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1979
Felbeck, H.  1979.  Rolle der Aminosaeuren im Stoffwechsel von Arenicola marina: Bedeutung fuer Anaerobiose und Osmoregulation. Ph. D.:78., Muenster: Westfaelische Wilhelms-Universitaet Abstract
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1980
Felbeck, H, Grieshaber MK.  1980.  Investigations on some enzymes involved in the anaerobic metabolism of amino acids of Arenicola marina L.. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology. 66:205-213.   10.1016/0305-0491(80)90054-1   AbstractWebsite

1. Glutamate oxalacetate transaminase, glutamate pyruvate transaminase, and malate dehydrogenase were isolated from body wall musculature of the lugworm Arenicola marina and some properties (molecular weight, pH-optima and Km-values) were analyzed. 2. The steady state concentrations of aspartate, alanine, succinate, and pyruvate and their alterations during 6 hr of anaerobic incubation were determined. 3. A model of “reductive transamination” is discussed.

Felbeck, H.  1980.  Investigations on the role of the amino acids in anaerobic metabolism of the lugworm Arenicola marina L.. Journal of Comparative Physiology. 137:183-192. AbstractWebsite

1) 14C-Aspartate or15N-glutamate were injected into intact lugworms which subsequently were subjected to experimental anaerobiosis. The distribution of the label after different periods of anoxia was analyzed.2) After two hours most of the radioactivity of14C-aspartate was recovered in malate and succinate.3) An increase of alanine was observed during an early phase of anaerobiosis which is probably correlated to the decrease of aspartate. However,d-alanine was found to arise in quantities similar to those ofl-alanine. Therefore, metabolism of aspartate does not account for the total alanine accumulated. A correlation between the opposite changes of the two amino acids was demonstrated by the distribution of15N between alanine and applied glutamate. In addition, inhibition of glutamate pyruvate transaminase by aminooxyacetate resulted in a delay of aspartate utilization, i.e. glutamate oxalacetate transaminase was influenced indirectly.4) Glycine which is present in very high concentrations in the body wall musculature ofArenicola, was not metabolized in significant quantities.5) The lugworms took up alanine and glycine from the surrounding water until their concentrations fell to about 15 μmol/l. The uptake of the amino acids, however, occurred only in the presence of oxygen.6) The possible role of aspartate in the anaerobic metabolism of Arenicola is discussed.

1981
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.  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.  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.

1982
Felbeck, H, Somero GN.  1982.  Primary production in deep-sea hydrothermal vent organisms: roles of sulfide-oxidizing bacteria. Trends in Biochemical Sciences. 7:201-204.   10.1016/0968-0004(82)90088-3   AbstractWebsite

The dense aggregations of animal and bacterial life at the deep-sea hydrothermal vents are supported, at least in part, by sulfide-energy-based primary productivity. Sulfide-oxidizing bacteria are found free-living in the vent waters, on the surface of basaltic rocks, and as symbionts within certain tissues of the large vent tube worms and bivalve molluscs.

1983
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
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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.  1983.  Sulfide oxidation and carbon fixation by the gutless clam Solemya reidi: an animal-bacteria symbiosis. Journal of Comparative Physiology. 152:3-11. AbstractWebsite

Solemya reidi, a protobranch clam lacking a digestive system and found exclusively in habitats rich in hydrogen sulfide (HS−), contains high densities of gram-negative bacteria within certain cells (“bacteriocytes”) of its large gills (Fig. 1). These bacteria are proposed to be responsible for the capacity ofS. reidi to oxidize HS− (Fig. 2) and produce sulfate. Some of the energy released during HS− oxidation could provide the necessary ATP and reducing power for the net fixation of CO2 via the reactions of the Calvin-Benson cycle, which have been found in the gills, but in no other tissues, of this clam.Solemya reidi exhibited a rapid fixation of H14CO 3 − compared to other clams and a fast transfer of label into a variety of metabolites, the labeling pattern varying with time of incubation (Tables 2–3). The CO2 fixation mechanism inS. reidi appears to involve an initial trapping of CO2 into a four-carbon compound (Table 2), which subsequently is decarboxylated to generate CO2 for the ribulose-1,5-bisphosphate carboxylase reaction of the Calvin-Benson cycle. Aspartate and malate were the major sites of14C during short-term incubations of intact clams or isolated gills; longer incubation periods led to appearance of radioactivity in a variety of amino acids and carboxylic acids. Of several carboxylating enzymes tested, only pyruvate carboxylase was found in gill tissue.Solemya reidi is capable of absorbing dissolved organic molecules from seawater (Tables 4 and 5). These findings indicate thatS. reidi may be nourished by reduced carbon and nitrogen compounds synthesized by symbiotic bacteria housed within its gills, and by dissolved organic material present in the muds in which the animal lives. The metabolic organization of this species is discussed in relation to the animal-bacteria symbioses recently discovered at the deep-sea hydrothermal vent sites where HS− may play an important role in driving primary productivity.

