Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms

Autor(en)

Harald Gruber-Vodicka, Ulrich Dirks, Nikolaus Leisch, Christian Baranyi, Kilian Stöcker, Silvia Bulgheresi, Niels Robert Heindl, Matthias Horn, Christian Lott, Alexander Loy, Michael Wagner, Jörg Ott

Abstrakt

Harnessing chemosynthetic symbionts is a recurring evolutionary strategy. Eukaryotes from six phyla as well as one archaeon have acquired chemoautotrophic sulfur-oxidizing bacteria. In contrast to this broad host diversity, known bacterial partners apparently belong to two classes of bacteria-the Gamma-and Epsilonproteobacteria. Here, we characterize the intracellular endosymbionts of the mouthless catenulid flatworm genus Paracatenula as chemoautotrophic sulfur-oxidizing Alphaproteobacteria. The symbionts of Paracatenula galateia are provisionally classified as "Candidatus Riegeria galateiae" based on 16S ribosomal RNA sequencing confirmed by fluorescence in situ hybridization together with functional gene and sulfur metabolite evidence. 16S rRNA gene phylogenetic analysis shows that all 16 Paracatenula species examined harbor host species-specific intracellular Candidatus Riegeria bacteria that form a monophyletic group within the order Rhodospirillales. Comparing host and symbiont phylogenies reveals strict cocladogenesis and points to vertical transmission of the symbionts. Between 33% and 50% of the body volume of the various worm species is composed of bacterial symbionts, by far the highest proportion among all known endosymbiotic associations between bacteria and metazoans. This symbiosis, which likely originated more than 500 Mya during the early evolution of flatworms, is the oldest known animal-chemoautotrophic bacteria association. The distant phylogenetic position of the symbionts compared with other mutualistic or parasitic Alphaproteobacteria promises to illuminate the common genetic predispositions that have allowed several members of this class to successfully colonize eukaryote cells.

Organisation(en)

Externe Organisation(en)

Max-Planck-Institut für marine Mikrobiologie

Journal

Proceedings of the National Academy of Sciences of the United States of America (PNAS)

Band

108

Seiten

12078-12083

Anzahl der Seiten

6

ISSN

0027-8424

DOI

https://doi.org/10.1073/pnas.1105347108

Publikationsdatum

2011

Peer-reviewed

Ja

ÖFOS 2012

106022 Mikrobiologie

Link zum Portal

https://ucrisportal.univie.ac.at/de/publications/c6559490-41e0-4410-81ce-f05f2fe45144