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. 2010 Dec 2:11:687.
doi: 10.1186/1471-2164-11-687.

Unprecedented loss of ammonia assimilation capability in a urease-encoding bacterial mutualist

Laura E Williams  1 , Jennifer J Wernegreen
Affiliations

Unprecedented loss of ammonia assimilation capability in a urease-encoding bacterial mutualist

Laura E Williams et al. BMC Genomics. .

Abstract

Background: Blochmannia are obligately intracellular bacterial mutualists of ants of the tribe Camponotini. Blochmannia perform key nutritional functions for the host, including synthesis of several essential amino acids. We used Illumina technology to sequence the genome of Blochmannia associated with Camponotus vafer.

Results: Although Blochmannia vafer retains many nutritional functions, it is missing glutamine synthetase (glnA), a component of the nitrogen recycling pathway encoded by the previously sequenced B. floridanus and B. pennsylvanicus. With the exception of Ureaplasma, B. vafer is the only sequenced bacterium to date that encodes urease but lacks the ability to assimilate ammonia into glutamine or glutamate. Loss of glnA occurred in a deletion hotspot near the putative replication origin. Overall, compared to the likely gene set of their common ancestor, 31 genes are missing or eroded in B. vafer, compared to 28 in B. floridanus and four in B. pennsylvanicus. Three genes (queA, visC and yggS) show convergent loss or erosion, suggesting relaxed selection for their functions. Eight B. vafer genes contain frameshifts in homopolymeric tracts that may be corrected by transcriptional slippage. Two of these encode DNA replication proteins: dnaX, which we infer is also frameshifted in B. floridanus, and dnaG.

Conclusions: Comparing the B. vafer genome with B. pennsylvanicus and B. floridanus refines the core genes shared within the mutualist group, thereby clarifying functions required across ant host species. This third genome also allows us to track gene loss and erosion in a phylogenetic context to more fully understand processes of genome reduction.

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Figures

Figure 1
Figure 1
Comparison of intact genes encoded by three Blochmannia genomes. To highlight potential metabolic differences among genomes, only intact genes are shown. These include protein-coding and RNA-coding genes. Eroded pseudogenes in a given genome are considered missing due to loss of function. Genes with a single frameshift in a polyA or polyT tract are considered intact for this purpose, because transcriptional slippage may restore expression of a full-length protein product. In this comparison, yidC and yidD in B. floridanus are counted as a single gene, due to fusion in B. pennsylvanicus and B. vafer.
Figure 2
Figure 2
Gene loss in B. vafer and B. floridanus compared to B. pennsylvanicus. (a) B. vafer genes were plotted against orthologs in B. pennsylvanicus. The x- and y-axes correspond to gene number in B. vafer and B. pennsylvanicus, respectively. Locations of missing genes (represented by a delta symbol) and eroded genes (represented by a psi symbol) are emphasized by larger dots. Gene names are listed next to the symbols. Two genes, marked with asterisks, are missing in one of the genomes and present only as a pseudogene in the other genome. The inset shows a more detailed view of the ~30 kb region in B. vafer near the putative replication origin, in which eight genes are missing compared to B. pennsylvanicus. The grey shaded region in the inset indicates the relocation of the origin in B. vafer compared to B. pennsylvanicus. (b) B. floridanus genes were plotted against orthologs in B. pennsylvanicus, using the same methodology as above.
Figure 3
Figure 3
GC content and GC skew of B. vafer genome. GC content (black) and GC skew (green and purple) of the B. vafer genome. For GC skew, the center line indicates the average GC skew value for the genome. Green shading above the line denotes GC skew values greater than the genome average, whereas purple shading below the line denotes GC skew values less than the genome average. Major and minor tick marks on the outermost and innermost circles show nucleotide position on the genome in 100 kbp and 20 kbp increments, respectively.
Figure 4
Figure 4
Frameshifts in polyA or polyT tracts in Blochmannia genes. Alignments illustrate frameshifted regions of the eleven genes that contain indels within homopolymeric tracts in one or more Blochmannia genomes. Apart from the frameshifts shown, these genes are otherwise in frame. The frameshifts may be corrected by transcriptional slippage to yield full-length, in-frame transcripts.
Figure 5
Figure 5
Gene loss and erosion in Blochmannia. The differential gene content of the three Blochmannia genomes is shown in a phylogenetic context to highlight small frameshifts and missing or eroded genes. Presence of a gene is shown with a plus sign and absence of a gene with a zero. Pseudogenes are indicated by a psi symbol (ψ), and frameshifts are denoted with the letter f. COG functional categories are shown on the bottom line. Genes for which frameshifts, erosion, or loss occur independently in different Blochmannia lineages are marked in boldface.
Figure 6
Figure 6
Gene content differences among select bacterial endosymbionts of insects. For each gene, the protein sequence from E. coli K12 MG1655 (NC_000913) was compared to endosymbiont genomes using TBLASTN. Black squares indicate presence of the gene, and white squares indicate that the gene is either missing or a pseudogene.
Figure 7
Figure 7
Possible alternative pathways for ammonia assimilation in B. vafer. Three possible pathways for ammonia assimilation in Blochmannia are shown. Glutamine synthetase (glnA) is crossed out because of the absence of glnA in B. vafer.
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