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Felbeck, H, Childress JJ.  1988.  Riftia pachyptila, a highly integrated symbiosis. Oceanologica Acta. 8:131-138. Abstract
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
Garcia-Esquivel, Z, Felbeck H.  2006.  Activity of digestive enzymes along the gut of juvenile red abalone, Haliotis rufescens, fed natural and balanced diets. Aquaculture. 261:615-625.   10.1016/j.aquaculture.2006.08.022   AbstractWebsite

Two carbohydrases (cellulase, lysozyme), three proteases (trypsin, aminopeptidase and non-specific protease), a non-specific lipase, and semiquantitative tests of 19 digestive enzymes were assayed in different gut sections of juvenile red abalone, Haliotis rufescens, in order to identify the regions where digestion takes place and investigate the extent to which diet composition can modify the digestive capacity of abalone. The abalone were fed either fresh kelp (K) or balanced diets containing 25 or 38% crude protein for 6 months. Enzyme assays were carried out on different sections of the abalone's gut at the end of this period. On a weight-specific basis, the digestive gland was the site containing most of the enzymes. On a protein-specific basis, two main digestion regions were identified: the digestive gland-stomach region that is characterized by high activities of cellulase and lysozyme, chymotrypsin and protease, and the mouth-intestine region with a typically high activity of lipase and amino peptidase. Significant dietary effects were observed on the activity of enzymes, especially in the digestive gland. Abalone fed with 25 and 38% crude protein diets exhibited higher cellulase (39.8 +/- 4.6 and 14.2 +/- 0.8 mU mg(-1) protein, respectively) and lysozyme activities (88.0 +/- 20.4 and 56.6 +/- 15.7 U, respectively) than those fed with fresh kelp (5.5 +/- 0.7 mU mg-1 protein and 17.1 +/- 1.8 U). In contrast, higher protease activity was found in kelp-fed organisms (234.1 +/- 20.4 mu g product/mg protein) than those fed the 25 and 38% crude protein diets (109.5 +/- 20.7 and 119.5 +/- 20.5 mu g product/mg protein, respectively). Semiquantitative API ZYM assays resulted in no clear food-specific effects on the activity of carbohydrases, proteases, ester hydrolases or phosphohydrolases, yet organ-specific differences were conspicuous in various cases, and generally agreed with quantitative results. It is suggested that the increased carbohydrase activity exhibited by organisms fed the balanced diets resulted from a combination of an increased number of resident bacteria in the abalone's gut and facilitated contact between dietary substrates and digestive cells. The present results indicate that H. rufescens can adjust their enzyme levels in order to maximize the acquisition of dietary protein and carbohydrates. This characteristic can be advantageously used to search for suitable diets in abalone aquaculture. Published by Elsevier B.V.

Anderson, AE, Felbeck H, Childress JJ.  1990.  Aerobic metabolism is maintained in animal tissue during rapid sulfide oxidation in the symbiont-containing clam Solemya reidi. Journal of Experimental Zoology. 256:130-134.   10.1002/jez.1402560203   AbstractWebsite

Solemya reidi is a gutless clam that contains intracellular, symbiotic sulfur-oxidizing chemoautotrophic bacteria in its gills. It lives in burrows in highly reducing muds rich in sulfide, a compound toxic at low levels to aerobic respiration. In these habitats there is wide variation in levels of O2 and sulfide, both of which are metabolic requirements for this symbiosis. In order to assess whether the animal tissues utilize aerobic or anaerobic ATP-generating pathways in the presence of sulfide, and to determine the sulfide concentrations that might induce a shift to anaerobiosis, clams were incubated in varying levels of sulfide and oxygen. Symbiont-free foot tissues from clams incubated in various levels of sulfide (50–500 μM) were analyzed for a common substrate (aspartate) and product (succinate) of invertebrate anaerobic metabolism. The concentrations of these metabolites were compared with those found in tissues of aerobic and anaerobic controls. Aerobic metabolism was maintained in animal tissues in the presence of up to 100 μM sulfide, levels at which maximum autotrophy has been previously reported; however, at higher concentrations, where inhibition of autotrophy has been reported, the onset of anaerobic pathways was evident. This use of anaerobic pathways was not due to the absence of O2, the classical definition of anaerobiosis, but rather to the inhibitory effect of sulfide on aerobic metabolism. The metabolic flexibility of this species in regard to energy metabolism is clearly advantageous living as it does at the interface between a highly oxic environment and an anoxic, highly reducing one.

