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 animalchemoautotrophic 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. intracellular symbiosis | marine catenulid | meiofauna | subtidal sand
Rod-shaped bacteria usually grow in length and place their FtsZ ring and division site at midcell, perpendicular to their long axis [1,2]. Here, we provide morphometric and immunocytochemical evidence that a nematode-associated gammaproteobacterium [3,4] grows in width, sets a constricting FtsZ ring parallel to its long axis, and divides longitudinally by default. Remarkably, the newly described FtsZ ring appears to be not only 90° shifted with respect to model rods, but also elliptical and discontinuous. This reveals an unexpected versatility of the gammaproteobacterial cytokinetic machinery.
Marine nematodes that carry sulfur-oxidizing bacteria on their cuticle (Stilbonematinae, Desmodoridae) migrate between oxidized and reduced sand layers thereby supplying their symbionts with oxygen and sulfide. These symbionts, in turn, constitute the worms' major food source. Due to the accessibility, abundance and relative simplicity of this association, stilbonematids may be useful to understand symbiosis establishment. Nevertheless, only the symbiont of Laxus oneistus has been found to constitute one single phylotype within the Gammaproteobacteria. Here, we characterized the symbionts of three yet undescribed nematodes that were morphologically identified as members of the genus Robbea. They were collected at the island of Corsica, the Cayman Islands and the Belize Barrier Reef. The surface of these worms is covered by a single layer of morphologically undistinguishable bacteria. 18S rDNA-based phylogenetic analysis showed that all three species belong to the Stilbonematinae, although they do not form a distinct cluster within that subfamily. 16S rDNA-based analysis of the symbionts placed them interspersed in the cluster comprising the sulfur-oxidizing symbionts of L. oneistus and of marine gutless oligochaetes. Finally, the presence and phylogeny of the aprA gene indicated that the symbionts of all three nematodes can use reduced sulfur compounds as an energy source.
Two long-standing paradigms in biology are that cells belonging to the same population exhibit little deviation from their average size and that symmetric cell division is size limited. Here, ultrastructural, morphometric and immunocytochemical analyses reveal that two Gammaproteobacteria attached to the cuticle of the marine nematodes Eubostrichus fertilis and E. dianeae reproduce by constricting a single FtsZ ring at midcell despite being 45 μm and 120 μm long, respectively. In the crescent-shaped bacteria coating E. fertilis, symmetric FtsZ-based fission occurs in cells with lengths spanning one order of magnitude. In the E. dianeae symbiont, formation of a single functional FtsZ ring makes this the longest unicellular organism in which symmetric division has ever been observed. In conclusion, the reproduction modes of two extraordinarily long bacterial cells indicate that size is not the primary trigger of division and that yet unknown mechanisms time the localization of both DNA and the septum.
Selection of a specific microbial partner by the host is an all-important process. It guarantees the persistence of highly specific symbioses throughout host generations. The cuticle of the marine nematode Laxus oneistus is covered by a single phylotype of sulfur-oxidizing bacteria. They are embedded in a layer of host-secreted mucus containing the mannose-binding protein Mermaid. This Ca(2+)-dependent lectin mediates symbiont aggregation and attachment to the nematode. Here, we show that Stilbonema majum-a symbiotic nematode co-occurring with L. oneistus in shallow water sediment-is covered by bacteria phylogenetically distinct to those covering L. oneistus. Mermaid cDNA analysis revealed extensive protein sequence variability in both the nematode species. We expressed three recombinant Mermaid isoforms, which based on the structural predictions display the most different carbohydrate recognition domains (CRDs). We show that the three CRDs (DNT, DDA and GDA types) possess different affinities for L. oneistus and S. majum symbionts. In particular, the GDA type, exclusively expressed by S. majum, displays highest agglutination activity towards its symbionts and lowest towards its L. oneistus symbionts. Moreover, incubation of L. oneistus in the GDA type does not result in complete symbiont detachment, whereas incubation in the other types does. This indicates that the presence of particular Mermaid isoforms on the nematode surface has a role in the attachment of specific symbionts. This is the first report of the functional role of sequence variability in a microbe-associated molecular patterns receptor in a beneficial association.
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