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.
Highlights
Which have allowed several ant lineages to colonize ecological niches that would otherwise not be accessible
These bacteria are mostly associated with herbivory in ants, they have in a few cases been identified in predatory ants of the genus Pheidole[6] and in omnivorous giant tropical ants of the genus Paraponera[12] no complete genome sequences are as yet available for the ant-specific group of Rhizobiales bacteria, nor is it known what effects these bacteria have on the health and lifestyle of the ants
We find that the ant-associated bacterial species of the Rhizobiales clade resembles Bartonella and Brucella in their lack of capacity to fix nitrogen, but like Brucella, and in contrast to Bartonella, contain genes for the urease protein complex
Summary
A maximum likelihood phylogeny inferred from the 16 S rRNA gene sequences showed that Bhsal belongs to a genetically diverse clade (94% bootstrap support) of bacterial strains isolated from herbivorous ants (Tetraponera attenuata and Dolichoderus coniger), omnivorous ants (Paraponera clavata) as well as from predatory ants (Pheidole sp.) (Fig. 2; Supplementary Fig. S1). The tree topology suggested with 100% bootstrap support that Bhsal diverged prior to the sister groups represented by B. tamiae and B. apis, all three of which subtended the canonical Bartonella spp. To test for artifacts caused by nucleotide compositional biases, we examined the topologies of single protein trees inferred from alignments of the 50 genes that differed the least in GC content at the first two codon positions in Bhsal and Bartonella in the 647 gene dataset that excluded the B. apis metagenome (Supplementary Table S3).
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