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Genome Evolution of Bartonellaceae Symbionts of Ants at the Opposite Ends of the Trophic Scale
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.
Harvard Univ, Dept Organism & Evolutionary Biol, Cambridge, MA 02138 USA.
Drexel Univ, Dept Biol, Philadelphia, PA 19104 USA.
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2018 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 10, no 7, p. 1687-1704Article in journal (Refereed) Published
Abstract [en]

Many insects rely on bacterial symbionts to supply essential amino acids and vitamins that are deficient in their diets, but metabolic comparisons of closely related gut bacteria in insects with different dietary preferences have not been performed. Here, we demonstrate that herbivorous ants of the genus Dolichoderus from the Peruvian Amazon host bacteria of the family Bartonellaceae, known for establishing chronic or pathogenic infections in mammals. We detected these bacteria in all studied Dolichoderus species, and found that they reside in the midgut wall, that is, the same location as many previously described nutritional endosymbionts of insects. The genomic analysis of four divergent strains infecting different Dolichoderus species revealed genes encoding pathways for nitrogen recycling and biosynthesis of several vitamins and all essential amino acids. In contrast, several biosynthetic pathways have been lost, whereas genes for the import and conversion of histidine and arginine to glutamine have been retained in the genome of a closely related gut bacterium of the carnivorous ant Harpegnathos saltator. The broad biosynthetic repertoire in Bartonellaceae of herbivorous ants resembled that of gut bacteria of honeybees that likewise feed on carbohydrate-rich diets. Taken together, the broad distribution of Bartonellaceae across Dolichoderus ants, their small genome sizes, the specific location within hosts, and the broad biosynthetic capability suggest that these bacteria are nutritional symbionts in herbivorous ants. The results highlight the important role of the host nutritional biology for the genomic evolution of the gut microbiota-and conversely, the importance of the microbiota for the nutrition of hosts.

Place, publisher, year, edition, pages
Oxford University Press, 2018. Vol. 10, no 7, p. 1687-1704
Keywords [en]
ants, bacteria, genomics, molecular evolution, nutritional symbionts
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-364009DOI: 10.1093/gbe/evy126ISI: 000442378100006PubMedID: 29982531OAI: oai:DiVA.org:uu-364009DiVA, id: diva2:1259687
Funder
Swedish Research Council, 349-2007-8732 621-2014-4460Knut and Alice Wallenberg Foundation, 2011.0148 2012.0075Available from: 2018-10-30 Created: 2018-10-30 Last updated: 2018-10-30Bibliographically approved

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Neuvonen, Minna M.Andersson, Siv G. E.

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