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Single cell genomics reveals low recombination frequencies in freshwater bacteria of the SAR11 clade
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
Uppsala University, Disciplinary Domain of Humanities and Social Sciences, Faculty of Languages, Department of Scandinavian Languages.
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2013 (English)In: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 14, no 11, R130Article in journal (Refereed) Published
Abstract [en]

Background: The SAR11 group of Alphaproteobacteria is highly abundant in the oceans. It contains a recently diverged freshwater clade, which offers the opportunity to compare adaptations to salt-and freshwaters in a monophyletic bacterial group. However, there are no cultivated members of the freshwater SAR11 group and no genomes have been sequenced yet. Results: We isolated ten single SAR11 cells from three freshwater lakes and sequenced and assembled their genomes. A phylogeny based on 57 proteins indicates that the cells are organized into distinct microclusters. We show that the freshwater genomes have evolved primarily by the accumulation of nucleotide substitutions and that they have among the lowest ratio of recombination to mutation estimated for bacteria. In contrast, members of the marine SAR11 clade have one of the highest ratios. Additional metagenome reads from six lakes confirm low recombination frequencies for the genome overall and reveal lake-specific variations in microcluster abundances. We identify hypervariable regions with gene contents broadly similar to those in the hypervariable regions of the marine isolates, containing genes putatively coding for cell surface molecules. Conclusions: We conclude that recombination rates differ dramatically in phylogenetic sister groups of the SAR11 clade adapted to freshwater and marine ecosystems. The results suggest that the transition from marine to freshwater systems has purged diversity and resulted in reduced opportunities for recombination with divergent members of the clade. The low recombination frequencies of the LD12 clade resemble the low genetic divergence of host-restricted pathogens that have recently shifted to a new host.

Place, publisher, year, edition, pages
2013. Vol. 14, no 11, R130
National Category
Microbiology
Identifiers
URN: urn:nbn:se:uu:diva-206203DOI: 10.1186/gb-2013-14-11-r130ISI: 000330616200009PubMedID: 24286338OAI: oai:DiVA.org:uu-206203DiVA: diva2:645058
Funder
Swedish Research Council, 349-2007-831 621-2008-3259 621-2011-4669-4669 2009-3784 2008-1923 2012-3892EU, European Research CouncilGöran Gustafsson Foundation for promotion of scientific research at Uppala University and Royal Institute of TechnologyKnut and Alice Wallenberg Foundation, KAW-2011.0148 KAW-2012.0075Swedish National Infrastructure for Computing (SNIC), p2006019 p2009043
Available from: 2013-09-03 Created: 2013-08-29 Last updated: 2017-12-06Bibliographically 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
2. Microbial Metagenomics: A Tale of the Dead and the Living
Open this publication in new window or tab >>Microbial Metagenomics: A Tale of the Dead and the Living
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

It is a microbial world we live in: microbes outnumber other organisms by several orders of magnitude, and they have great importance for the environment. However, environmental microbes are notoriously difficult to grow in the laboratory, and using culture independent techniques is necessary to expand our view. In this thesis, I apply metagenomics and single-cell genomics to environmental samples from ancient human remains and lakes.

First, I used metagenomics to learn about bacteria from a Neanderthal’s bone and the gut of Ötzi, a frozen natural mummy. Both were exploratory studies where the main question was what kind of bacteria are present. I found out that Streptomyces dominated this particular Neanderthal fossil, and the DNA lacked the damage that is often seen in ancient samples. Ötzi's gut sample was dominated by Clostridia and fungi belonging to Basidiomycota.

Second, ten single-cell amplified genomes of freshwater Alphaproteobacterium LD12 and three metagenomes from Swedish lakes were sequenced. Comparative metagenomics allowed hypothesizing about which functions are important for microbe proliferation in freshwater, pointing to osmoregulation and transport proteins and, possibly, to different strategies of metabolizing sugars. I also focused on SAR11 sister-groups in oceans and lakes. Phylogenies and sequence evolutionary distance estimates indicated the existence of microclusters within LD12, showing variation in abundance between lakes. The most striking difference was the relative amount of recombination compared to mutation, the estimated r/m ratio. SAR11 marine and their freshwater cousins are found at the opposite extremes of the r/m range, lowest and highest, respectively. The genetic background or sequence diversity did not explain the observed dramatic difference, so it is possibly connected to environmental adaptation or population dynamics.

In addition, I have spent a substantial amount of effort benchmarking available metagenomic methods, for example fragment recruitment of metagenomes to reference genomes.

In conclusion, my exploratory metagenomic studies have shed some light on the bacteria present in ancient human remains; comparative metagenomics has suggested the importance of substrate preference on functional differences between lakes and oceans; finally, single-cell genomes have allowed some insight into molecular evolutionary processes taking place in the freshwater LD12 bacterium. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. 108 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1067
Keyword
single-cell genomics, single cell, fossil metagenome, freshwater metagenome, LD12
National Category
Microbiology Bioinformatics and Systems Biology
Identifiers
urn:nbn:se:uu:diva-206702 (URN)978-91-554-8742-3 (ISBN)
Public defence
2013-10-18, B41, Husargatan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2013-09-25 Created: 2013-09-03 Last updated: 2014-01-23

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