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Origin and evolution of the mitochondrial aminoacyl-tRNA synthetases
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
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2007 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 24, no 3, 743-756 p.Article in journal (Refereed) Published
Abstract [en]

Many theories favor a fusion of 2 prokaryotic genomes for the origin of the Eukaryotes, but there are disagreements on the origin, timing, and cellular structures of the cells involved. Equally controversial is the source of the nuclear genes for mitochondrial proteins, although the α-proteobacterial contribution to the mitochondrial genome is well established. Phylogenetic inferences show that the nuclearly encoded mitochondrial aminoacyl-tRNA synthetases (aaRSs) occupy a position in the tree that is not close to any of the currently sequenced α-proteobacterial genomes, despite cohesive and remarkably well-resolved α-proteobacterial clades in 12 of the 20 trees. Two or more α-proteobacterial clusters were observed in 8 cases, indicative of differential loss of paralogous genes or horizontal gene transfer. Replacement and retargeting events within the nuclear genomes of the Eukaryotes was indicated in 10 trees, 4 of which also show split α-proteobacterial groups. A majority of the mitochondrial aaRSs originate from within the bacterial domain, but none specifically from the α-Proteobacteria. For some aaRS, the endosymbiotic origin may have been erased by ongoing gene replacements on the bacterial as well as the eukaryotic side. For others that accurately resolve the α-proteobacterial divergence patterns, the lack of affiliation with mitochondria is more surprising. We hypothesize that the ancestral eukaryotic gene pool hosted primordial "bacterial-like" genes, to which a limited set of α-proteobacterial genes, mostly coding for components of the respiratory chain complexes, were added and selectively maintained.

Place, publisher, year, edition, pages
2007. Vol. 24, no 3, 743-756 p.
Keyword [en]
Aminoacyl-tRNA synthetase, Mitochondria, Phylogeny
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:uu:diva-14983DOI: 10.1093/molbev/msl202ISI: 000244662000013PubMedID: 17182897OAI: oai:DiVA.org:uu-14983DiVA: diva2:42754
Available from: 2008-02-01 Created: 2008-02-01 Last updated: 2017-12-11Bibliographically approved
In thesis
1. Mitochondrial and Eukaryotic Origins: A Phylogenetic Perspective
Open this publication in new window or tab >>Mitochondrial and Eukaryotic Origins: A Phylogenetic Perspective
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Mitochondria are eukaryotic cellular organelles responsible for power-generation, believed to have come into existence by an endo-symbiontic event where a bacterial cell was incorporated by an un-specified "proto-eukaryote". Phylogenetic analysis have shown that the mitochondrial ancestor was most related to present-day alpha-proteobacteria, although the exact nature of the mitochondrial progenitor remains disputed.

In this work, I have used phylogenetic and other methods to investigate the identity of the organism giving rise to mitochondria, by analysing the evolutionary history of select proteins, the events where they have been transfered to the eukaryotic nucleus, and the time-point of mitochondrial establishment. In addition, a search for mitochondrially related organisms in the ocean metagenome was performed, in the hope that something more related to the mitochondrial progenitor than anything previously identified could be found.

Previous analysis have shown that a large fraction of mitochondrial proteins does indeed trace their descent to the alpha-proteobacteria, but I found that the amino-acyl tRNA-synthetases display more general bacterial descent, making it likely that these proteins are of a different origin from the mitochondria themselves.

While the synthetases are encoded on the nuclear genome, most mitochondria still posses most of the tRNA on their own genomes. In the cases where the tRNA has been lost from the mitochondrial genome, I found that the probability of loss correspond to the evolutionary history of their synthetase.

The ocean metagenome represents an order of magnitude more data than previously available, making it suitable for improving the analyses dealing with mitochondrial placement. This large of amount of data was utilised to improve the phylogenetic analyses, showing that previous works might have suffered from artefacts inflating the support for placement of mitochondria with a specific alpha-proteobacterial group.

Eukaryotic/mitochondrial radiation was shown to be as old, or older, than radiation of extant alpha-proteobacteria, casting doubt on previous analysis identifying a specific alpha-proteobacterial group as the mitochondrial ancestor.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2009. 51 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 637
Keyword
Molecular evolution, Phylogenetics, Mitochondrial origin and Evolution
National Category
Biochemistry and Molecular Biology
Research subject
Molecular Biology
Identifiers
urn:nbn:se:uu:diva-100147 (URN)978-91-554-7507-9 (ISBN)
Public defence
2009-05-20, Lindahlsalen, Evolutionsbiologiskt centrum, Norbyvägen 18, 75236 Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2009-04-28 Created: 2009-03-26 Last updated: 2009-05-04
2. Phylogenomics of Oceanic Bacteria
Open this publication in new window or tab >>Phylogenomics of Oceanic Bacteria
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The focus of this thesis has been the phylogenomics and evolution of the Alphaproteobacteria. This is a very diverse group which encompasses bacteria from intraceullar parasites, such as the Rickettsiales, to freeliving bacteria such as the most abundant bacteria on earth, the SAR11. The genome sizes of the Alphaproteobacteria range between 1 Mb and 10 Mb. This group is also connected to the origin of the mitochondria.

Several studies have placed the SAR11 clade together with the Rickettsiales and mitochon- dria. Here I have shown that this placement is an artifact of compositional heterogeneity. When choosing genes or sites less affected by heterogeneity we find that the SAR11-clade instead groups with free-living alphaproteobacteria. Gene-content analysis showed that SAR11 was missing several genes for recombination and DNA-repair. The relationships within the SAR11- clade has also been examined and questioned. Specifically, we found no support for placing the taxon referred to as HIMB59 within the SAR11. Ocean metagenomes have been investigated to determine whether the SAR11-clade is a potential relative of the mitochondria. No such relationship was found.

Further I have shown how important it is to take the phylogenetic relationships into account when doing statistical analyzes of genomes.

The evolution of LD12, the freshwater representative of SAR11, was investigated. Phyloge- nies and synonymous substitution frequencies showed the presence of three distinct subclades within LD12. The recombination to mutation rate was found to be extremely low. This is re- markable in light of the very high rate in the oceanic SAR11. This is may be due to adaptation to a more specialized niche.

Finally we have compared structure-based and sequence-based methods for orthology pre- diction. A high fraction of the orfan proteins were predicted to code for intrinsically disordered proteins.

Many phylogenetic methods are sensitive to heterogeneity and this needs to be taken into ac- count when doing phylogenies. There have been at least three independent genome reductions in the Alphaproteobacteria. The frequency of recombination differ greatly between freshwater and oceanic SAR11. Forces affecting the size of bacterial genomes and mechanisms of evolu- tionary change depend on the environmental context.

 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. 33 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1083
Keyword
phylogenetics, SAR11, mitochondria
National Category
Evolutionary Biology Bioinformatics and Systems Biology
Identifiers
urn:nbn:se:uu:diva-208441 (URN)978-91-554-8767-6 (ISBN)
Public defence
2013-11-14, BMC, B41, Husargatan 8, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2013-10-23 Created: 2013-10-01 Last updated: 2014-01-23

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Brindefalk, BjörnViklund, JohanLarsson, DanielThollesson, MikaelAndersson, Siv G.E.

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