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Functionally structured genome architectures in Lactobacillus – insights into their variability and 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.
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.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Bacterial genome architectures evolve in response to selective pressures on the interplay between replication and gene expression. Several genomes contain a higher fraction of genes coding for proteins involved in information processes near the origin of replication, which is thought to be due to selection for rapid growth. We recently described a novel type of genome architecture in Lactobacillus kunkeei (Tamarit, et al. 2015). In this genome, vertically inherited genes encoding proteins with roles in translation and replication have accumulated in the chromosomal half surrounding the terminus of replication, while species-specific genes, and genes encoding proteins with metabolic and transport functions have accumulated in the chromosomal half around the origin of replication. Here, we show that this pattern is present also in the closest relatives of L. kunkeei, and similar but not identical biased genome architectures are present in other groups within the Lactobacillaceae. Thus, the biased genome structure in L. kunkeei has emerged from an ancestral clustering of vertically inherited genes around the terminus of replication, while horizontally acquired genes have been inserted near the origin of replication. The genome bias has been lost independently in several groups due to insertions of mobile elements near the terminus of replication and/or major genome rearrangements. We propose chromosomal structuring in macrodomains in the Lactobacillaceae, and suggest that further exploration of its functional consequences and generality will provide valuable insights into the forces that shape genome organization in bacteria. 

Keyword [en]
genome organization, replication axis
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
URN: urn:nbn:se:uu:diva-301781OAI: oai:DiVA.org:uu-301781DiVA: diva2:955251
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.
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: 2016-09-22

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