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

Abstract

BackgroundBlochmannia 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.ResultsAlthough 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.ConclusionsComparing 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.

Microbial composition of spiny ants (Hymenoptera: Formicidae: Polyrhachis) across their geographic range

“…Blochmannia also maintains certain genes for basic cellular functions, such as biosynthesis of the nine essential amino acids (excluding Arginine), and urease cofactors and enzymes, which allows the symbiont to recycle urea nitrogen provided by the host’s excretory system [73, 75, 76]. In addition, the nutritional role of Blochmannia is not the only potential interaction with its host, as it has also maintained genes needed to contribute to the metabolism of nitrogen, sulfur and lipids [24–26]. …”

“…Blochmannia is a Proteobacteria specific to the Camponotini, which has been demonstrated to assist in providing essential amino acids to their host since their diets are defficient in nutrients as a consequence of their arboreal habitats [22, 23]. The nutritional role of Blochmannia is not the only beneficial aspect to the host, as it has been shown that Blochmannia also has the necessary genes to contribute to the metabolism of nitrogen, sulfur and lipids [24–26]. In addition to Blochmannia endosymbionts, among members of the Camponotini tribe, there are other species of endosymbionts that have been documented from these hosts, including Arsenophonus spp., Cardinium hertigii , Hamiltonella defense , and Spiroplasma spp.…”

Metabolic stasis in an ancient symbiosis: genome-scale metabolic networks from two Blattabacterium cuenoti strains, primary endosymbionts of cockroaches

“…The dependence on host-supplied Gln has also been recently described in Blochmannia vafer , the primary endosymbiont of the ant Camponotus vafer , which contains urease but lacks both Glu dehydrogenase and Gln synthase [36]. …”

The Human Ureaplasma Species as Causative Agents of Chorioamnionitis

“…Interestingly, the Ureaplasma spp. are some of the few bacterial species which encode a urease enzyme but lack the ability to assimilate ammonia into glutamine or glutamate (274), potentially explaining the very high intracellular ammonia concentration of these microorganisms (140).…”