Arndt, C, Gaill F, Felbeck H.  2001.  Anaerobic sulfur metabolism in thiotrophic symbioses. Journal of Experimental Biology. 204:741-750. AbstractWebsite

Hydrogen sulfide is generally accepted to be the energy source for the establishment of sulfur-oxidizing symbiotic communities. Here, we show that sulfur-storing symbioses not only consume but also produce large amounts of hydrogen sulfide. The prerequisite for this process appears to be the absence of oxygen, Anaerobic sulfide production is widespread among different thiotrophic symbioses from vent and non-vent sites (Riftia pachyptila, Calyptogena magnifica, Bathymodiolus thermophilus, Lucinoma aequizonata and Calyptogena elongata), The extent of H2S generation correlates positively with the amount of elemental sulfur stored in the symbiont-bearing tissues of the hosts. Sulfide production starts a few hours after anoxia sets in, with H2S initially accumulating in the circulatory system before it is excreted into the surrounding environment. We propose that not sulfate but the elemental sulfur deposited in the symbionts serves as a terminal electron acceptor during anoxia and is reduced to sulfide. In anoxia-tolerant symbioses such as L. aequizonata, anaerobic sulfur respiration may be important for producing maintenance energy to help the species survive several months without oxygen, The increased levels of cysteine in the gills of L. aequizonata may be caused by a lack of reoxidation due to the absence of oxygen.

Arndt, C, Schiedek D, Felbeck H.  1998.  Anaerobiosis in the hydrothermal vent tube-worm Riftia pachyptila. Cahiers De Biologie Marine. 39:271-273. AbstractWebsite
Duplessis, MR, Dufour SC, Blankenship LE, Felbeck H, Yayanos AA.  2004.  Anatomical and experimental evidence for particulate feeding in Lucinoma aequizonata and Parvilucina tenuisculpta (Bivalvia : Lucinidae) from the Santa Barbara Basin. Marine Biology. 145:551-561.   10.1007/s00227-004-1350-6   AbstractWebsite

Previous nutritional models for adults of the lucinid bivalve Lucinoma aequizonata contend that symbiotic chemoautotrophic bacteria provide most of the organic carbon for the host. The existence of this symbiosis, coupled with the host's distinctive anatomical features, shaped the impression that particulate feeding was not a significant part of L. aequizonata nutrition. Here, we use several techniques to show that particulate feeding is a consistent and important part of the L. aequizonata nutritional strategy. Histological and scanning electron microscopy observations reveal that the gills of L. aequizonata, like those of the lucinid Parvilucina tenuisculpta, have functional mucociliary epithelia, able to transport captured particles to the mouth. Observations of gut content and radiolabeled feeding experiments indicate that L. aequizonata does ingest and assimilate carbon from particulate organic matter. Furthermore, molecular identification of a broad spectrum of organisms in the guts of native adult specimens demonstrates that L. aequizonata is non-selective when ingesting organic material, and has a mixotrophic diet.

Fiala-Medioni, A, Felbeck H.  1990.  Autotrophic processes in invertebrate nutrition: bacterial symbiosis in bivalve molluscs. Comparative Physiology. 5( Kinne RKH, Kinne-Saffran E, Beyenbach KW, Eds.).:49-68., Basel: Karger Abstract
Southward, AJ, Southward EC, Dando PR, Rau GH, Felbeck H, Flugel H.  1981.  Bacterial symbionts and low 13C/12C ratios in tissues of Pogonophora indicate unusual nutrition and metabolism. Nature. 293:616-620.   10.1038/293616a0   AbstractWebsite

Observations on fine structure, metabolic enzymes and stable isotope ratios of several species of Pogonophora from a wide range of habitats suggest that members of this enigmatic phylum of worm-like deep-sea animals use internal chemoauto -trophic bacteria as part of their nutrition, allowing them to exploit scarce nutrient and energy resources.

