1. |
- Ellegaard, Kirsten M., et al.
(author)
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Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut
- 2015
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In: BMC Genomics. - : Springer Science and Business Media LLC. - 1471-2164. ; 16
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Journal article (peer-reviewed)abstract
- Background: In the honeybee Apis mellifera, the bacterial gut community is consistently colonized by eight distinct phylotypes of bacteria. Managed bee colonies are of considerable economic interest and it is therefore important to elucidate the diversity and role of this microbiota in the honeybee. In this study, we have sequenced the genomes of eleven strains of lactobacilli and bifidobacteria isolated from the honey crop of the honeybee Apis mellifera. Results: Single gene phylogenies confirmed that the isolated strains represent the diversity of lactobacilli and bifidobacteria in the gut, as previously identified by 16S rRNA gene sequencing. Core genome phylogenies of the lactobacilli and bifidobacteria further indicated extensive divergence between strains classified as the same phylotype. Phylotype-specific protein families included unique surface proteins. Within phylotypes, we found a remarkably high level of gene content diversity. Carbohydrate metabolism and transport functions contributed up to 45% of the accessory genes, with some genomes having a higher content of genes encoding phosphotransferase systems for the uptake of carbohydrates than any previously sequenced genome. These genes were often located in highly variable genomic segments that also contained genes for enzymes involved in the degradation and modification of sugar residues. Strain-specific gene clusters for the biosynthesis of exopolysaccharides were identified in two phylotypes. The dynamics of these segments contrasted with low recombination frequencies and conserved gene order structures for the core genes. Hits for CRISPR spacers were almost exclusively found within phylotypes, suggesting that the phylotypes are associated with distinct phage populations. Conclusions: The honeybee gut microbiota has been described as consisting of a modest number of phylotypes; however, the genomes sequenced in the current study demonstrated a very high level of gene content diversity within all three described phylotypes of lactobacilli and bifidobacteria, particularly in terms of metabolic functions and surface structures, where many features were strain-specific. Together, these results indicate niche differentiation within phylotypes, suggesting that the honeybee gut microbiota is more complex than previously thought.
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2. |
- Ling, Jiaxin, et al.
(author)
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Evolution and postglacial colonization of Seewis hantavirus with Sorex araneus in Finland
- 2018
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In: Infection, Genetics and Evolution. - : Elsevier BV. - 1567-1348 .- 1567-7257. ; 57, s. 88-97
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Journal article (peer-reviewed)abstract
- Hantaviruses have co-existed with their hosts for millions of years. Seewis virus (SWSV), a soricomorph-borne hantavirus, is widespread in Eurasia, ranging from Central Siberia to Western Europe. To gain insight into the phylogeography and evolutionary history of SWSV in Finland, lung tissue samples of 225 common shrews (Sorex araneus) trapped from different parts of Finland were screened for the presence of SWSV RNA. Forty-two of the samples were positive. Partial small (S), medium (M) and large (L) segments of the virus were sequenced, and analyzed together with all SWSV sequences available in Genbank. The phylogenetic analysis of the partial S-segment sequences suggested that all Finnish SWSV strains shared their most recent common ancestor with the Eastern European strains, while the L-segment suggested multiple introductions. The difference between the Land S-segment phylogenies implied that reassortment events play a role in the evolution of SWSV. Of the Finnish strains, variants from Eastern Finland occupied the root position in the phylogeny, and had the highest genetic diversity, supporting the hypothesis that SWSV reached Finland first form the east. During the spread in Finland, the virus has formed three separate lineages, identified here by correlation analysis of genetic versus geographic distance combined with median-joining network analysis. These results support the hypothesis that Finnish SWSV recolonized Finland with its host, the common shrew, from east after the last ice age 12,000-8000 years ago, and then subsequently spread along emerging land bridges towards west or north with the migration and population expansion of its host.
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3. |
- Neuvonen, Minna M., et al.
(author)
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The genome of Rhizobiales bacteria in predatory ants reveals urease gene functions but no genes for nitrogen fixation
- 2016
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In: Scientific Reports. - : Springer Science and Business Media LLC. - 2045-2322. ; 6, s. 1-11
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Journal article (peer-reviewed)abstract
- Gut-associated microbiota of ants include Rhizobiales bacteria with affiliation to the genus Bartonella. These bacteria may enable the ants to fix atmospheric nitrogen, but no genomes have been sequenced yet to test the hypothesis. Sequence reads from a member of the Rhizobiales were identified in the data collected in a genome project of the ant Harpegnathos saltator. We present an analysis of the closed 1.86 Mb genome of the ant-associated bacterium, for which we suggest the species name Candidatus Tokpelaia hoelldoblerii. A phylogenetic analysis reveals a relationship to Bartonella and Brucella, which infect mammals. Novel gene acquisitions include a gene for a putative extracellular protein of more than 6,000 amino acids secreted by the type I secretion system, which may be involved in attachment to the gut epithelium. No genes for nitrogen fixation could be identified, but genes for a multi-subunit urease protein complex are present in the genome. The urease genes are also present in Brucella, which has a fecal-oral transmission pathway, but not in Bartonella, which use blood-borne transmission pathways. We hypothesize that the gain and loss of the urease function is related to transmission strategies and lifestyle changes in the host-associated members of the Rhizobiales.
