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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.

Gros, O, Duplessis MR, Felbeck H.  1999.  Embryonic development and endosymbiont transmission mode in the symbiotic clam Lucinoma aequizonata (Bivalvia : Lucinidae). Invertebrate Reproduction & Development. 36:93-103.   10.1080/07924259.1999.9652683   AbstractWebsite

Lucinoma aequizonata is a large lucinid clam which lives in reducing mud around 500 m deep. Adults harbor intracellular chemoautotrophic sulfur-oxidizing bacteria in specialized gill cells called bacteriocytes. The embryonic and early larval development of L. aequizonata is described by using light and scanning electron microscopy. Gametes were obtained by injection of 0.2 ml of 4 mM serotonin solution in seawater into the posterior adductor muscle. The oocytes, 200 mu m in diameter, are surrounded by a glycoprotein capsule which gives to the egg a total diameter of 500 mu m. The development which occurs at 10 degrees C is slow. The first polar body is detected 2.5 h after contact between sperm and oocytes (T-0 + 2.5 h), and the first cleavage begins 10 h later (T-0 +12.5 h). The following successive cleavages produce a nonciliated morula, then a ciliated gastrula which begins to rotate within the egg-capsule at T-0 + 4.5 days. At this stage, the first shell pellicle appears on the dorsal side of the embryo. At T-0 + 8 days, the trochophore larvae develop discrete ciliary bands which constitute the prototroch. Typical straight-hinge veligers, D-shaped larvae, hatch from the egg-capsule 12 days after fertilization. The newly hatched larvae are 240 mu m in length and 200 mu m in height, and the straight hinge 150 mu m long. To elucidate the symbiont transmission mode, two symbiont-specific primers were designed and used in amplifications by PCR. This primer set was unsuccessful in amplifying symbiont DNA targets from mature gonads, spawned oocytes, eggs, and veligers whereas successful amplifications were obtained from symbiont-containing gill tissues. These data rule out the vertical transmission mode and strongly suggest that the symbionts are environmentally transmitted to the new host generation in L. aequizonata as for all tropical lucinids examined to date.

Felbeck, H, Jarchow J.  1998.  Carbon release from purified chemoautotrophic bacterial symbionts of the hydrothermal vent tubeworm Riftia pachyptila. Physiological Zoology. 71:294-302. AbstractWebsite

The gutless hydrothermal tubeworm Riftia pachyptila Tones relies mainly on its chemoautotrophic bacterial symbionts to supply nutrients in the form of secreted organic compounds resulting from fixation and incorporation of CO2. In this study, symbionts were purified, tested for viability, and incubated in the presence of labeled CO2. We demonstrated that purified symbionts can be used as a viable alternative to experiments with bacterial cultures. Several organic acids, sugars, and amino acids were labeled, but their fraction of the total label stayed generally constant during the incubation times used. However, increasing fractions of succinate and, to a lesser degree, glutamate were excreted into the incubation medium, indicating that these are probably the main carbon-containing compounds transferred from the symbionts to the host. Glutamate could also account for the transport of nitrogen from the symbionts to the host.

Hentschel, U, Cary SC, Felbeck H.  1993.  Nitrate respiration in chemoautotrophic symbionts of the bivalve Lucinoma aequizonata. Marine Ecology-Progress Series. 94:35-41.   10.3354/meps094035   AbstractWebsite

Chemoautotrophic bacteria live symbiotically in gills of Lucinoma aequizonata, an infaunal clam inhabiting an oxygen-poor environment. These intracellular symbionts respire nitrate, i.e. they use nitrate instead of oxygen as a terminal electron acceptor in the respiratory chain. Nitrate is only reduced to nitrite and not further to nitrogen gas. Nitrate is respired by the symbionts under fully aerobic conditions at the same rate as under anaerobic conditions. The bacterial symbionts contain a nitrate reductase that is associated with the membrane-containing fraction of the symbiont cell and that is sensitive to respiratory inhibitors; both features are consistent with the respiratory role of this enzyme. A review of nitrate reductase in chemoautotrophic symbionts suggests that nitrate respiration may be common among these symbioses. Symbiont nitrate reductase may be an ecologically important factor permitting the survival of animal hosts in oxygen-poor environments.

Polz, MF, Felbeck H, Novak R, Nebelsick M, Ott JA.  1992.  Chemoautotrophic, sulfur-oxidizing symbiotic bacteria on marine nematodes: Morphological and biochemical characterization. Microbial Ecology. 24:313-329.   10.1007/bf00167789   AbstractWebsite

The marine, free-living Stilbonematinae (Nematoda: Desmodorida) inhabit the oxygen sulfide chemocline in marine sands. They are characterized by an association with ectosymbiotic bacteria. According to their ultrastructure the bacteria are Gram-negative and form morphologically uniform coats that cover the entire body surface of the worms. They are arranged in host-genus or host-species specific patterns: cocci form multilayered sheaths, rods, and crescent- or filament-shaped bacteria form monolayers. The detection of enzymes associated with sulfur metabolism and of ribulose- 1,5 bisphosphate carboxylase oxygenase, as well as elemental sulfur in the bacteria indicate a chemolithoautotrophic nature of the symbionts. Their reproductive patterns appear to optimize space utilization on the host surface: vertically standing rods divide by longitudinal fission, whereas other bacteria form nonseptate filaments of up to 100 mum length.