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1999
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.

Millikan, DS, Felbeck H, Stein JL.  1999.  Identification and characterization of a flagellin gene from the endosymbiont of the hydrothermal vent tubeworm Riftia pachyptila. Applied and Environmental Microbiology. 65:3129-3133. AbstractWebsite

The bacterial endosymbionts of the hydrothermal vent tubeworm Riftia pachyptila play a key role in providing their host with fixed carbon. Results of prior research suggest that the symbionts are selected from an environmental bacterial population, although a free-living form has been neither cultured from nor identified in the hydrothermal vent environment. To begin to assess the free-living potential of the symbiont, we cloned and characterized a flagellin gene from a symbiont fosmid library. The symbiont fliC gene has a high degree of homology with other bacterial flagellin genes in the amino- and carboxy-terminal regions, while the central region was found to be nonconserved. A sequence that was homologous to that of a consensus sigma(28) RNA polymerase recognition site lay upstream of the proposed translational start site. The symbiont protein was expressed in Escherichia coli, and flagella were observed by electron microscopy. A 30,000-M-r protein subunit was identified in whole-cell extracts by Western blot analysis. These results provide the first direct evidence of a motile free-living stage of a chemoautotrophic symbiont and support the hypothesis that the symbiont of R. pachyptila is acquired with each new host generation.

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.

1998
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.

Pospesel, MA, Hentschel U, Felbeck H.  1998.  Determination of nitrate in the blood of the hydrothermal vent tubeworm Riftia pachyptila using a bacterial nitrate reduction assay. Deep-Sea Research Part I-Oceanographic Research Papers. 45:2189-2200.   10.1016/s0967-0637(98)00054-5   AbstractWebsite

The vestimentiferan tubeworm Riftia pachyptila derives most or all of its nutrition from intracellular chemosynthetic bacterial symbionts. Because purified preparations of symbionts respire nitrate, possibly nitrite, and oxygen, host transport of nitrate is a topic of interest. In the present study, we have developed a nitrate detection assay that utilizes a nitrite reductase-deficient Escherichia coli strain for the reduction of nitrate to nitrite, which is then determined spectrophotometrically. Nitrate and nitrite concentrations were measured in the blood and coelomic fluids of R. pachyptila collected from hydrothermal vent sites at 9 degrees N and 13 degrees N. The blood was shown to have nitrate concentrations up to one hundred times that of ambient sea water (40 mu M). Blood nitrate levels reached concentrations of >1 mM, while nitrite was measured in the range of 400-700 mu M. The concentrations of nitrate and nitrite in the coelomic fluids were 150-240 mu M and <20 mu M, respectively. The nitrate determination technique we present here is simple, applicable for laboratory and shipboard use on sea water or biological fluids, and works reliably within the 0.5 to 2000 mu M range. (C) 1998 Elsevier Science Ltd. All rights reserved.

Maxwell, B, Felbeck H.  1998.  An abundant heme protein in Riftia pachyptila symbionts is a nitrite reductase. Cahiers De Biologie Marine. 39:317-320. AbstractWebsite
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Arndt, C, Schiedek D, Felbeck H.  1998.  Anaerobiosis in the hydrothermal vent tube-worm Riftia pachyptila. Cahiers De Biologie Marine. 39:271-273. AbstractWebsite
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Hentschel, U, Pospesel MA, Felbeck H.  1998.  Evidence for a nitrate uptake mechanism in the hydrothermal vent tube-worm Riftia pachyptila. Cahiers De Biologie Marine. 39:301-304. AbstractWebsite
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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.