Felbeck, H, Childress JJ, Somero GN.  1983.  Biochemical interactions between molluscs and their symbionts. The mollusca Vol. 2, Environmental biochemistry and physiology. ( Hochachka PW, Ed.).:331-358., New York; London: Academic Press Abstract
Felbeck, H, Childress JJ, Somero GN.  1981.  Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature. 293:291-293.   10.1038/293291a0   AbstractWebsite

The role of sulphide oxidation-driven production of reduced carbon in the nutrition of animals adapted to life in sulphide-rich habitats such as the deep-sea hydrothermal vents and intertidal mudflats has been a topic of recent interest1–4. Chemoautotrophic sulphide-oxidizing bacteria have been isolated from samples of sulphide-rich vent water5–8, and it has been suggested that these could provide a food source for filter-feeding animals that live at the vents. The recent discovery of prokaryotic cells9 and activities of sulphide-oxidizing enzymes (which generate reducing power and ATP) and Calvin—Benson cycle enzymes10 within the trophosome tissue of the large vestimentiferan tubeworm of the vents, Riftia pachyptila Jones (Phylum Pogonophora)11 suggests that sulphide-oxidizing chemoauto-trophic bacteria exist in a symbiotic relationship with at least this vent species. This discovery led us to measure enzyme activities associated with sulphide oxidation, the Calvin-Benson cycle and nitrate reduction in a variety of other vestimentiferan tube-worms and bivalve molluscs which occur in sulphide-rich habitats. All the vestimentiferan worms and several of the molluscs were found to contain these enzymatic activities, suggesting that the putative animal-bacterial symbiosis first described in Riftia pachyptila may be of widespread occurrence in species living in environments offering simultaneous access to sulphide and oxygen.

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.

Felbeck, H.  1981.  Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera) . Science. 213:336-338.   10.1126/science.213.4505.336   AbstractWebsite

Trophosome tissue of the hydrothermal vent tube worm, Riftia pachyptila (Vestimentifera), contains high activities of several enzymes associated with chemoautotrophic existence. Enzymes catalyzing synthesis of adenosine triphosphate using energy contained in sulfur compounds such as hydrogen sulfide, and two diagnostic enzymes of the Calvin-Benson cycle of carbon dioxide fixation, ribulosebisphosphate carboxylase and ribulose 5-phosphate kinase, are present at high levels in trophosome, but are absent in muscle. These data are consistent with an autotrophic mode of nutrition for this worm, which lives in hydrogen sulfide-rich waters and lacks a mouth and digestive system.

Stein, JL, Cary SC, Hessler RR, Ohta S, Vetter RD, Childress JJ, Felbeck H.  1988.  Chemoautotrophic symbiosis in a hydrothermal vent gastropod. Biological Bulletin. 174:373-378.   10.2307/1541963   AbstractWebsite

An undescribed gastropod species collected from recently discovered deep-sea hydrothermal vents in the western Pacific contains endosymbiotic bacteria within specialized gill cells. The snails inhabit rocky vent openings where they are exposed directly to warm (2- 25°C) sulfide-rich (750 µM) water emitted from the vents. The gills of this snail contain elemental sulfur and high activities of enzymes catalyzing sulfide metabolism (sulfide oxidase, ATP-sulfurylase, APS-reductase, rhodanese) and autotrophic CO2 fixation (ribulose bisphosphate carboxylase) indicating that the bacteria function as sulfur oxidizing chemoautotrophic endosymbionts - a symbiosis described previously only in vestimentiferan and pogonophoran tubeworms, oligocheate worms, and bivalve molluscs. This represents the first documenta- tion of chemoautotrophic potential among the numerous gastropod species found inhabiting the interface of reducing and oxidizing 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.

