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Lost and Found at Sea: a Phylomentagenomic Exploration of Mitochondrial Affiliations with Oceanic Bacteria.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Molecular Evolution. (Siv Andersson)
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. (Siv Andersson)
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
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(English)Manuscript (Other academic)
Abstract [en]

 

Background

According to the endosymbiont hypothesis, the mitochondrial system for aerobic respiration was derived from a free-living bacterium related to present-day alpha-proteobacteria. Recent studies have identified two lineages as the closest mitochondrial relatives among bacteria with sequenced genomes; the Rickettsiales, a lineage comprising obligate intracellular pathogens, and Pelagibacter ubique, a member of the SAR11 clade that is highly abundant in the upper surface waters of the global oceans.

 

Principal Findings

Here, we present a phylogenetic study incorporating metagenomic data of mitochondrial genes for aerobic respiration that includes sequence data from the Global Ocean Sampling (GOS) Expedition, thereby increasing the sampling of alpha-proteobacterial sequences available for analysis greatly. Phylogenetic analysis of these expanded datasets including oceanic sequences that had been pruned down in numbers but still maintained the full genetic diversity present failed to show an increased support for a specific mitochondrial affiliation to any alpha-proteobacterial group, although concatenated datasets of different genes gave good support for conflicting mitochondrial placement. We utilized a jack-knifing method to randomly sample sequences from the GOS dataset and examined how the inclusion of such sequences influenced the support for mitochondrial affiliation in trees inferred from proteins in aerobic respiration. No evidence of an increased support for a specific mitochondrial placement in the alpha-proteobacterial tree in the jack-knifing analysis was obtained. A systematic search for sequences affiliated with mitochondria in the GOS dataset suggests the existence of previously unidentified clades of deeply diverging alpha-proteobacteria, with an unclear affiliation.

 

Conclusions/Significance

Our findings have several important implications. First, they support an early divergence of the mitochondrial ancestor from the alpha-proteobacterial lineage, possibly pre-dating the radiation of alpha-proteobacterial species with sequenced genomes. Second, they reject the hypothesis that the system for aerobic respiration in mitochondria is affiliated with the SAR11 clade. Third, they indicate horizontal transfer of genes for respiratory chain proteins in bacteria adapted to the upper surface waters of the oceans. Fourth, they show the presence of oceanic sequences for respiratory chain proteins that diverge as deeply as mitochondria in the alpha-proteobacterial phylogeny, possibly indicating a previously unidentified alpha-proteobacterial group at a basal position of the alpha-proteobacterial tree, underscoring the importance of expanding studies on mitochondrial origins beyond those of cultivated and intracellular bacteria. Finally, our study outlines a new methodology, phylometagenomics, which provides guidance on how to incorporate metagenome data into a phylogenetic framework for inferences of early evolutionary events.

 

National Category
Biochemistry and Molecular Biology
Research subject
Molecular Biology
Identifiers
URN: urn:nbn:se:uu:diva-100841OAI: oai:DiVA.org:uu-100841DiVA: diva2:211101
Available from: 2009-04-08 Created: 2009-04-08 Last updated: 2010-01-14
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)
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Available from: 2009-04-28 Created: 2009-03-26 Last updated: 2009-05-04

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Brindefalk, Björn

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