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Origin and evolution of the Bartonella Gene Transfer Agent
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.ORCID iD: 0000-0002-4940-719X
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
University of Lausanne.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.ORCID iD: 0000-0001-8354-2398
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2018 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 2, p. 451-464Article in journal (Refereed) Published
Abstract [en]

Gene transfer agents (GTAs) are domesticated bacteriophages that have evolved into molecular machines for the transferof bacterial DNA. Despite their widespread nature and their biological implications, the mechanisms and selective forcesthat drive the emergence of GTAs are still poorly understood. Two GTAs have been identifiedintheAlphaproteobacteria:the RcGTA, which is widely distributed in a broad range of species; and the BaGTA, which has a restricted host range thatincludes vector-borne intracellular bacteria of the genusBartonella. The RcGTA packages chromosomal DNA randomly,whereas the BaGTA particles contain a relatively higher fraction of genes for host interaction factors that are amplifiedfrom a nearby phage-derived origin of replication. In this study, we compare the BaGTA genes with homologous bac-teriophage genes identified in the genomes ofBartonellaspecies and close relatives. Unlike the BaGTA, the prophagegenes are neither present in all species, nor inserted into homologous genomic sites. Phylogenetic inferences and sub-stitution frequency analyses confirm codivergence of the BaGTA with the host genome, as opposed to multiple integra-tion and recombination events in the prophages. Furthermore, the organizationof segments flanking the BaGTA differsfrom that of the prophages by a few rearrangement events,which have abolished the normal coordination betweenphage genome replication and phage gene expression. Based on the results of our comparative analysis, we propose amodel for how a prophage may be transformed into a GTA that transfers amplified bacterial DNA segments.

Place, publisher, year, edition, pages
2018. Vol. 35, no 2, p. 451-464
Keyword [en]
mobile elements, Phage domestication, GTA
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
URN: urn:nbn:se:uu:diva-301779DOI: 10.1093/molbev/msx299ISI: 000423713100014PubMedID: 29161442OAI: oai:DiVA.org:uu-301779DiVA, id: diva2:955250
Funder
Swedish Research Council, 349-2007-8732, 621-2014-4460Knut and Alice Wallenberg Foundation, 2011.0148, 2012.0075
Available from: 2016-08-25 Created: 2016-08-25 Last updated: 2018-03-20Bibliographically approved
In thesis
1. Evolution of symbiotic lineages and the origin of new traits
Open this publication in new window or tab >>Evolution of symbiotic lineages and the origin of new traits
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

This thesis focuses on the genomic study of symbionts of two different groups of hymenopterans: bees and ants. Both groups of insects have major ecological impact, and investigating their microbiomes increases our understanding of their health, diversity and evolution.

The study of the bee gut microbiome, including members of Lactobacillus and Bifidobacterium, revealed genomic processes related to the adaptation to the gut environment, such as the expansion of genes for carbohydrate metabolism and the acquisition of genes for interaction with the host. A broader genomic study of these genera demonstrated that some lineages evolve under strong and opposite substitution biases, leading to extreme GC content values. A comparison of codon usage patterns in these groups revealed ongoing shifts of optimal codons.

In a separate study we analysed the genomes of several strains of Lactobacillus kunkeei, which inhabits the honey stomach of bees but is not found in their gut. We observed signatures of genome reduction and suggested candidate genes for host-interaction processes. We discovered a novel type of genome architecture where genes for metabolic functions are located in one half of the genome, whereas genes for information processes are located in the other half. This genome organization was also found in other Lactobacillus species, indicating that it was an ancestral feature that has since been retained. We suggest mechanisms and selective forces that may cause the observed organization, and describe processes leading to its loss in several lineages independently.

We also studied the genome of a species of Rhizobiales bacteria found in ants. We discuss its metabolic capabilities and suggest scenarios for how it may affect the ants’ lifestyle. This genome contained a region with homology to the Bartonella gene transfer agent (GTA), which is a domesticated bacteriophage used to transfer bacterial DNA between cells. We propose that its unique behaviour as a specialist GTA, preferentially transferring host-interaction factors, originated from a generalist GTA that transferred random segments of chromosomal DNA.

These bioinformatic analyses of previously uncharacterized bacterial lineages have increased our understanding of their physiology and evolution and provided answers to old and new questions in fundamental microbiology.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2016. p. 96
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1415
Keyword
symbiosis, host-association, Lactobacillus, Bifidobacterium, Rhizobiales, Bartonella, honeybees, ants, codon usage bias, genome architecture, genome organization, gene transfer agent, evolutionary genomics, comparative genomics
National Category
Evolutionary Biology Genetics Microbiology
Research subject
Biology with specialization in Molecular Evolution; Biology with specialization in Evolutionary Genetics; Biology with specialization in Microbiology
Identifiers
urn:nbn:se:uu:diva-301939 (URN)978-91-554-9672-2 (ISBN)
Public defence
2016-10-14, B41, Biomedical Center (BMC), Husargatan 3, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2016-09-22 Created: 2016-08-25 Last updated: 2016-10-11

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Tamarit, DanielNeuvonen, Minna M.Guy, LionelAndersson, Siv G. E.

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