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Dryad

Primary data of thiotrophic free-living and ectosymbiotic genomes

Abstract

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.