Publications

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2017
Ponnudurai, R, Sayavedra L, Kleiner M, Heiden SE, Thurmer A, Felbeck H, Schluter R, Sievert SM, Daniel R, Schweder T, Markert S.  2017.  Genome sequence of the sulfur-oxidizing Bathymodiolus thermophilus gill endosymbiont. Standards in Genomic Sciences. 12   10.1186/s40793-017-0266-y   AbstractWebsite

Bathymodiolus thermophilus, a mytilid mussel inhabiting the deep-sea hydrothermal vents of the East Pacific Rise, lives in symbiosis with chemosynthetic Gammaproteobacteria within its gills. The intracellular symbiont population synthesizes nutrients for the bivalve host using the reduced sulfur compounds emanating from the vents as energy source. As the symbiont is uncultured, comprehensive and detailed insights into its metabolism and its interactions with the host can only be obtained from culture-independent approaches such as genomics and proteomics. In this study, we report the first draft genome sequence of the sulfur-oxidizing symbiont of B. thermophilus, here tentatively named Candidatus Thioglobus thermophilus. The draft genome (3.1 Mb) harbors 3045 protein-coding genes. It revealed pathways for the use of sulfide and thiosulfate as energy sources and encodes the Calvin-Benson-Bassham cycle for CO2 fixation. Enzymes required for the synthesis of the tricarboxylic acid cycle intermediates oxaloacetate and succinate were absent, suggesting that these intermediates may be substituted by metabolites from external sources. We also detected a repertoire of genes associated with cell surface adhesion, bacteriotoxicity and phage immunity, which may perform symbiosis-specific roles in the B. thermophilus symbiosis.

2003
Gros, O, Liberge M, Felbeck H.  2003.  Interspecific infection of aposymbiotic juveniles of Codakia orbicularis by various tropical lucinid gill-endosymbionts. Marine Biology. 142:57-66.   10.1007/s00227-002-0921-7   AbstractWebsite

Previous molecular phylogenetic analyses have shown that five tropical lucinid species living in or near Thalassia testudinum seagrass beds are colonized by the same bacterial symbiont species. In addition, a new Iucinid species belonging to the genus Anodontia, which inhabits reducing sediment found near seagrass beds and in mangrove swamps, has been included in the present study. Endosymbiosis in Anodontia alba was examined according to symbiont phylogenetic and gill ultrastructural analysis. Phylogenetic analysis showed that partial 16S rDNA sequences of A. alba- and Codakia orbicularis-symbionts were 100% identical at all nucleotide positions determined, suggesting that A. alba also harbors the same symbiont species as C. orbicularis (and, consequently, as C. orbiculata, C. pectinella, Linga pensylvanica and Divaricella quadrisulcata). Based on light and electron microscopy, the cellular organization of the gill filament appeared similar to those already described in other lucinids. The most distinctive feature is the lack of "granule cells" in the lateral zone of A. alba gill filaments. In order to confirm the single-species hypothesis, purified fractions of gill bacterial symbionts obtained from the gills of each of the six tropical lucinids cited above were used to infect aposymbiotic juveniles of C. orbicularis. In each case, aposymbiotic juvenile batches were successfully infected by the gill-endosymbiont fractions, whereas, during the experiments, juveniles from the negative control were still uninfected. These experimental data confirm the phylogenetic data and also demonstrate that chemoautotrophic bacterial endosymbionts from their host cells can colonize aposymbiotic juveniles. The conclusion also follows that intracellular gill-endosymbionts still have the capacity to recognize and colonize new host generations. Lucinids provide a unique model for the study of sulfide-oxidizing symbiosis, even if symbionts remain unculturable.

2000
Gros, O, Frenkiel L, Felbeck H.  2000.  Sulfur-oxidizing endosymbiosis in Divaricella quadrisulcata (Bivalvia : Lucinidae): Morphological, ultrastructural, and phylogenetic analysis. Symbiosis. 29:293-317. AbstractWebsite

Based on light and electron microscopy, the cellular organization of the gill filament of Divaricella quadrisulcata is described and compared with other gill filaments of lucinids examined to date. TEM observations revealed a dense population of Gram-negative bacteria located within bacteriocytes in the lateral zone of the gill filament which looks similar to that of Codakia orbicularis with typical "granule cells". The digestive tract of this shallow-water lucinid species is less modified than in other lucinid species. The stomach has a well developed gastric shield, a cristalline style protruding in the stomach from a typical style sac, and active digestive diverticula. The mid gut is coiled through the visceral mass. Therefore, D. quadrisulcata appears to be at least partially dependent on filter-feeding for nutrition. Only one type of bacterial 16S rRNA gene was FCR-amplified from symbiont-containing gill tissue of two specimens, indicating a symbiont population composed of a single species. Phylogenetic analysis showed that sequences of D. quadrisulcata- and C. orbicularis-symbiont were 100% identical at all nucleotide positions determined, suggesting that this other tropical lucinid species harbors the same bacterial symbiont species as the previously analyzed C. orbicularis. Thus, D. quadrisulcata appears as the fifth tropical bivalve colonized by the same symbiont species even though it lives in a different habitat as the four other ones. The symbiont transmission mode was investigated by PCR amplifications from mature ovaries and testes. The C. orbicularis-specific 16S rDNA primer set was unsuccesful in amplifying DNA target for all individuals investigated suggesting that the gill-endosymbionts are environmentally transmitted to the new host generation as for all lucinids examined to date.

1996
Hentschel, U, Hand SC, Felbeck H.  1996.  The contribution of nitrate respiration to the energy budget of the symbiont-containing clam Lucinoma aequizonata: A calorimetric study. Journal of Experimental Biology. 199:427-433. AbstractWebsite

Heat production and nitrate respiration rates were measured simultaneously in the gill tissue of Lucinoma aequizonata. This marine bivalve contains chemoautotrophic, intracellular, bacterial symbionts in its gill tissue. The symbionts show constitutive anaerobic respiration, using nitrate instead of oxygen as a terminal electron acceptor. An immediate increase in heat production was observed after the addition of nitrate to the perfusion medium of the calorimeter and this was accompanied by the appearance of nitrite in the effluent sea water. The nitrate-stimulated heat output was similar under aerobic and anaerobic conditions, which is consistent with the constitutive nature of nitrate respiration. The amount of heat released was dependent on the concentration of nitrate in the perfusion medium. At nitrate concentrations between 0.5 and 5 mmoll(-1), the total heat production was increased over twofold relative to baseline values. A mean (+/-S.E.M.) enthalpy of -130+/-22.6 kJ mol(-1) nitrite (N=13) was measured for this concentration range.