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The Genome of Rhizobiales Bacteria in Predatory Ants Reveals Urease Gene Functions but No Genes for Nitrogen Fixation

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The Genome of Rhizobiales Bacteria in Predatory Ants Reveals Urease Gene Functions but No Genes for Nitrogen Fixation

Minna-Maria Neuvonen et al. Sci Rep.

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.

Figures

Figure 1
Figure 1. Circular representation of the Bhsal genome.
Features from the outer circle to the center are: genes on the forward strand, genes on the reverse strand, single-copy orthologs from all the 17 surveyed genomes (red), genes uniquely present in Bhsal and a few other species (green), singletons in Bhsal (blue) and genes coding for proteins of special interest (yellow) such as: a, GTA-like phage; b, Bartonella adhesin (BadA); c, type III secretion system (T3SS); d, urease; e, CRISPR-cas type I-C; f, CRISPR-cas type II-C; g, BadA; h, autotransporters; i, putative extracellular protein secreted by the type I secretion system; j, filamentous hemagglutinin (FHA). The two innermost circles show the GC-bias and the GC-skew. The figure was obtained with dnaplotter, and edited with Adobe Illustrator.
Figure 2
Figure 2. Phylogenetic placement of Bhsal.
The phylogenies were based on (a) the 16 S rRNA gene and (b) a concatenated protein alignment. Colors represent the ant-associated sequence (red), the bee-associated sequences (yellow), the B. tamiae lineage (lime), and the clade formed by the canonical Bartonella species (blue). Ant and bee cliparts represent groups of sequences obtained from ant and bee samples, respectively. In (a), only the clade containing the Bartonella and the sequences obtained from ant and bee samples are shown; the complete tree is shown in Supplementary Fig. S1. In (b), dashed squares above key branches represent the percentage of single-gene trees that include those branches with high support (>70%), out of the total of 630 single-copy panorthologs. Both trees were inferred with the maximum likelihood method. Only bootstrap values higher than 80% are shown. The figure was drawn with Figtree (Andrew Rambaut, available on the author’s website: http://tree.bio.ed.ac.uk/software/figtree/), and edited with Adobe Illustrator.
Figure 3
Figure 3. Gene flux analysis.
Gains and losses of protein families were mapped onto the reference phylogeny of the Bhsal, B. tamiae and the canonical Bartonella species shown in Supplementary Fig. S2a. Above each branch, gains of protein families are shown in green, while losses are shown in red. Beneath each branch, the total number of protein families is shown. Only the ingroup is shown; the full tree and the full set of family gains and losses are shown in Supplementary Fig. S2b. The figure was drawn using custom perl and bash scripts, and edited with Adobe Illustrator.
Figure 4
Figure 4. Domain structure of a putative extracellular protein secreted by the type I secretion system.
(a) Gene order structure of the segment containing genes for a giant protein (putative extracellular protein) and a tryptophan halogenase. Arrows represent genes, and colors represent orthologs (red), genes uniquely present in Bhsal and a few other species (green), singletons in Bhsal (blue). Rectangles represent hits to Bacterial Ig-like domain (group 3) repeat IPR022038 (orange), SCOP family integrin alpha N-terminal domain SSF69318 (blue), serralysin-like metalloprotease C-terminal domain IPR011049 (purple) and the TIGRFam domain Type I secretion C-terminal target domain IPR019960 (red). (b) Phylogeny of tryptophan halogenase, where GI numbers are shown in parentheses, and only bootstrap values above 75 are shown. The figure was generated with genoplotR, and edited with Adobe Illustrator.
Figure 5
Figure 5. Phylogenetic inference of urease and glutamine synthetase.
Phylogenies of (a) the urease subunit alpha (ureC) and (b) and glutamine synthetase (glnA), based on their protein sequences. Accession numbers for each sequence are shown in parentheses. Only bootstrap values higher than 75% are shown. Red color represents the Bhsal sequences; green, B. tamiae; and blue, B. apis. The outgroup sequences were removed to aid visualization, these being: (a) AEV60653, CAH36667 and AF411018 from Pseudomonas fluorescens, Burkholderia pseudomallei and Nitrosospira sp. NpAVin, respectively, and (b) YP_008745196 and EAP72618 from Burkholderia pseudomallei and Ralstonia solanacearum, respectively. The figure was drawn with Figtree (Andrew Rambaut, available on the author’s website: http://tree.bio.ed.ac.uk/software/figtree/), and edited with Adobe Illustrator.

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