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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.

Hahlbeck, E, Pospesel MA, Zal F, Childress JJ, Felbeck H.  2005.  Proposed nitrate binding by hemoglobin in Riftia pachyptila blood. Deep-Sea Research Part I-Oceanographic Research Papers. 52:1885-1895.   10.1016/j.dsr.2004.12.011   AbstractWebsite

Riftia pachyptila lives in the unstable environment at hydrothermal vent sites along oceanic spreading zones in the Eastern Pacific. The tubeworm has a symbiosis with intracellular carbon-fixing and sulfide-oxidizing bacteria. Nitrate is the main source of nitrogen available from their habitat. This compound serves as a substrate either for nitrate respiration or for biosynthesis after transformation into ammonia. Very high nitrate (up to 3.2 mM) and nitrite (up to 0.8 mM) concentrations in vascular blood of R. pachyptila indicate a novel uptake mechanism. The dialysis experiments reported here demonstrate the binding and transport of nitrate to the symbionts by high molecular weight components in the blood, most likely hemoglobin. The extent to which nitrate is bound differed markedly between blood from different animals. In addition, a strong inverse correlation was found between the concentrations of sulfide and nitrate in vascular blood, as well as between the sulfur content of trophosome and the nitrate content of vascular blood. Specimens with low sulfur stores showed much lower nitrate levels than those with pale green trophosome due to high levels of elemental sulfur. (c) 2005 Elsevier Ltd. All rights reserved.

Felbeck, H, Arndt C, Hentschel U, Childress JJ.  2004.  Experimental application of vascular and coelomic catheterization to identify vascular transport mechanisms for inorganic carbon in the vent tubeworm, Riftia pachyptila. Deep-Sea Research Part I-Oceanographic Research Papers. 51:401-411.   10.1016/j.dsr.2003.10.012   AbstractWebsite

Maintaining deep sea animals in in situ conditions has always been technically difficult because of the high-pressure requirements. Even more difficult are any attempts in manipulating or sampling these organisms while keeping them alive in high-pressure aquaria. We present a technique to withdraw blood samples by vascular catheterization which allows withdrawal of samples of during maintenance of specimens under high-pressure conditions. We have developed this technique to answer a long debated question, how carbon dioxide is transported from the ambient sea water to the bacterial symbionts inside the trophosome of the hydrothermal vent tubeworm. Riftia pachyptila. Our results indicate that the carbon supply to the symbionts is mainly through inorganic CO2 while its incorporation into malate and succinate may serve storage functions at periods Of low CO2 availability in the environment. (C) 2003 Elsevier Ltd. All rights reserved.

Hentschel, U, Millikan DS, Arndt C, Cary SC, Felbeck H.  2000.  Phenotypic variations in the gills of the symbiont-containing bivalve Lucinoma aequizonata. Marine Biology. 136:633-643.   10.1007/s002270050723   AbstractWebsite

The marine bivalve Lucinoma aequizonata (Lucinidae) maintains a population of sulfide-oxidizing chemoautotrophic bacteria in its gill tissue. These are housed in large numbers intracellularly in specialized host cells, termed bacteriocytes. In a natural population of L. aequizonata, striking variations of the gill colors occur, ranging from yellow to grey, brown and black. The aim of the present study was to investigate how this phenomenon relates to the physiology and numbers of the symbiont population, Our results show that in aquarium-maintained animals, black gills contained fewer numbers of bacteria as well as lower concentrations of sulfur and total protein. Nitrate respiration was stimulated by sulfide (but not by thiosulfate) 33-fold in homogenates of black gills and threefold in yellow gill homogenates. The total rates of sulfide-stimulated nitrate respiration were the same. Oxygen respiration could be measured in animals with yellow gills but not in animals with black gills. The cumulative data suggest that black-gilled clams maintained in the aquarium represent a starvation state. When collected from their natural habitat black gills contain the same number of bacteria as yellow gills. Also, no significant difference in glycogen concentrations of the host tissues was observed. Therefore, starvation is unlikely the cause of black gill color in a natural population. Alternative sources of nutrition to sulfur-based metabolism are discussed. Denaturing gradient gel electrophoresis (DGGE) performed on the different gill tissues, as well as on isolated symbionts, resulted in a single gill symbiont amplification product, the sequence of which is identical to published data. These findings provide molecular evidence that one dominant phylotype is present in the morphologically different gill tissues. Nevertheless, the presence of other phylotypes cannot formally be excluded. The implications of this study are that the gill of L. aequizonata is a highly dynamic organ which lends itself to more detailed studies regarding the molecular and cellular processes underlying nutrient transfer, regulation of bacterial numbers and host-symbiont communication.

