Primary data of thiotrophic free-living and ectosymbiotic genomes

Thiotrophic symbioses between sulfur-oxidizing bacteria and various
unicellular and metazoan eukaryotes are widespread in reducing marine
environments. The giant colonial ciliate Zoothamnium niveum and its
vertically transmitted ectosymbiont Candidatus Thiobius zoothamnicola
(short Thiobius), however, is the only thiotrophic mutualism that has been
cultivated so far. Because theoretical predictions posit a smaller genome
in vertically transmitted endosymbionts compared to free-living relatives,
we investigated whether this is true also for an ectosymbiont. We used
metagenomics to recover the high-quality draft genome of this bacterial
symbiont. For comparison, we have also sequenced a closely related
free-living cultured but not formally described strain Milos ODIII6 (short
ODIII6). We then performed comparative genomics to assess the functional
capabilities at the gene, metabolic pathway, and trait levels. 16S rRNA
gene trees and average amino acid identity confirmed the close
phylogenetic relationship of both bacteria. Indeed, Thiobius had about a
third smaller genome than its free-living relative ODIII6, with reduced
metabolic capabilities and fewer functional traits. The functional
capabilities of Thiobius were mostly a subset of those of the more
versatile ODIII6, which possessed additional genes in the context of
oxygen, sulfur, and hydrogen utilization and for the acquisition of
phosphorus illustrating the adaptations to instable environmental
conditions at hydrothermal vents. In contrast, Thiobius possessed genes
for heterotrophy potentially enabling it to utilize lactate and acetate,
which may be provided as byproducts by the host. The present study
illustrates the effect of strict host-dependence of a bacterial
ectosymbiont on genome evolution and host adaptation.