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Switches in Genomic GC Content Drive Shifts of Optimal Codons under Sustained Selection on Synonymous Sites
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.
2016 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653Article in journal (Refereed) Published
Abstract [en]

The major codon preference model suggests that codons read by tRNAs in high concentrations are preferentially utilized in highly expressed genes. However, the identity of the optimal codons differs between species although the forces driving such changes are poorly understood. We suggest that these questions can be tackled by placing codon usage studies in a phylogenetic framework and that bacterial genomes with extreme nucleotide composition biases provide informative model systems. Switches in the background substitution biases from GC to AT have occurred in Gardnerella vaginalis (GC = 32%), and from AT to GC in Lactobacillus delbrueckii (GC=62%) and Lactobacillus fermentum (GC = 63%). We show that despite the large effects on codon usage patterns by these switches, all three species evolve under selection on synonymous sites. In G. vaginalis, the dramatic codon frequency changes coincide with shifts of optimal codons. In contrast, the optimal codons have not shifted in the two Lactobacillus genomes despite an increased fraction of GC-ending codons. We suggest that all three species are in different phases of an on-going shift of optimal codons, and attribute the difference to a stronger background substitution bias and/or longer time since the switch in G. vaginalis. We show that comparative and correlative methods for optimal codon identification yield conflicting results for genomes in flux and discuss possible reasons for the mispredictions. We conclude that switches in the direction of the background substitution biases can drive major shifts in codon preference patterns even under sustained selection on synonymous codon sites.

Place, publisher, year, edition, pages
Keyword [en]
Codon Usage, Lactobacillus, Bifidobacterium, GC content
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
URN: urn:nbn:se:uu:diva-300909DOI: 10.1093/gbe/evw201OAI: oai:DiVA.org:uu-300909DiVA: diva2:952853
Available from: 2016-08-15 Created: 2016-08-15 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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Publisher's full texthttp://gbe.oxfordjournals.org/content/early/2016/08/13/gbe.evw201

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