Felbeck, H.  1985.  CO2 fixation in the hydrothermal vent tube worm Riftia pachyptila (Jones). Physiological Zoology. 58:272-281. AbstractWebsite
Felbeck, H, Liebezeit G, Dawson R, Giere O.  1983.  CO2 fixation in tissues of marine oligochaetes (Phallodrilus leukodermatus and P. planus) containing symbiotic, chemoautotrophic bacteria. Marine Biology. 75:187-191.   10.1007/bf00406001   AbstractWebsite

The gutless marine oligochaetes Phallodrilus leukodermatus and P. planus are known to contain bacteria in their tissues. In this study, we demonstrate that these worms, collected and studied 1982 in Bermuda, contain enzymes characteristic for chemoautotrophic bacteria, as has previously been shown for pogonophorans and some bivalve moliuscs. The enzymes are ribulose-1.5-diphosphate carboxylase (RuBPCase), ATP-sulfurylase, sulfite oxidase and nitrate reductase. Adenosinephosphosulfate reductase and rhodanese could not be detected. In addition, P. leukodermatus was tested for the ability to take up and metabolize radiolabeled bicarbonate and glucose from the surrounding seawater. During incubation periods of up to 6 h. most of the radioactivity administered as bicarbonate was found in malate and succinate; sugars and sugar phosphates were heavily labeled only after short incubation periods of up to 30 min. In comparison to bicarbonate, glucose was taken up from the medium slewly. The quantitative importance of the fixation of bicarbonate versus uptake of dissolved organic matter for the worms' metabolic needs are discussed.

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.

Garcia-Esquivel, Z, Felbeck H.  2009.  Comparative performance of juvenile red abalone, Haliotis rufescens, reared in laboratory with fresh kelp and balanced diets. Aquaculture Nutrition. 15:209-217.   10.1111/j.1365-2095.2008.00585.x   AbstractWebsite

Juvenile Haliotis rufescens were reared in the laboratory in order to investigate the extent to which fresh kelp and formulated feeds with 250 g kg(-1) (25P) and 380 g kg(-1) protein content (38P) affected their growth rate, gut residence time (GRT), food consumption (C), food conversion ratio (FCR) and digestibility. Abalone from 38P attained the highest growth rate (70.5 +/- 4.2 mu m day(-1); 98.3 +/- 6.95 mu g day(-1)), followed by 25P (47.9 +/- 2.79 mu m day(-1); 67.4 +/- 2.82 mu g day(-1)) and kelp (23.6 +/- 3.36 mu m day(-1); 28.2 +/- 4.11 mu g day(-1)). No significant differences were observed in consumption rate among treatments (0.61-0.68% body weight per day), yet kelp-fed abalone exhibited higher FCR (2.44), protein efficiency ratio (4.42), and apparent digestibility of dry matter (69.5%), protein (69.8%) and gross energy (79.2%) than 38P organisms (59.8, 62.4 and 62.2%, respectively). They also showed longer GRT (23.1 +/- 0.93 h). This study demonstrated that formulated diets with 250 g kg(-1) and 380 g kg(-1) protein inclusion can sustain higher growth rates of juvenile H. rufescens than fresh algae. These differences seem to be due to the amount of dietary protein. Kelp meal appears to improve the consumption and digestibility of balanced diets, and its inclusion in formulated diets is recommended.

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.

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 and D-amino acid oxidase (EC 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.

Gros, O, Liberge M, Heddi A, Khatchadourian C, Felbeck H.  2003.  Detection of the free-living forms of sulfide-oxidizing gill endosymbionts in the lucinid habitat (Thalassia testudinum environment). Applied and Environmental Microbiology. 69:6264-6267.   10.1128/aem.69.10.6264-6267.2003   AbstractWebsite

Target DNA from the uncultivable Codakia orbicularis endosymbiont was PCR amplified from sea-grass sediment. To confirm that such amplifications originated from intact bacterial cells rather than free DNA, whole-cell hybridization (fluorescence in situ hybridization technique) with the specific probe Symco2 was performed along with experimental infection of aposymbiotic juveniles placed in contact with the same sediment. Taken together, the data demonstrate that the sulfide-oxidizing gill endosymbiont of Codakia orbicularis is present in the environment as a free-living uncultivable form.

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.

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.

Stein, JL, Haygood M, Felbeck H.  1990.  Diversity of ribulose biphosphate carboxylase genes in sulfur-oxidizing symbioses. Endocytobiology IV : 4th International Colloquium on Endocytobiology and Symbiosis, INSA-Villeurbanne (France), July 4-8, 1989. ( Nardon P, Glaninazzi-Pearson V, Grenier AM, Margulis L, Smith DC, Eds.).:343-347., Paris: Institut national de la recherche agronomique Abstract