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Proc Biol Sci. 2017 Jul 12;284(1858). pii: 20170764. doi: 10.1098/rspb.2017.0764.

Specificity in diversity: single origin of a widespread ciliate-bacteria symbiosis.

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Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany
Department of Integrative Zoology, University of Vienna, Althanstraße 14, 1090 Vienna, Austria.
Department of Limnology and Bio-Oceanography, University of Vienna, Althanstraße 14, 1090 Vienna, Austria.
Max Planck Genome Centre Cologne, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Cologne, Germany.
Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.
MARUM, Center for Marine Environmental Sciences, University of Bremen, 28359 Bremen, Germany.


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.


Gammaproteobacteria; ciliate; symbiosis; thiotrophy

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