Abstract
Symbioses between eukaryotes and sulfur-oxidizing (thiotrophic) bacteria have convergently evolved multiple times. Although well described in at least eight classes of metazoan animals, almost nothing is known about the evolution of thiotrophic symbioses in microbial eukaryotes (protists). In this study, we characterized the symbioses between mouthless marine ciliates of the genus Kentrophoros, and their thiotrophic bacteria, using comparative sequence analysis and fluorescence in situ hybridization. Ciliate small-subunit rRNA sequences were obtained from 17 morphospecies collected in the Mediterranean and Caribbean, and symbiont sequences from 13 of these morphospecies. We discovered a new Kentrophoros morphotype where the symbiont-bearing surface is folded into pouch-like compartments, illustrating the variability of the basic body plan. Phylogenetic analyses revealed that all investigated Kentrophoros belonged to a single clade, despite the remarkable morphological diversity of these hosts. The symbionts were also monophyletic and belonged to a new clade within the Gammaproteobacteria, with no known cultured representatives. Each host morphospecies had a distinct symbiont phylotype, and statistical analyses revealed significant support for host–symbiont codiversification. Given that these symbioses were collected from two widely separated oceans, our results indicate that symbiotic associations in unicellular hosts can be highly specific and stable over long periods of evolutionary time.
Highlights
Symbiotic associations between eukaryotes and sulfur-oxidizing bacteria have evolved several times in different groups of both hosts and symbionts [1,2]
Much less is known about thiotrophic symbioses in protists, with only two groups described as hosts, namely euglenozoans [3] and ciliates [4]
The symbiotic bacteria have remained unidentified, they were described a long time ago [15,16]. It is not known whether the Kentrophoros symbionts are all close relatives to each other or if they come from different clades, nor is it possible to infer from morphology and physiology alone if they are related to known groups of thiotrophic bacteria
Summary
Symbiotic associations between eukaryotes and sulfur-oxidizing (thiotrophic) bacteria have evolved several times in different groups of both hosts and symbionts [1,2]. The symbiotic bacteria have remained unidentified, they were described a long time ago [15,16] It is not known whether the Kentrophoros symbionts are all close relatives to each other or if they come from different clades, nor is it possible to infer from morphology and physiology alone if they are related to known groups of thiotrophic bacteria. H sections from two individuals were separately hybridized with four different probe sets of increasing taxonomic specificity: EUB338I-III targeting most Bacteria [43,44], Gam42a (with unlabelled Beta42a competitor) targeting most Gammaproteobacteria [45], chr4Ca (with unlabelled helper probes) targeting most Kentrophoros candidate symbiont sequences and chr4Ba, targeting only the candidate symbiont of K. sp. Volumes of the segmented areas (entire body, symbiont region and nuclei) were measured with the ‘measurement’ option in Amira
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