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The genome of Rhizobiales bacteria in predatory ants indicates a role for urease in lifestyle switches
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
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.
Arizona State University Tempe.
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2016 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322Article in journal (Refereed) Submitted
Abstract [en]

Bacterial symbionts provide amino acids to herbivorous ants, but their role in carnivores is a puzzle. The most prevalent bacterial lineage in ants belongs to the order Rhizobiales. Sequence reads with similarity to Bartonella, a member of the Rhizobiales, were identified in the data collected in a genome project of the carnivorous ant Harpegnatos saltator. Here, we present an analysis of the closed 1.86 Mb genome of the Bartonella-like bacterium, here abbreviated Bhsal. A phylogenetic study showed that Bhsal diverged prior to the radiation of the Bartonella species. Uniquely present in the Bhsal genome is a gene for a giant protein of 6,177 amino acids with a repeated domain structure. We also identified genes for a multi- subunit urease protein complex, potentially involved in the hydrolysis of urea into ammonium. We hypothesize that the urease function protects Bhsal from the acidic environment of the ant gut. The urease genes are also present in Brucella, which has a fecal-oral transmission pathway, but they have been lost in Bartonella species, which use blood-borne transmission pathways. Taken together, the results suggest that the urease function has served an important role for transmission strategies and lifestyle changes in the host-associated members of the Rhizobiales. 

Place, publisher, year, edition, pages
Keyword [en]
symbiosis, genomics, Bartonella
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
URN: urn:nbn:se:uu:diva-301778OAI: oai:DiVA.org:uu-301778DiVA: diva2:955249
Available from: 2016-08-25 Created: 2016-08-25 Last updated: 2016-08-26
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, Daniel
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Molecular EvolutionDepartment of Medical Biochemistry and Microbiology
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