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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.

Arndt-Sullivan, C, Lechaire JP, Felbeck H.  2008.  Extreme tolerance to anoxia in the Lucinoma aequizonata symbiosis. Journal of Shellfish Research. 27:119-127.   10.2983/0730-8000(2008)27[119:ettait];2   AbstractWebsite

Our study describes the extraordinary capability of the endosymbiont-bearing bivalve Lucinoma aequizonata to tolerate environmental anoxia. The clam survives without oxygen for 262 days (50% mortality). The total quantity of glycogen in a specimen does not decrease significantly after long-term anoxia (10.5 mo). Common glycogen-derived anaerobic products (opines, lactate, succinate, acetate, and propionate) are only produced in minor quantities. This indicates either severe metabolic depression or the utilization of alternative energy sources. We have found indications that the endosymbiotic bacteria might function as an important carbon source for the bivalve. Transmission electron microscopy studies showed that the symbionts are largely degraded after L. aequizonata was incubated anoxically for 10.5 mo. Polyphosphates detected in symbiont granules by energy dispersive X-ray spectrometry (EDX) might represent an alternative energy source for the clam's metabolism under this stress situation.

Dufour, SC, Felbeck H.  2006.  Symbiont abundance in thyasirids (Bivalvia) is related to particulate food and sulphide availability. Marine Ecology-Progress Series. 320:185-194.   10.3354/meps320185   AbstractWebsite

Many bivalve species with chemoautotrophic symbionts have mixotrophic diets and some of their nutritional requirements are met by particulate feeding. The symbionts require reduced compounds (such as sulphide) for their autotrophic production. As the concentration of both particulate food and sulphide can vary in their habitat, it has been suggested that symbiont numbers may vary in response. To address whether symbiont abundance can be influenced by the external medium, we compared symbiont. abundance (1) in specimens kept with or without particulate food, and (2) in specimens kept in sediments with low or high dissolved sulphide content. The relative surface area occupied by symbionts on semi-thin gill sections was determined for Thyasira flexuosa (and, in the sulfide experiment, for Parathyasira equalis and T sarsi) kept for up to 3 wk in experimental microcosms, where the quantity of particulate food or dissolved sulphide was manipulated. Symbiont abundance declined with time; the decline was greater in particle-starved thyasirids and in specimens kept in low sulphide. In the latter conditions, T flexuosa may have also had a greater symbiont digestion rate. The observed patterns may be due to a combination of increased symbiont uptake by the bivalve host, and reduced symbiont vigour under the imposed conditions. The flexible feeding mode of chemosymbiotic thyasirids may help them to survive in fluctuating environments.

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.

Hentschel, U, Berger EC, Bright M, Felbeck H, Ott JA.  1999.  Metabolism of nitrogen and sulfur in ectosymbiotic bacteria of marine nematodes (Nematoda, Stilbonematinae). Marine Ecology-Progress Series. 183:149-158.   10.3354/meps183149   AbstractWebsite

Nematodes of the family Stilbonematinae are known for their highly specific association with ectosymbiotic bacteria. These worms are members of the meiofauna in marine, sulfide-rich sediments, where they migrate around the redox boundary layer. In this study, bacterial ectosymbionts of 2 species of marine nematodes, Stilbonema sp. and Laxus oneistus, were shown to be capable of the respiratory reduction of nitrate and nitrite (denitrification). The use of these alternative electron accepters to oxygen by the bacteria allows the animals to migrate into the deeper, anoxic sediments, where they can exploit the sulfide-rich patches of the deeper sediment layers. The accumulation of thiols (sulfide, thiosulfate, sulfate and glutathione) in body tissues of the worms was determined following incubation in the presence of various electron donors (sulfide, thiosulfate) and accepters (nitrate). In their chemoautotrophic metabolic potential, the ectosymbionts of the 2 nematode species were found to resemble the phylogenetically related, intracellular symbionts of macrofaunal hosts of deep-sea hydrothermal vents and other sulfide-rich habitats.

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.