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Genome Evolution of a Bee- Associated Bacterium Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1953 Genome evolution of a bee- associated bacterium ANDREA GARCÍA-MONTANER ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 ISBN 978-91-513-0986-6 UPPSALA urn:nbn:se:uu:diva-416847 2020 Dissertation presented at Uppsala University to be publicly examined in A1:111a, Biomedicinskt centrum (BMC), Husargatan 3, Uppsala, Thursday, 24 September 2020 at 09:15 for the degree of Doctor of Philosophy. The examination will be conducted in English. Faculty examiner: Professor Matthias Horn (Department of Microbial Ecology and Ecosystem Science, Division of Microbial Ecology). Abstract García-Montaner, A. 2020. Genome evolution of a bee-associated bacterium. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1953. 80 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-0986-6. The use of large-scale comparative genomics allows us to explore the genetic diversity and mechanisms of evolution of related organisms. This thesis has focused on the application of such approaches to study Lactobacillus kunkeei, a bacterial inhabitant of the honeybee gut. We produced 102 novel complete genomes from L. kunkeei, which were used in four large comparative studies. In the first study, 41 bacterial strains were isolated from the crop of honeybees whose populations were geographically isolated. Their genome sequences revealed differences in gene contents, including the mobilome, which were mostly phylogroup- specific. However, differences in strain diversity and co-occurrence between both locations were observed. In the second study, we obtained 61 bacterial isolates from neighboring hives at different timepoints during the summer. We observed that strain diversity seemed hive- specific and relatively constant in time. Surprisingly, the observed mobilome also showed hive specificity and was maintained through the summer. The novel genome data were combined with previously published genomes, allowing us to perform deep comparative analyses on the evolution of the species using a total of 126 genomes. We determined that, despite the large number of sequenced genomes, L. kunkeei has an open pangenome. Besides, we evaluated the effects of recombination on the species core genome, and concluded that it mainly evolves through mutation events. In the last study we described the mechanisms of evolution of a cluster of 5 giant genes (about 90 kb long in total) that are unique to L. kunkeei and the closest sister species. Their patterns of evolution do not reflect those of the species core genome. We concluded that they originated by duplication events, and have diverged by accumulation of both mutations and recombination events. We predicted a potential interaction between the proteins encoded by two of them, and we hypothesized a role in host-specific interaction for another protein. In conclusion, these studies have provided novel and cohesive knowledge on the composition and dynamics of different populations of L. kunkeei, and may have contributed to better understand its ecological niche. Keywords: Bacterial evolution, Genomics, Symbiosis, Honeybees Andrea García-Montaner, Department of Cell and Molecular Biology, Molecular Evolution, Box 596, Uppsala University, SE-752 37 Uppsala, Sweden. © Andrea García-Montaner 2020 ISSN 1651-6214 ISBN 978-91-513-0986-6 urn:nbn:se:uu:diva-416847 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-416847) Para los que más quiero. Cover art by Tomás Montaner Carbó, my dear grandpa, who beautifully captured the dynamic nature of bacterial genomes (front) and the incredible diversity enclosed within a single species (back), two key aspects of this doctoral thesis. List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Garcia-Montaner, A., Tamarit, D., Näslund, K., Webster, M.T., Andersson, S.G.E. (2020) Comparative genomics of Lactobacil- lus kunkeei in two insular populations of honeybees. Manuscript. II Garcia-Montaner, A.*, Dyrhage, K.*, Näslund, K., Vasquez, A., Andersson, S.G.E. (2020). Strain diversity and evolution of Lactobacillus kunkeei throughout the summer months. Manu- script. III Garcia-Montaner, A.*, Tamarit, D.*, Andersson, S.G.E. (2020) Role of recombination and mutation to the evolution of the core genome in Lactobacillus kunkeei. Manuscript. IV Garcia-Montaner, A., Andersson, S.G.E. (2020). Molecular evolution of giant genes in Lactobacillus bacteria isolated from social bees. Manuscript. (*) Equal contribution Reprints were made with permission from the respective publishers. Contents Introduction to this thesis ...........................................................................11 Chapter 1: Genome evolution in bacteria ...................................................12 Genomic organization ...........................................................................12 Sources of genetic innovation ................................................................14 Birth of new genes ............................................................................14 Nucleotide substitutions ....................................................................14 Duplications, deletions and rearrangements .......................................15 Horizontal gene transfer ....................................................................15 Recombination .................................................................................17 Forces of evolution................................................................................19 Chapter 2: Host-microbe systems ...............................................................20 Host-associated lifestyles ......................................................................21 Genome reduction .................................................................................22 Surface interaction in bacterial symbionts..............................................23 Animal microbiomes .............................................................................28 Bacterial composition .......................................................................29 Beneficial roles of the microbiota .....................................................30 Model systems for microbiota studies ...............................................31 Chapter 3: The honeybee as a model system ..............................................33 Ecology and nutrition ............................................................................33 Health and disease.................................................................................34 Gut microbiota ......................................................................................35 Chapter 4: Lactobacillus kunkeei ...............................................................39 Taxonomic context: The genus Lactobacillus ........................................39 Evolutionary context .............................................................................41 Ecological context .................................................................................43 Potential symbiotic role ....................................................................43 Metabolic profile ...................................................................................45 Genomic traits .......................................................................................48 Aims .........................................................................................................51 Results ......................................................................................................52 Paper I ..................................................................................................52 Paper II .................................................................................................53 Paper III ................................................................................................55 Paper IV................................................................................................56 Perspectives...............................................................................................58 Svensk sammanfattning .............................................................................61 Resumen en español ..................................................................................63 Acknowledgements ...................................................................................66 References .................................................................................................70 Abbreviations 6-PG/PK 6-phosphogluconate/phosphoketolase ADH Alcohol dehydrogenase ALDH Acetaldehyde dehydrogenase AMP Antimicrobial peptides ANI Average nucleotide identity CCD Colony collapse disorder dN Non-synonymous nucleotide substitution rate dS Synonymous nucleotide substitutions rate EMP Embden-Meyerhof-Parnas FLAB Fructophilic lactic acid bacteria HGT Horizontal gene transfer LAB Lactic acid bacteria MEP Methylerythritol 4-phosphate MGE Mobile genetic element MVA Mevalonate MYA Million years ago r/m Recombination rate over mutation rate Introduction to this thesis - Life is hard, Mr. Scoresby, but we cling to it all the same. - And this journey we’re on? Is that folly or wisdom? - The greatest wisdom I know. ― Philip Pullman, His Dark Materials I have been fascinated by the animal world since an early age. As you probably guessed, I wanted to become a vet.
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