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Phylogenomics of Oceanic Bacteria
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
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 [en]
phylogenetics, SAR11, mitochondria
National Category
Evolutionary Biology Bioinformatics and Systems Biology
Identifiers
URN: urn:nbn:se:uu:diva-208441ISBN: 978-91-554-8767-6 (print)OAI: oai:DiVA.org:uu-208441DiVA: diva2:652587
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
List of papers
1. Origin and evolution of the mitochondrial aminoacyl-tRNA synthetases
Open this publication in new window or tab >>Origin and evolution of the mitochondrial aminoacyl-tRNA synthetases
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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.

Keyword
Aminoacyl-tRNA synthetase, Mitochondria, Phylogeny
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-14983 (URN)10.1093/molbev/msl202 (DOI)000244662000013 ()17182897 (PubMedID)
Available from: 2008-02-01 Created: 2008-02-01 Last updated: 2017-12-11Bibliographically approved
2. A Phylometagenomic Exploration of Oceanic Alphaproteobacteria Reveals Mitochondrial Relatives Unrelated to the SAR11 Clade
Open this publication in new window or tab >>A Phylometagenomic Exploration of Oceanic Alphaproteobacteria Reveals Mitochondrial Relatives Unrelated to the SAR11 Clade
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2011 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 6, no 9, e24457- p.Article in journal (Refereed) Published
Abstract [en]

Background: According to the endosymbiont hypothesis, the mitochondrial system for aerobic respiration was derived from an ancestral Alphaproteobacterium. Phylogenetic studies indicate that the mitochondrial ancestor is most closely related to the Rickettsiales. Recently, it was suggested that Candidatus Pelagibacter ubique, a member of the SAR11 clade that is highly abundant in the oceans, is a sister taxon to the mitochondrial-Rickettsiales clade. The availability of ocean metagenome data substantially increases the sampling of Alphaproteobacteria inhabiting the oxygen-containing waters of the oceans that likely resemble the originating environment of mitochondria.

Methodology/Principal Findings: We present a phylogenetic study of the origin of mitochondria that incorporates metagenome data from the Global Ocean Sampling (GOS) expedition. We identify mitochondrially related sequences in the GOS dataset that represent a rare group of Alphaproteobacteria, designated OMAC (Oceanic Mitochondria Affiliated Clade) as the closest free-living relatives to mitochondria in the oceans. In addition, our analyses reject the hypothesis that the mitochondrial system for aerobic respiration is affiliated with that of the SAR11 clade.

Conclusions/Significance: Our results allude to the existence of an alphaproteobacterial clade in the oxygen-rich surface waters of the oceans that represents the closest free-living relative to mitochondria identified thus far. In addition, our findings underscore the importance of expanding the taxonomic diversity in phylogenetic analyses beyond that represented by cultivated bacteria to study the origin of mitochondria.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-159787 (URN)10.1371/journal.pone.0024457 (DOI)000295039700022 ()
Available from: 2011-10-10 Created: 2011-10-10 Last updated: 2017-12-08Bibliographically approved
3. Independent Genome Reduction and Phylogenetic Reclassification of the Oceanic SAR11 Clade
Open this publication in new window or tab >>Independent Genome Reduction and Phylogenetic Reclassification of the Oceanic SAR11 Clade
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.

Keyword
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:nbn:se:uu:diva-165703 (URN)10.1093/molbev/msr203 (DOI)000299129000013 ()21900598 (PubMedID)
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
4. Single cell genomics reveals low recombination frequencies in freshwater bacteria of the SAR11 clade
Open this publication in new window or tab >>Single cell genomics reveals low recombination frequencies in freshwater bacteria of the SAR11 clade
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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.

National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-206203 (URN)10.1186/gb-2013-14-11-r130 (DOI)000330616200009 ()24286338 (PubMedID)
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
5. Comparative and Phylogenomic Evidence that the Alphaproteobacterium HIMB59 is not a Member of the Oceanic SAR11 Clade
Open this publication in new window or tab >>Comparative and Phylogenomic Evidence that the Alphaproteobacterium HIMB59 is not a Member of the Oceanic SAR11 Clade
2013 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 11, e78858- p.Article in journal (Refereed) Published
Abstract [en]

SAR11 is a globally abundant group of Alphaproteobacteria in the oceans that is taxonomically not well defined. It has been suggested SAR11 should be classified into the novel order Pelagibacterales. Features such as conservation of gene content and synteny have been taken as evidence that also the divergent member HIMB59 should be included in the order. However, this proposition is controversial since phylogenetic analyses have questioned the monophyly of this grouping. Here, we performed phylogenetic analyses and reinvestigated the genomic similarity of SAR11 and HIMB59. Our phylogenetic analysis confirmed that HIMB59 is not a sister group to the other SAR11 strains. By placing the comparison in the context of the evolution of the Alphaproteobacteria, we found that none of the measures of genomic similarity supports a clustering of HIMB59 and SAR11 to the exclusion of other Alphaproteobacteria. First, pairwise sequence similarity measures for the SAR11 and HIMB59 genomes were within the range observed for unrelated pairs of Alphaproteobacteria. Second, pairwise comparisons of gene contents revealed a higher similarity of SAR11 to several other alphaproteobacterial genomes than to HIMB59. Third, the SAR11 genomes are not more similar in gene order to the HIMB59 genome than what they are to several other alphaproteobacterial genomes. Finally, in contrast to earlier reports, we observed no sequence similarity between the hypervariable region HVR2 in the SAR11 genomes and the region located at the corresponding position in the HIMB59 genome. Based on these observations, we conclude that the alphaproteobacterium HIMB59 is not monophyletic with the SAR11 strains and that genome streamlining has evolved multiple times independently in Alphaproteobacteria adapted to the upper surface waters of the oceans.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-208438 (URN)10.1371/journal.pone.0078858 (DOI)000326499300036 ()
Available from: 2013-10-01 Created: 2013-10-01 Last updated: 2017-12-06Bibliographically approved
6. On the importance of taxonomically representative groups for the inference of adaptive traits in surface oceanic bacteria
Open this publication in new window or tab >>On the importance of taxonomically representative groups for the inference of adaptive traits in surface oceanic bacteria
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-208439 (URN)
Available from: 2013-10-01 Created: 2013-10-01 Last updated: 2013-11-06
7. New protein functions evolve by expansion of ancestral fold architectures and evolution of disordered proteins de novo
Open this publication in new window or tab >>New protein functions evolve by expansion of ancestral fold architectures and evolution of disordered proteins de novo
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-208436 (URN)
Available from: 2013-10-01 Created: 2013-10-01 Last updated: 2013-11-06

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