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Evolution of streamlined genomes in ultra-small aquatic bacteria
Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för cell- och molekylärbiologi, Molekylär evolution.
2019 (Engelska)Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
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.

Ort, förlag, år, upplaga, sidor
Uppsala: Uppsala universitet, 2019. , s. 48
Serie
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1857
Nyckelord [en]
streamlined genome, aquatic bacteria, single cell genomics, metagenomics, evolutionary genomics, salinity, Baltic Sea
Nationell ämneskategori
Evolutionsbiologi
Forskningsämne
Biologi med inriktning mot molekylär evolution
Identifikatorer
URN: urn:nbn:se:uu:diva-393351ISBN: 978-91-513-0755-8 (tryckt)OAI: oai:DiVA.org:uu-393351DiVA, id: diva2:1352843
Disputation
2019-11-07, B41, Biomedicinskt centrum (BMC), Husargatan 3, Uppsala, 13:15 (Engelska)
Opponent
Handledare
Tillgänglig från: 2019-10-15 Skapad: 2019-09-20 Senast uppdaterad: 2019-11-12
Delarbeten
1. Single cell genomics reveals low recombination frequencies in freshwater bacteria of the SAR11 clade
Öppna denna publikation i ny flik eller fönster >>Single cell genomics reveals low recombination frequencies in freshwater bacteria of the SAR11 clade
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2013 (Engelska)Ingår i: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 14, nr 11, artikel-id R130Artikel i tidskrift (Refereegranskat) 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.

Nationell ämneskategori
Mikrobiologi
Identifikatorer
urn:nbn:se:uu:diva-206203 (URN)10.1186/gb-2013-14-11-r130 (DOI)000330616200009 ()24286338 (PubMedID)
Forskningsfinansiär
Vetenskapsrådet, 349-2007-831 621-2008-3259 621-2011-4669-4669 2009-3784 2008-1923 2012-3892EU, Europeiska forskningsrådetGöran Gustafssons Stiftelse för främjande av vetenskaplig forskning vid Uppsala universitet och Kungl tekniska högskolan (UU/KTH)Knut och Alice Wallenbergs Stiftelse, KAW-2011.0148 KAW-2012.0075Swedish National Infrastructure for Computing (SNIC), p2006019 p2009043
Tillgänglig från: 2013-09-03 Skapad: 2013-08-29 Senast uppdaterad: 2019-09-20Bibliografiskt granskad
2. Rapid diversification of functional homologs in replacement genomic islands of freshwater Actinobacteria
Öppna denna publikation i ny flik eller fönster >>Rapid diversification of functional homologs in replacement genomic islands of freshwater Actinobacteria
(Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
Nationell ämneskategori
Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-393357 (URN)
Tillgänglig från: 2019-09-19 Skapad: 2019-09-19 Senast uppdaterad: 2019-09-26
3. Evolution of subclass Candidatus Actinomarinidae inferred from single-cell amplified genomes of saltwater Actinobacteria
Öppna denna publikation i ny flik eller fönster >>Evolution of subclass Candidatus Actinomarinidae inferred from single-cell amplified genomes of saltwater Actinobacteria
(Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
Nationell ämneskategori
Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-393359 (URN)
Tillgänglig från: 2019-09-19 Skapad: 2019-09-19 Senast uppdaterad: 2019-09-23
4. A phylometagenomic study based on single-cell amplified genomes from Actinobacteria in the brackish waters of the Baltic Sea
Öppna denna publikation i ny flik eller fönster >>A phylometagenomic study based on single-cell amplified genomes from Actinobacteria in the brackish waters of the Baltic Sea
Visa övriga...
(Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
Nationell ämneskategori
Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-393361 (URN)
Tillgänglig från: 2019-09-19 Skapad: 2019-09-19 Senast uppdaterad: 2019-09-26

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