Genome Evolution of Bartonellaceae Symbionts of Ants at the Opposite Ends of the Trophic Scale.

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.

Origin and Evolution of the Bartonella Gene Transfer Agent.

Gene transfer agents (GTAs) are domesticated bacteriophages that have evolved into molecular machines for the transfer of bacterial DNA. Despite their widespread nature and their biological implications, the mechanisms and selective forces that drive the emergence of GTAs are still poorly understood. Two GTAs have been identified in the Alphaproteobacteria: the RcGTA, which is widely distributed in a broad range of species; and the BaGTA, which has a restricted host range that includes vector-borne intracellular bacteria of the genus Bartonella. The RcGTA packages chromosomal DNA randomly, whereas the BaGTA particles contain a relatively higher fraction of genes for host interaction factors that are amplified from a nearby phage-derived origin of replication. In this study, we compare the BaGTA genes with homologous bacteriophage genes identified in the genomes of Bartonella species and close relatives. Unlike the BaGTA, the prophage genes are neither present in all species, nor inserted into homologous genomic sites. Phylogenetic inferences and substitution frequency analyses confirm codivergence of the BaGTA with the host genome, as opposed to multiple integration and recombination events in the prophages. Furthermore, the organization of segments flanking the BaGTA differs from that of the prophages by a few rearrangement events, which have abolished the normal coordination between phage genome replication and phage gene expression. Based on the results of our comparative analysis, we propose a model for how a prophage may be transformed into a GTA that transfers amplified bacterial DNA segments.

The genome of Rhizobiales bacteria in predatory ants reveals urease gene functions but no genes for nitrogen fixation.

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.