Hughes, DS, Felbeck H, Stein JL.  1998.  Signal transduction and motility genes from the bacterial endosymbionts of Riftia pachyptila. Cahiers De Biologie Marine. 39:305-308. AbstractWebsite
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1997
Hughes, DS, Felbeck H, Stein JL.  1997.  A histidine protein kinase homolog from the endosymbiont of the hydrothermal vent tubeworm Riftia pachyptila. Applied and Environmental Microbiology. 63:3494-3498. AbstractWebsite

The uncultivated bacterial endosymbionts of the hydrothermal vent tubeworm Riftia pachyptila play a central role in providing their host with fixed carbon. While this intimate association between host and symbiont indicates tight integration and coordination of function via cellular communication mechanisms, no such systems have been identified. To elucidate potential signal transduction pathways in symbionts that may mediate symbiont-host communication, we cloned and characterized a gene encoding a histidine protein kinase homolog isolated from a symbiont fosmid library. The gene, designated rssA (for Riftia symbiont signal kinase), resembles known sensor kinases and encodes a protein capable of phosphorylating response regulators in Escherichia coli. A second open reading Frame, rssB (for Riftia symbiont signal regulator), encodes a protein similar to known response regulators. These results suggest that the symbionts utilize a phosphotransfer signal transduction mechanism to communicate external signals that may mediate recognition of or survival within the host. The specific signals eliciting a response by the signal transduction proteins of the symbiont remain to be elucidated.

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.

1995
Boetius, A, Felbeck H.  1995.  Digestive enzymes in marine invertebrates from hydrothermal vents and other reducing environments. Marine Biology. 122:105-113.   10.1007/bf00349283   AbstractWebsite

The present study demonstrates the potential hydrolytic activities in the symbiont-containing tissues of the vent invertebrates Riftia pachyptila, Bathymodiolus thermophilus (collected in 1991 at the East Pacific Rise) and the shallow-water bivalve Lucinoma aequizonata (collected in 1991 from the Santa Barbara Basin). Activities of phosphatases, esterases, beta-glucuronidase and leucine aminopeptidase were comparable to those of digestive tract tissues of other marine invertebrates. A lack in most glycosidases as well as in trypsin and chymotrypsin was observed. Activities of lysozyme and chitobiase were rather high. In all vent invertebrates with symbionts and in L. aequizonata, the symbiont-containing tissues and the symbiont-free tissues had similar levels of enzymatic activities, indicating that polymeric nutrients could be hydrolysed after release from the symbionts and cellular uptake. The high activities of alpha-fucosidase in all vent invertebrates as well as in the shallow-water bivalve L. aequizonata could point to the existence of a yet undescribed substrate available to hydrolysation. The ectosymbionts-carrying polychaete Alvinella pompejana (collected in 1991 at the East Pacific Rise, EPR) shows high lysozyme activities in its gut, consistent with the proposed food source of bacteria. For the vent crab Bythogrea thermydron (also collected in 1991 at the EPR) hydrolytic activities were highest in the gut, dominated by esterase and peptidase activities which support their proposed carnivorous food source. A snail and a limpet collected from R. pachyptila tubes showed high levels of chitobiase suggesting a food source of grazed bacteria or ingested R. pachyptila tube.

Felbeck, H, Turner PJ.  1995.  CO2 transport in catheterized hydrothermal vent tubeworms, Riftia pachyptila (vestimentifera). Journal of Experimental Zoology. 272:95-102.   10.1002/jez.1402720203   AbstractWebsite

Isolated plumes and vestimenta of the tubeworm Riftia pachyptila were perfused to determine the form in which carbon is transported to the animal's symbionts via the circulatory system. Catheters supplying colored saline were inserted into an afferent blood vessel while samples were collected from the efferent vessel. During perfusion, the plumes were immersed in sea water containing radiolabeled CO2. The effluent showed radioactivity in inorganic carbonate (Sigma CO2, sum of all forms), malate, and succinate. When isolated vestimenta were perfused with saline containing labeled CO2, labeled malate and succinate could be detected in the effluent. Carbon transport in the blood as Sigma CO2 is estimated to be of similar importance to that transported after incorporation into organic carbon. The significance for the establishment of the carbon isotope ratio of tubeworms is discussed. (C) 1995 Wiley-Liss, Inc.

