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Independent Genome Reduction and Phylogenetic Reclassification of the Oceanic SAR11 Clade
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
2011 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 29, no 2, 599-615 p.Article in journal (Refereed) Published
Abstract [en]

The SAR11 clade, here represented by Candidatus Pelagibacter ubique, is the most successful group of bacteria in the upper surface waters of the oceans. In contrast to previous studies that have associated the 1.3 Mb genome of Ca. Pelagibacter ubique with the less than 1.5 Mb genomes of the Rickettsiales, our phylogenetic analysis suggests that Ca. Pelagibacter ubique is most closely related to soil and aquatic Alphaproteobacteria with large genomes. This implies that the SAR11 clade and the Rickettsiales have undergone genome reduction independently. A gene flux analysis of 46 representative alphaproteobacterial genomes indicates the loss of more than 800 genes in each of Ca. Pelagibacter ubique and the Rickettsiales. Consistent with their different phylogenetic affiliations, the pattern of gene loss differs with a higher loss of genes for repair and recombination processes in Ca. Pelagibacter ubique as compared with a more extensive loss of genes for biosynthetic functions in the Rickettsiales. Some of the lost genes in Ca. Pelagibacter ubique, such as mutLS, recFN, and ruvABC, are conserved in all other alphaproteobacterial genomes including the small genomes of the Rickettsiales. The mismatch repair genes mutLS are absent from all currently sequenced SAR11 genomes and also underrepresented in the global ocean metagenome data set. We hypothesize that the unique loss of genes involved in repair and recombination processes in Ca. Pelagibacter ubique has been driven by selection and that this helps explain many of the characteristics of the SAR11 population, such as the streamlined genomes, the long branch lengths, the high recombination frequencies, and the extensive sequence divergence within the population.

Place, publisher, year, edition, pages
2011. Vol. 29, no 2, 599-615 p.
Keyword [en]
genome reduction, SAR11, Alphaproteobacteria, mismatch repair system, ocean surface waters, Candidatus Pelagibacter ubique, recombination, gene loss
National Category
Microbiology Evolutionary Biology Bioinformatics and Systems Biology
Identifiers
URN: urn:nbn:se:uu:diva-165703DOI: 10.1093/molbev/msr203ISI: 000299129000013PubMedID: 21900598OAI: oai:DiVA.org:uu-165703DiVA: diva2:474471
Funder
EU, European Research CouncilSwedish Research Council, 621-2009-4813 315-2004-6676 349-2007-831 621-2008-3259Swedish Foundation for Strategic Research Göran Gustafsson Foundation for promotion of scientific research at Uppala University and Royal Institute of TechnologyKnut and Alice Wallenberg FoundationSwedish National Infrastructure for Computing (SNIC), p2006019
Available from: 2012-01-09 Created: 2012-01-09 Last updated: 2017-12-08Bibliographically approved
In thesis
1. 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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Viklund, JohanEttema, ThijsAndersson, Siv G. E.

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