1984
Giere, O, Felbeck H, Dawson R, Liebezeit G.  1984.  The gutless oligochaete Phallodrilus leukodermatus Giere, a tubificid of structural, ecological and physiological relevance. Hydrobiologia. 115:83-89.   10.1007/bf00027897   AbstractWebsite

Phallodrilus leukodermatus is not only characterized by the complete absence of mouth, gut, anus and nephridia, but also by an exceptional dermal ultrastructure which is associated with gram-negative bacteria. The vertical distribution of the worms from Bermudian carbonate sands is also unusual in attaining population maximum at oligoxic or anoxic depths around the redox discontinuity (RPD) layer, where extremely high concentrations of amino acids and sugars are to be recorded. Based on results from current ecophysiological and ultrastructural studies, an interpretation of the unique biology of the worms is attempted.

1985
Felbeck, H.  1985.  CO2 fixation in the hydrothermal vent tube worm Riftia pachyptila (Jones). Physiological Zoology. 58:272-281. AbstractWebsite
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Felbeck, H, Powell MA, Hand SA, Somero GN.  1985.  Metabolic adaptations of hydrothermal vent animals. Proc. Biol. Soc. Wash.. 6:261-272. Abstract
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Felbeck, H.  1985.  Occurrence and metabolism of D-aspartate in the gutless bivalve Solemya reidi. Journal of Experimental Zoology. 234:145-149.   10.1002/jez.1402340116   AbstractWebsite

High concentrations of free D-aspartate were measured in foot tissue and symbiotic bacteria containing gill tissue of Solemya reidi. The enzyme D-aspartate racemase could be shown to be present in the tissues but not D-aspartate oxidase or glutamate oxaloacetate transaminase (D-aspartate as substrate). Externally administered radiolabeled D-aspartate is rapidly taken up and metabolized by the tissues of the animal. The possible role of D-aspartate in the metabolism of S. reidi is discussed.

Schweimanns, M, Felbeck H.  1985.  Significance of the occurrence of chemoautotrophic bacterial endosymbionts in lucinid clams from Bermuda. Marine Ecology-Progress Series. 24:113-120.   10.3354/meps024113   AbstractWebsite

Five species of lucinid clams from Bermuda (Codakia costata, Ctena orbiculata, Par- vilucina multilineata, Lucina radians, Anodontia philippiana) had ribulose-1.5-bisphosphate carboxyl- ase activity in the gills. Presence of this enzyme of the Calvin-Benson cycle along with dark coloration of gills and morphologically simplified digestive tract strongly suggests presence of chemoautotrophic bacteria living symbiotically with the clams. Natural history is described for these 5 lucinids and several others not studied biochemically All inhabit reduced sediments rich in organic matter, where hydrogen sulfide is detectable. Results, along wlth previously published studies, indlcate that most clams of the family Lucinidae live symbiotically with chemoautotrophic bacteria in their gills and inhabit sulfide-rich environments.

1987
Distel, DL, Felbeck H.  1987.  Endosymbiosis in the lucinid clams Lucinoma aequizonata, Lucinoma annulata and Lucina floridana: a reexamination of the functional morphology of the gills as bacteria-bearing organs. Marine Biology. 96:79-86.   10.1007/bf00394840   AbstractWebsite

A three-dimensional representation of the structure of the endosymbiont-containing gills of Lucinoma aequizonata, L. annulata and Lucina floridana was constructed using light and electron microscopy of fresh and plastic-embedded thin-sectioned samples. The gills of these lucinids are identical in overall structure, each being composed of three structurally and functionally distinct regions here called the ctenidial filament zone (CFZ), the transition zone (TZ), and the bacteriocyte zone (BZ). Rather than a simple medial extension of the filament tissue, the bacteriocyte tissue is organized as an array of cylindrical tubes, the walls of which are composed primarily of bacteriocyte cells covered by a thin microvillar epithelium. The physical relationship between the symbionts, the host tissues and the external environment are examined, and structural constraints on the potential functions of bacteria in this host-symbiont system are discussed.

