title: Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms.
abstract: 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.
authors.affiliation: Department of Marine Biology, University of Vienna, A-1090 Vienna, Austria. harald.gruber@univie.ac.at
authors.forename: Harald Ronald
authors.initials: HR
authors.lastname: Gruber-Vodicka
authors.forename: Ulrich
authors.initials: U
authors.lastname: Dirks
authors.forename: Nikolaus
authors.initials: N
authors.lastname: Leisch
authors.forename: Christian
authors.initials: C
authors.lastname: Baranyi
authors.forename: Kilian
authors.initials: K
authors.lastname: Stoecker
authors.forename: Silvia
authors.initials: S
authors.lastname: Bulgheresi
authors.forename: Niels Robert
authors.initials: NR
authors.lastname: Heindl
authors.forename: Matthias
authors.initials: M
authors.lastname: Horn
authors.forename: Christian
authors.initials: C
authors.lastname: Lott
authors.forename: Alexander
authors.initials: A
authors.lastname: Loy
authors.forename: Michael
authors.initials: M
authors.lastname: Wagner
authors.forename: Jörg
authors.initials: J
authors.lastname: Ott
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001483:Base Sequence; D001499:Bayes Theorem; D005075:Biological Evolution; D016000:Cluster Analysis; D017931:DNA Primers / Q000235:genetics; D017404:In Situ Hybridization, Fluorescence; D016013:Likelihood Functions; D008855:Microscopy, Electron, Scanning; D046529:Microscopy, Electron, Transmission; D008957:Models, Genetic; D008969:Molecular Sequence Data; D010802:Phylogeny; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D012245:Rhodospirillales / Q000235:genetics* / Q000648:ultrastructure; D017422:Sequence Analysis, DNA; D013045:Species Specificity; D013059:Spectrum Analysis, Raman; D013559:Symbiosis; D014419:Turbellaria / Q000382:microbiology* / Q000648:ultrastructure
chemical_list: D017931:DNA Primers; D012336:RNA, Ribosomal, 16S