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Evolution of streamlined genomes in ultra-small aquatic bacteria
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

This thesis investigates the evolutionary processes of streamlined genomes from aquatic bacteria adapting to different salinities, using two groups of ultra-small aquatic bacteria (LD12 Alphaproteobacteria and acI Actinobacteria). Due to difficulties in obtaining pure cultures of these bacteria, culture-free approaches (single-cell genomics and metagenomics) were used to construct and compare genomes, and to study the mechanisms and selective forces of adaptation to freshwater, brackish, and marine ecosystems.

A study of single-cell amplified genomes (SAGs) from freshwater LD12 Alphaproteobacteria revealed that LD12 forms a clade embedded within the globally dominant marine Alphaproteobacteria SAR11, and subclades were organized into distinct microclusters. LD12 genomes had a very low ratio of recombination to point mutations, in contrast to their marine relatives which had a very high ratio of recombination to mutation. We suggested that the transition from marine to freshwater was a bottleneck event, resulting in reduced opportunities for recombination.

In a separate study, we analyzed complete genomes and SAGs from acI Actinobacteria abundant in freshwater ecosystems, and found overall low rates of sequence divergence with however a dramatic acceleration near genomic island 1 (GI-1). We also identified a type IV topoisomerase, the delta subunit of DNA polymerase, and an RNA polymerase sigma factor near GI-1. Based on these results, we proposed a model for the evolution and expression of novel genes in these genomes.

We also isolated and analyzed the genomes of single cells from a marine Actinobacteria (subclass Candidatus Actinomarinidae). These were not related to acI, but to Acidimicrobiia, which suggested salinity barriers have been crossed several times by Actinobacteria.

To further understand the transition to different salinities, we obtained acI SAGs from three different intermediate-salinity Baltic Sea locations. We took sequence reads from 21 metagenomes taken along the salinity gradient, and recruited these fragments to both the freshwater and brackish acI reference genomes. These results indicated that transitions between fresh and brackish waters have occurred multiple times in acI Actinobacteria and some of these strains are globally present in coastal waters.

Place, publisher, year, edition, pages
Uppsala: Uppsala universitet, 2019. , p. 48
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1857
Keywords [en]
streamlined genome, aquatic bacteria, single cell genomics, metagenomics, evolutionary genomics, salinity, Baltic Sea
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
URN: urn:nbn:se:uu:diva-393351ISBN: 978-91-513-0755-8 (print)OAI: oai:DiVA.org:uu-393351DiVA, id: diva2:1352843
Public defence
2019-11-07, B41, Biomedicinskt centrum (BMC), Husargatan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2019-10-15 Created: 2019-09-20 Last updated: 2019-11-12
List of papers
1. 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, article id 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: 2019-09-20Bibliographically approved
2. Rapid diversification of functional homologs in replacement genomic islands of freshwater Actinobacteria
Open this publication in new window or tab >>Rapid diversification of functional homologs in replacement genomic islands of freshwater Actinobacteria
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-393357 (URN)
Available from: 2019-09-19 Created: 2019-09-19 Last updated: 2019-09-26
3. Evolution of subclass Candidatus Actinomarinidae inferred from single-cell amplified genomes of saltwater Actinobacteria
Open this publication in new window or tab >>Evolution of subclass Candidatus Actinomarinidae inferred from single-cell amplified genomes of saltwater Actinobacteria
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-393359 (URN)
Available from: 2019-09-19 Created: 2019-09-19 Last updated: 2019-09-23
4. A phylometagenomic study based on single-cell amplified genomes from Actinobacteria in the brackish waters of the Baltic Sea
Open this publication in new window or tab >>A phylometagenomic study based on single-cell amplified genomes from Actinobacteria in the brackish waters of the Baltic Sea
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-393361 (URN)
Available from: 2019-09-19 Created: 2019-09-19 Last updated: 2019-09-26

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