Felbeck, H, Wiley S.  1987.  Free D-amino acids in the tissues of marine bivalves. Biological Bulletin. 173:252-259.   10.2307/1541877   AbstractWebsite
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Childress, JJ, Felbeck H, Somero GN.  1987.  Symbiosis in the Deep-Sea. Scientific American. 256:114-121. AbstractWebsite
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1988
Felbeck, H, Childress JJ.  1988.  Riftia pachyptila, a highly integrated symbiosis. Oceanologica Acta. 8:131-138. Abstract
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Cary, SC, Fisher CR, Felbeck H.  1988.  Mussel growth supported by methane as sole carbon and energy source. Science. 240:78-80.   10.1126/science.240.4848.78   AbstractWebsite

Symbioses between chemoautotrophic bacteria and several specialized marine invertebrates are well documented. However, none of these symbioses have been demonstrated to provide sufficient energy and carbon to the host to enable it to grow. Growth rates of seep mussels collected from hydrocarbon seeps off the coast of Louisiana were measured in a controlled environment where methane was the sole carbon and energy source. The growth rates increased to a maximum of 17.2 micrometers per day in response to methane and approached zero in the absence of methane. These mussels contain methanotrophic symbiotic bacteria in their gills, which suggests that these bacteria provide their hosts with a net carbon flux originating from methane.

Distel, DL, Felbeck H.  1988.  Pathways of inorganic carbon fixation in the endosymbiont-bearing lucinid clam Lucinoma aequizonata. Part 1. Purification and characterization of the endosymbiotic bacteria. Journal of Experimental Zoology. 247:1-10.   10.1002/jez.1402470102   AbstractWebsite

Two simple techniques by which the sulfur-oxidizing endosymbiotic bacteria may be purified from the bacteriocyte tissues of the marine bivalve Lucinoma aequizonata, are described. Tissue homogenates are prepared from symbiont-containing tissues, and symbionts are recovered by centrifugation through gradients of Percoll density gradient medium. The high density of the endosymbionts (probably because of the presence of numerous sulfur deposits within the cells) allows clean, rapid, and efficient separation of these cells from host cells and cell constituents. Light and electron microscopy and enzymatic and biochemical techniques are used to demonstrate the identity, quality, and purity of the symbiont isolates from this lucinid clam. The techniques described here for L. aequizonata, have also been used successfully to purify sulfur-oxidizing endosymbionts from a variety of marine invertebrates, including the bivalves L. annulata, Lucina floridana, Calyptogena magnifica, and Codakia orbicularis, and from the vestimentiferan tubeworms Riftia pachyptila, and Tevnia jerichonana. Such preparations should prove useful for investigating these and similar sulfur-oxidizing symbioses.

Distel, DL, Felbeck H.  1988.  Pathways of inorganic carbon fixation in the endosymbiont-bearing lucinid clam Lucinoma aequizonata. Part 2. Analysis of the individual contributions of host and symbiont cells to inorganic carbon assimilation. Journal of Experimental Zoology. 247:11-22.   10.1002/jez.1402470103   AbstractWebsite

The incorporation of 14C from H14CO−3 into acid-soluble metabolites was examined in the endosymbiont-containing gills and purified symbionts of the lucinid clam Lucinoma aequizonata. HPLC, paper chromatography, and enzymatic techniques were used to identify and quantify compounds into which label was incorporated in continuous and pulse-labeling experiments. Both symbiont and host cells fix carbon in considerable quantities; however, each incorporates carbon into a distinctly different subset of compounds. In intact gills the initial carbon fixation product is malate. Label subsequently accumulates in succinate, glucose phosphate, glutamate, alanine, and glycogen. In the symbiont cells carbon is incorporated into aspartate, 3-phosphoglycerate, malate, and citrate. Purified symbionts incorporate carbon into the same compounds in the same proportions as do symbionts that are exposed to labeled H14CO−3 while still within the host tissues. Under the conditions tested, purified symbionts released no significant quantities of labeled compounds into the incubation medium.

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

Distel, DL, Lane DJ, Olsen GJ, Giovannoni SJ, Pace B, Pace NR, Stahl DA, Felbeck H.  1988.  Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences.. Journal of Bacteriology. 170:2506-2510. AbstractWebsite

The 16S rRNAs from the bacterial endosymbionts of six marine invertebrates from diverse environments were isolated and partially sequenced. These symbionts included the trophosome symbiont of Riftia pachyptila, the gill symbionts of Calyptogena magnifica and Bathymodiolus thermophilus (from deep-sea hydrothermal vents), and the gill symbionts of Lucinoma annulata, Lucinoma aequizonata, and Codakia orbicularis (from relatively shallow coastal environments). Only one type of bacterial 16S rRNA was detected in each symbiosis. Using nucleotide sequence comparisons, we showed that each of the bacterial symbionts is distinct from the others and that all fall within a limited domain of the gamma subdivision of the purple bacteria (one of the major eubacterial divisions previously defined by 16S rRNA analysis [C. R. Woese, Microbiol. Rev. 51: 221-271, 1987]). Two host specimens were analyzed in five of the symbioses; in each case, identical bacterial rRNA sequences were obtained from conspecific host specimens. These data indicate that the symbioses examined are species specific and that the symbiont species are unique to and invariant within their respective host species.