Arndt, C, Schiedek D, Felbeck H.  1998.  Metabolic responses of the hydrothermal vent tube worm Riftia pachyptila to severe hypoxia. Marine Ecology-Progress Series. 174:151-158.   10.3354/meps174151   AbstractWebsite

The metabolic capabilities of the hydrothermal vent tube worm Riftia pachyptila to tolerate short- and long-term exposure to hypoxia were investigated. After incubating specimens under anaerobic conditions the metabolic changes in body fluids and tissues were analyzed over time. The tube worms tolerated anoxic exposure up to 60 h. Prior to hypoxia the dicarboxylic acid, malate, was found in unusually high concentrations in the blood (up to 26 mM) and tissues (up to 5 pmol g(-1) fresh wt). During hypoxia, most of the malate was degraded very quickly, while large quantities of succinate accumulated (blood: about 17 mM; tissues: about 13 mu mol g(-1) fresh wt). Volatile, short-chain fatty acids were apparently not excreted under these conditions. The storage compound, glycogen, was mainly found in the trophosome and appears to be utilized only during extended anaerobiosis. The succinate formed during hypoxia does not account for the use of malate and glycogen, which possibly indicates the presence of yet unidentified metabolic end products. Glutamate concentration in the trophosome decreased markedly during hypoxia, presumably due to a reduction in the autotrophic function of the symbionts during hypoxia. In conclusion, R. pachyptila is physiologically well adapted to the oxygen fluctuations frequently occurring in the vent habitat.

Distel, DL, Felbeck H, Cavanaugh CM.  1994.  Evidence for phylogenetic congruence among sulfur-oxidizing chemoautotrophic bacterial endosymbionts and their bivalve hosts. Journal of Molecular Evolution. 38:533-542.   10.1007/bf00178852   AbstractWebsite

Sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria are now known to occur as endosymbionts in phylogenetically diverse bivalve hosts found in a wide variety of marine environments. The evolutionary origins of these symbioses, however, have remained obscure. Comparative 16S rRNA sequence analysis was used to investigate whether thioautotrophic endosymbionts are monophyletic or polyphyletic in origin and to assess whether phylogenetic relationships inferred among these symbionts reflect those inferred among their hosts. 16S rRNA gene sequences determined for endosymbionts from nine newly examined bivalve species from three families (Vesicomyidae, Lucinidae, and Solemyidae) were compared with previously published 16S rRNA sequences of thioautotrophic symbionts and free-living bacteria. Distance and parsimony methods were used to infer phylogenetic relationships among these bacteria. All newly examined symbionts fall within the gamma subdivision of the Proteobacteria, in clusters containing previously examined symbiotic thioautotrophs. The closest free-living relatives of these symbionts are bacteria of the genus Thiomicrospira. Symbionts of the bivalve superfamily Lucinacea and the family Vesicomyidae each form distinct monophyletic lineages which are strongly supported by bootstrap analysis, demonstrating that host phylogenies inferred from morphological and fossil evidence are congruent with phylogenies inferred for their respective symbionts by molecular sequence analysis. The observed congruence between host and symbiont phylogenies indicates shared evolutionary history of hosts and symbiont lineages and suggests an ancient origin for these symbioses.