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Functionally Structured Genomes in Lactobacillus kunkeei Colonizing the Honey Crop and Food Products of Honeybees and Stingless Bees
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
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2015 (English)In: Genome Biology and Evolution, ISSN 1759-6653, Vol. 7, no 6, 1455-1473 p.Article in journal (Refereed) Published
Abstract [en]

Lactobacillus kunkeei is the most abundant bacterial species in the honey crop and food products of honeybees. The 16 S rRNA-genes of strains isolated from different bee species are nearly identical in sequence and therefore inadequate as markers for studies of coevolutionary patterns. Here, we have compared the 1.5Mb genomes of ten L. kunkeei strains isolated from all recognized Apis species and another two strains from Meliponini species. Agene flux analysis, including previously sequenced Lactobacillus species as outgroups, indicated the influence of reductive evolution. The genome architecture is unique in that vertically inherited core genes are located near the terminus of replication, whereas genes for secreted proteins and putative host-adaptive traits are located near the origin of replication. We suggest that these features have resulted from a genome-wide loss of genes, with integrations of novel genes mostly occurring in regions flanking the origin of replication. The phylogenetic analyses showed that the bacterial topology was incongruent with the host topology, and that strains of the same microcluster have recombined frequently across the host species barriers, arguing against codiversification. Multiple genotypes were recovered in the individual hosts and transfers of mobile elements could be demonstrated for strains isolated from the same host species. Unlike other bacteria with small genomes, short generation times and multiple rRNA operons suggest that L. kunkeei evolves under selection for rapid growth in its natural growth habitat. The results provide an extended framework for reductive genome evolution and functional genome organization in bacteria.

Place, publisher, year, edition, pages
2015. Vol. 7, no 6, 1455-1473 p.
Keyword [en]
genome organization, Lactobacillus kunkeei, honeybee, genome reduction, recombination
National Category
Biological Sciences
URN: urn:nbn:se:uu:diva-261322DOI: 10.1093/gbe/evv079ISI: 000358800100005PubMedID: 25953738OAI: oai:DiVA.org:uu-261322DiVA: diva2:850881
Available from: 2015-09-02 Created: 2015-09-01 Last updated: 2016-08-26Bibliographically 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: 2016-10-11

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