Hidden genetic diversity among Blochmanniella endosymbionts of closely related carpenter ant populations

TL;DR

This study reveals hidden genetic diversity in Blochmanniella bacteria living in closely related carpenter ant populations.

Contribution

The discovery of a novel Blochmanniella lineage, BSEQ, with unique gene losses and functions in a geographically distinct C. vicinus population.

Findings

The BSEQ lineage has lost genes related to membrane maintenance, bacterial cell information, and nutrition synthesis.

BSEQ can supply 7 of 10 essential amino acids to its host and assist in breaking down urea and repairing DNA damage.

Most protein-coding genes in BSEQ and related lineages are under strong or relaxed purifying selection.

Abstract

Carpenter ants (Family Formicidae; Genus Camponotus) are a globally distributed, arboreal clade. They harbor an intracellular obligate bacterial endosymbiont known as “Candidatus Blochmanniella spp.” (hereafter Blochmanniella). The host ant species, C. vicinus, is geographically dispersed across the western United States of America and western Canada. To investigate how Blochmanniella have differentially evolved from related host-endosymbiont lineages, we sampled a C. vicinus population from California’s Sierra Nevada mountains, California, U.S.A., at an elevation of 2,300 m. Using morphological characters and Cytochrome Oxidase I markers, we determined that this population is genetically distinct from geographically distributed lineages of C. vicinus from Central California and Western North America (Arizona, U.S.A. to British Columbia, Canada). Thus, we sequenced the genome of the Blochmanniella endosymbiont from this host to understand how closely related symbiont lineages evolve. While our newly sequenced lineage is syntenic with other Blochmanniella, it has lost genes involved in membrane maintenance, bacterial cell information, and nutrition synthesis. Protein-coding genes across its genome are highly divergent as well (average sequence similarity = 93.6%). Therefore, we refer to our novel lineage as the B. vicinus Sequoia lineage (BSEQ). BSEQ can provide 7 of the 10 essential amino acids required by its insect host. It can also help break down toxic urea and repair UV radiation-induced DNA damage. Tests of selection reveal that most protein-coding genes BSEQ and related lineages are under strong or relaxed purifying selection. Taken together, our results demonstrate that while BSEQ and related Blochmanniella lineages have highly conserved content, there is considerable evolutionary diversity between them.

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