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4. |
- Ponce-de-Leon, Miguel, et al.
(author)
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Determinism and Contingency Shape Metabolic Complementation in an Endosymbiotic Consortium
- 2017
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In: Frontiers in Microbiology. - : FRONTIERS MEDIA SA. - 1664-302X. ; 8
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Journal article (peer-reviewed)abstract
- Bacterial endosymbionts and their insect hosts establish an intimate metabolic relationship. Bacteria offer a variety of essential nutrients to their hosts, whereas insect cells provide the necessary sources of matter and energy to their tiny metabolic allies. These nutritional complementations sustain themselves on a diversity of metabolite exchanges between the cell host and the reduced yet highly specialized bacterial metabolism-which, for instance, overproduces a small set of essential amino acids and vitamins. A well-known case of metabolic complementation is provided by the cedar aphid Cinara cedri that harbors two co-primary endosymbionts, Buchnera aphidicola BCc and Ca. Serratia symbiotica SCc, and in which some metabolic pathways are partitioned between different partners. Here we present a genome-scale metabolic network (GEM) for the bacterial consortium from the cedar aphid iBSCc. The analysis of this GEM allows us the confirmation of cases of metabolic complementation previously described by genome analysis (i.e., tryptophan and biotin biosynthesis) and the redefinition of an event of metabolic pathway sharing between the two endosymbionts, namely the biosynthesis of tetrahydrofolate. In silico knock-out experiments with iBSCc showed that the consortium metabolism is a highly integrated yet fragile network. We also have explored the evolutionary pathways leading to the emergence of metabolic complementation between reduced metabolisms starting from individual, complete networks. Our results suggest that, during the establishment of metabolic complementation in endosymbionts, adaptive evolution is significant in the case of tryptophan biosynthesis, whereas vitamin production pathways seem to adopt suboptimal solutions.
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5. |
- Sun, Yu, et al.
(author)
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Switches in Genomic GC Content Drive Shifts of Optimal Codons under Sustained Selection on Synonymous Sites
- 2017
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In: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653. ; 9:10, s. 2560-2579
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Journal article (peer-reviewed)abstract
- 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.
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6. |
- Tamarit, Daniel, 1988-
(author)
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Evolution of symbiotic lineages and the origin of new traits
- 2016
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Doctoral thesis (other academic/artistic)abstract
- 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.
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7. |
- Tamarit, Daniel, et al.
(author)
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Functionally Structured Genomes in Lactobacillus kunkeei Colonizing the Honey Crop and Food Products of Honeybees and Stingless Bees
- 2015
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In: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653. ; 7:6, s. 1455-1473
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Journal article (peer-reviewed)abstract
- 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.
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8. |
- Tamarit, Daniel, 1988-, et al.
(author)
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Origin and evolution of the Bartonella Gene Transfer Agent
- 2018
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In: Molecular biology and evolution. - : Oxford University Press. - 0737-4038 .- 1537-1719. ; 35:2, s. 451-464
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Journal article (peer-reviewed)abstract
- Gene transfer agents (GTAs) are domesticated bacteriophages that have evolved into molecular machines for the transferof bacterial DNA. Despite their widespread nature and their biological implications, the mechanisms and selective forcesthat drive the emergence of GTAs are still poorly understood. Two GTAs have been identifiedintheAlphaproteobacteria:the RcGTA, which is widely distributed in a broad range of species; and the BaGTA, which has a restricted host range thatincludes vector-borne intracellular bacteria of the genusBartonella. The RcGTA packages chromosomal DNA randomly,whereas the BaGTA particles contain a relatively higher fraction of genes for host interaction factors that are amplifiedfrom a nearby phage-derived origin of replication. In this study, we compare the BaGTA genes with homologous bac-teriophage genes identified in the genomes ofBartonellaspecies and close relatives. Unlike the BaGTA, the prophagegenes are neither present in all species, nor inserted into homologous genomic sites. Phylogenetic inferences and sub-stitution frequency analyses confirm codivergence of the BaGTA with the host genome, as opposed to multiple integra-tion and recombination events in the prophages. Furthermore, the organizationof segments flanking the BaGTA differsfrom that of the prophages by a few rearrangement events,which have abolished the normal coordination betweenphage genome replication and phage gene expression. Based on the results of our comparative analysis, we propose amodel for how a prophage may be transformed into a GTA that transfers amplified bacterial DNA segments.
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