotic gene transfer. Results Here, we demonstrate that the difference in the per-cell copy number of the organellar and nuclear genomes presents an energetic incentive to the cell to either delete organellar genes or transfer them to the nuclear genome. We show that, for the majority of transferred organellar genes, the energy saved by nuclear transfer exceeds the costs incurred from importing the encoded protein into the organelle where it can provide its function. Finally, we show that the net energy saved by endosymbiotic gene transfer can constitute an appreciable proportion of total cellular energy budgets and is therefore sufficient to impart a selectable advantage to the cell. Conclusion Thus, reduced cellular cost and improved energy efficiency likely played a role in the reductive evolution of mitochondrial and chloroplast genomes and the transfer of organellar genes to the nuclear genome.

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Plastid evolution: gene transfer and the maintenance of 'stolen' organelles

BMC Biology ◽

10.1186/1741-7007-8-73 ◽

2010 ◽

Vol 8 (1) ◽

Cited By ~ 14

Author(s):

Eunsoo Kim ◽

John M Archibald

Keyword(s):

Gene Transfer ◽

Plastid Evolution

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Endosymbiotic Gene Transfer

Encyclopedia of Genetics, Genomics, Proteomics and Informatics ◽

10.1007/978-1-4020-6754-9_5334 ◽

2008 ◽

pp. 608-608

Keyword(s):

Gene Transfer ◽

Endosymbiotic Gene Transfer

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Endosymbiotic Gene Transfer in Tertiary Plastid-Containing Dinoflagellates

Eukaryotic Cell ◽

10.1128/ec.00299-13 ◽

2013 ◽

Vol 13 (2) ◽

pp. 246-255 ◽

Cited By ~ 34

Author(s):

Fabien Burki ◽

Behzad Imanian ◽

Elisabeth Hehenberger ◽

Yoshihisa Hirakawa ◽

Shinichiro Maruyama ◽

...

Keyword(s):

Gene Transfer ◽

Host Genome ◽

Data Sets ◽

Transcriptome Data ◽

Endosymbiotic Gene Transfer ◽

Low Level ◽

Long Period ◽

Host Nucleus ◽

Endosymbiotic Origin

ABSTRACTPlastid establishment involves the transfer of endosymbiotic genes to the host nucleus, a process known as endosymbiotic gene transfer (EGT). Large amounts of EGT have been shown in several photosynthetic lineages but also in present-day plastid-lacking organisms, supporting the notion that endosymbiotic genes leave a substantial genetic footprint in the host nucleus. Yet the extent of this genetic relocation remains debated, largely because the long period that has passed since most plastids originated has erased many of the clues to how this process unfolded. Among the dinoflagellates, however, the ancestral peridinin-containing plastid has been replaced by tertiary plastids on several more recent occasions, giving us a less ancient window to examine plastid origins. In this study, we evaluated the endosymbiotic contribution to the host genome in two dinoflagellate lineages with tertiary plastids. We generated the first nuclear transcriptome data sets for the “dinotoms,” which harbor diatom-derived plastids, and analyzed these data in combination with the available transcriptomes for kareniaceans, which harbor haptophyte-derived plastids. We found low level of detectable EGT in both dinoflagellate lineages, with only 9 genes and 90 genes of possible tertiary endosymbiotic origin in dinotoms and kareniaceans, respectively, suggesting that tertiary endosymbioses did not heavily impact the host dinoflagellate genomes.

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