Wiley, S, Felbeck H.  1995.  D-alanine metabolism in the lucinid clam Lucinoma aequizonata. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology. 164:561-569. AbstractWebsite

The chemoautotrophic symbiont-bearing clam Lucinoma aequizonata contains very high levels of free D-alanine in all tissues. The possible sources for this amino acid and its involvement in the clams' metabolism were investigated. Very low levels of D-alanine (generally below 1 mu mol.l(-1)) were measured in the sediment pore-waters from the habitat of the clams. Experiments with C-14-labeled tracers demonstrate an active metabolism of D-alanine in the clams rather than a role as inert waste product. D-alanine is metabolized at about 0.12 mu mol.g fw(-1).h(-1). Label from aspartate, but not glucose and CO2, is incorporated into D-alanine. Incubation with labeled D-alanine did not result in formation of radioactive L-alanine. Tests for alanine racemase (EC 5.1.1.1) and D-amino acid oxidase (EC 1.4.3.3.) did not show activity in either gill, i.e. symbiont and host, or foot tissue. D-Alanine amino transferase (EC 2.6.1.b.) was demonstrated in gill and foot tissues. Two sources for D-alanine are proposed: a degradation of cell walls of symbiotic bacteria and production by the host using a D-specific alanine transaminase.

Hentschel, U, Felbeck H.  1995.  Nitrate respiration in chemoautotrophic symbionts of the bivalve Lucinoma aequizonata is not regulated by oxygen. Applied and Environmental Microbiology. 61:1630-1633. AbstractWebsite

The marine bivalve Lucinoma aequizonata has intracellular chemoautotrophic symbionts residing in the gill tissue. These bacteria are capable of nitrate respiration even under fully saturated oxygen conditions. Nitrate reductase in the symbionts of L. aequizonata appears to be constitutively expressed and without significant regulation by oxygen or nitrate. We discuss the stationary-phase growth state of the symbionts as an explanation for the lack of enzyme induction.

1994
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.

Polz, MF, Distel DL, Zarda B, Amann R, Felbeck H, Ott JA, Cavanaugh CM.  1994.  Phylogenetic analysis of a highly specific association between ectosymbiotic, sulfur-oxidizing bacteria and a marine nematode. Applied and Environmental Microbiology. 60:4461-4467. AbstractWebsite

The phylogenetic relationship of chemoautotrophic, sulfur-oxidizing, ectosymbiotic bacteria growing on a marine nematode, a Laxus sp. (formerly a Catanema sp.), to known endosymbionts and free-living bacteria was determined. Comparative 16S rRNA sequencing was used to investigate the unculturable nematode epibionts, and rRNA-targeted oligonucleotide hybridization probes were used to identify the ectosymbionts in situ. Both analyses revealed a remarkably specific and stable symbiosis. Unique hybridization of a specific probe to the ectosymbionts indicated that only one species of bacteria was present and growing on the cuticle of the nematode. Distance and parsimony methods used to infer phylogenetic trees both placed the nematode ectosymbionts at the base of a branch containing chemoautotrophic, sulfur-oxidizing endosymbionts of three bivalve families and of the tube worm Riftia pachyptila. The most closely related free-living bacteria were chemoautotrophic sulfur oxidizers belonging to the genus Thiomicrospira. Furthermore, our results suggested that a second, only distantly related group of thioautotrophic endosymbionts has as its deepest branch surface-colonizing bacteria belonging to the genus Thiothrix, some of which are capable of sulfur-oxidizing chemoautotrophic growth.

1993
Hentschel, U, Felbeck H.  1993.  Nitrate respiration in the hydrothermal vent tubeworm Riftia pachyptila. Nature. 366:338-340.   10.1038/366338a0   AbstractWebsite

THE vestimentiferan tubeworm Riftia packyptila is found around hydrothermal vent areas in the deep sea. Intracellular bacterial chemoautotrophic symbionts use the oxidation of sulphide from the effluent of the vents as an energy source for CO2 fixation. They apparently provide most or all of the nutritional requirements for their gutless hosts1-5. This kind of symbiosis has since been found in many other species from various other phyla from other habitats6-9. Here we present results that the bacteria of R. pachyptila may cover a significant fraction of their respiratory needs by the use of nitrate in addition to oxygen. Nitrate is reduced to nitrite, which may be the end product (nitrate respiration)10 or it may be further reduced to nitrogen gas (denitrification)11. This metabolic trait may have an important role in the colonization of hypoxic habitats in general by animals with this kind of symbiosis.

