Unprecedented Loss of Ammonia Assimilation Capability in a Urease-Encoding Bacterial Mutualist

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

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Ammonia / metabolism*
  • Animals
  • Ants / microbiology
  • Base Composition / genetics
  • Base Sequence
  • DNA, Intergenic / genetics
  • Enterobacteriaceae / enzymology*
  • Enterobacteriaceae / genetics*
  • Evolution, Molecular
  • Frameshift Mutation / genetics
  • Gene Deletion
  • Genes, Bacterial / genetics*
  • Glutamate-Ammonia Ligase / genetics
  • Metabolic Networks and Pathways / genetics
  • Molecular Sequence Data
  • Multigene Family / genetics
  • Phylogeny
  • Poly A / genetics
  • Replication Origin / genetics
  • Symbiosis / genetics*
  • Urease / genetics*

Substances

  • DNA, Intergenic
  • Poly A
  • Ammonia
  • Urease
  • Glutamate-Ammonia Ligase