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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.ORCID iD: F-4815-2016
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
University of Lausanne.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Gene transfer agents (GTAs) are bacteriophage particles that transfer bacterial DNA. Two GTAs have been identified in the Alphaproteobacteria: the RcGTA, which is widely distributed in a broad range of species; and the more recently evolved BaGTA, which is thought to have been important for the explosive radiation of the genus Bartonella. The BaGTA preferentially packages genes for host interaction factors amplified from an alternative, phage-derived origin of replication. Here, we show that the RcGTAs and the BaGTAs have non-overlapping phyletic distribution patterns in the Alphaproteobacteria. We identify BaGTA-like phage islands in Candidatus Tokpelaia hoelldoblerii, an early diverging lineage of Bartonella, as well as in three more distantly related alphaproteobacterial species. Moreover, we identify several BaGTA-like phage islands within the genus Bartonella, but unlike the BaGTA these are not conserved in either occurrence or genomic location. We thus hypothesize that the transfer of random DNA fragments with the aid of the GTA was an early innovation, which predated the amplification and targeted transfer of DNA segments flanking the phage-derived origin of replication. We propose a model for the gradual transformation of a prophage into a specialist GTA in a process driven by selection for transfer and recombination of host interaction factors within the bacterial population. 

Keyword [en]
mobile elements, Phage domestication, GTA
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
URN: urn:nbn:se:uu:diva-301779OAI: oai:DiVA.org:uu-301779DiVA: diva2:955250
Available from: 2016-08-25 Created: 2016-08-25 Last updated: 2016-08-31Bibliographically 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. 96 p.
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1415
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
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)
Available from: 2016-09-22 Created: 2016-08-25 Last updated: 2016-09-22

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