Childress, JJ, Lee RW, Sanders NK, Felbeck H, Oros DR, Toulmond A, Desbruyeres D, Kennicutt MC, Brooks J.  1993.  Inorganic carbon uptake in hydrothermal vent tubeworms facilitated by high environmental pC02. Nature. 362:147-149.   10.1038/362147a0   AbstractWebsite

THE marine invertebrate Riftia pachyptila has a remarkable symbiosis with intracellular carbon-fixing sulphide-oxidizing bacteria which was first discovered at 2,450 m depth on the Galapagos Rift1-4. Such symbiotic arrangements have since been found in a variety of invertebrate taxa and habitat5,6. Studies of these symbioses have focused on temperature, sulphide and oxygen as critical environmental parameters5,7-9. As Riftia has a high growth rate and its symbionts are far removed from the host surface10,11, inorganic carbon supply to the symbionts has been recognized as a problem and host mechanisms to concentrate inorganic carbo have been posited12,13. Increased environmental CO2 partial pressure (pCO2) has not seriously been considered as a critical environmental parameter7,14. Here we report that elevated pCO2 (2.9 kPa) in the worms' environment is a determinant of internal total CO2 (SIGMACO2) and pCO2, facilitating CO2 transport and diffusion to the symbionts. We propose that elevated pCO2 is a potentially critical environmental factor for this species as well as for other chemoautotrophic symbioses.

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.

Fiala-Medioni, A, Boulegue J, Ohta S, Felbeck H, Mariotti A.  1993.  Source of energy sustaining the Calyptogena populations from deep trenches in subduction zones off Japan. Deep-Sea Research Part I-Oceanographic Research Papers. 40:1241-1258.   10.1016/0967-0637(93)90136-q   AbstractWebsite

Deep tow camera surveys during the Hakuho Maru cruise (KH-89-1) and Nautile dives during the Kaiko-Nankai cruise (November 1989) demonstrate the presence of dense animal communities at depths around 2000 and 3800 m. The dominant organisms are vesicomyid bivalve molluscs, with two new very large (up to 28 cm long) species of Calyptogena and the two species previously found in the Nankai Trough during the Kaiko cruise (1985), C. laubieri and C. kaikoi. They apparently rely on sulfide-based chemoautotrophy through symbiotic bacteria associated with their gills. Evidence of sulfur-oxidizing metabolism includes ultrastructural features of symbionts, absence of methanol dehydrogenase activity, presence of ATP-sulfurylase and abundant elemental sulfur in the gill. Carbon isotope ratios are close to values obtained in other sulfur-oxidizing symbiont-bearing species (from -35.6 to -38.7 parts per thousand for the 3950 m species and from -36 to -37.4 parts per thousand for the 2050 m species). Nitrogen isotope ratios show highly variable values (from -4 to -9.7 parts per thousand for the 3950 m species and from -0.2 to +4.4 parts per thousand for the 2050 m species). C-14 analyses indicates growth based on water CO2 with limited or no input of fossil carbon.

Stein, JL, Felbeck H.  1993.  Kinetic and physical properties of a recombinant RuBisCO cloned from a chemoautotrophic endosymbiont. Molecular Marine Biology and Biotechnology. 2:280-290. Abstract
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Felbeck, H.  1993.  Symbiose mit chemoautotrophen Bakterien: Eine alternative Nahrungsquelle. Ökosystem Darm V: Immunologie, Mikrobiologie, Funktionsstörungen, klinische Manifestation: Klinik und Therapie akuter und chronischer Darmerkrankungen. ( Bockemühl J, Zeitz M, Lux G, Ottenjahn R, Eds.).:263-268., Berlin; New York: Springer-Verlag Abstract
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