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1992
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, Distel DL.  1992.  Prokaryotic symbionts of marine invertebrates. The Prokaryotes : a handbook on the biology of bacteria : ecophysiology, isolation, identification, applications. 4( Balows A, Trueper HG, Dworkin M, Harder W, Schleifer KH, Eds.).:3891-3906., New York: Springer-Verlag Abstract
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1990
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.

Stein, JL, Haygood M, Felbeck H.  1990.  Nucleotide sequence and expression of a deep-sea ribulose-1,5-bisphosphate carboxylase gene cloned from a chemoautotrophic bacterial endosymbiont. Proceedings of the National Academy of Sciences of the United States of America. 87:8850-8854.   10.1073/pnas.87.22.8850   AbstractWebsite

The gene coding for ribulose-1,5-bisphosphate carboxylase [RuBisCO; 3-phospho-D-glycerate carboxy-lyase (dimerizing), EC 4.1.1.39] was cloned from a sulfur-oxidizing chemoautotrophic bacterium that resides as an endosymbiont within the gill tissues of Alvinoconcha hessleri, a gastropod inhabiting deep-sea hydrothermal vents. Nucleotide sequence analysis of the cloned fragment demonstrated that the genes encoding the large (RbcL) and small (RbcS) subunits of the symbiont RuBisCO were organized similarly to the RuBisCO operons of free-living photo- and chemoautotrophic prokaryotes. The symbiont rbcL gene shared the highest degree of nucleotide sequence identity with the cyanobacterium Anabaena (69%) while the rbcS nucleotide sequence shared 61% identity with that of the green alga Chlamydomonas reinhardtii. Comparison with a 153-nucleotide partial rbcL sequence from a symbiont of the bivalve Solemya reidi indicated that the two symbiont sequences shared 85% sequence identity at the nucleotide level and 93% at the amino acid level, suggesting a relatively recent common origin. Escherichia coli transformed with a plasmid carrying the RuBisCO operon of the gastropod symbiont in the proper orientation for transcription from the plasmid lac promoter expressed catalytically active RuBisCO. The presence of enzyme activity suggests the proper assembly of the subunits of this deep-sea RuBisCO into the holoenzyme.

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
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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
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Fiala-Medioni, A, Felbeck H, Childress JJ, Fisher CR, Vetter RD.  1990.  Lysosomic resorption of bacterial symbionts in deep-sea bivalves. 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.).:335-338., Paris: Institut national de la recherche agronomique Abstract
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Felbeck, H.  1990.  Symbiosis of bacteria with invertebrates in the deep sea. 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.).:327-334., Paris: Institut national de la recherche agronomique Abstract
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1989
Cary, SC, Vetter RD, Felbeck H.  1989.  Habitat characterization and nutritional strategies of the endosymbiont-bearing bivalve Lucinoma aequizonata. Marine Ecology-Progress Series. 55:31-45.   10.3354/meps055031   AbstractWebsite

A population of the lucinid bivalve Lucinorna aequizonata, with sulfur-oxidizing endosymbiotic bacteria in the gills, is restricted to a narrow depth range (500 ±10m) on the slope of the Santa Barbara Basin, California, USA. In this zone, the seawater just above the substratum is sub-oxic (O2 < 20 µM).The organically rich sediments in which these clams live are well mixed by bioturbation, which appears to maintain a redox condition limiting the extensive accumulation of hydrogen sulfide. However, thiol levels in the blood of the clams indicate an exposure to significant amounts of sulfide and/or thiosulfate apparently from randomly dispersed short-lived pockets of sulfidic mud that can be reached by the clam's burrowing vermiform foot. When the bivalves are incubated in the presence of hydrogen sulfide, thiosulfate is concentrated in the blood and apparently utilized by the bacteria for metabohc energy and the production of intracellular elemental sulfur. Laboratory growth experiments demonstrated that sulfide concentrations greater than 10 µM were detrimental to the host, even though the bacteria continued to accumulate elemental sulfur. The utilization of thiosulfate under near anaerobic conditions and the accumulation of intracellular elemental sulfur by the endosymbiotic bacteria coupled with the high availability of environmental nitrate and low molecular oxygen suggests a metabolic strategy analogous to the free-living sulfur oxidizer Thlobacillus denjtrificans. The δ13C values of the purified endosymbiont bacteria (-34.0 5 0.8‰) were significantly lighter than those of the host tissue (-29.0 +0.7‰)suggesting that in addition to the nutrition provided by the bacteria, over 25 % of the host carbon may be attributed to exogenous dissolved carbon which is in high concentrations in its natural habitat.

Cary, SC, Felbeck H, Holland ND.  1989.  Observations on the reproductive biology of the hydrothermal vent tube worm Riftia pachyptila. Marine Ecology-Progress Series. 52:89-94.   10.3354/meps052089   AbstractWebsite

On the Hydronaut Expedition to 13"N on the East Pacific Rise, we made some observations on the reproductive biology of Riftia pachyptila relevant to larval dispersal, symbiont acquisition, and sperm transfer. Two females spawned in a pressure chamber about 15 h after collection. During each 30 min spawning episode, the relatively small (105pm), lipid-rich eggs were emitted in large numbers from the female gonopores and floated upward in still seawater at about 2 cm min^-1. Therefore, it is likely that early development takes place in deep water well above the vent habitat of the adults. Two males spawned in non-pressurized aquaria about 45 min after reaching the deck of the ship. Semen issuing from the male gonopores contained sperm bundles, each composed of several hundred sperm wlth remarkable detached acrosomes. Each bundle swam vigorously through seawater by the beating of all its flagella In unison Motilty was not inhibited by hydrogen sulfide concentratlons greater than those at the vent habitat. After swimmlng for about 15 min, the bundles broke up into individual sperm that were relatively immotile. It is reasonable to assume that sperm bundles swim from the male to the female's tube or body where they adhere by their detached acrosomes before disintegrating into individual sperm that subsequently ferhhze the eggs.

Cary, C, Fry B, Felbeck H, Vetter RD.  1989.  Multiple trophic resources for a chemoautotrophic community at a cold water brine seep at the base of the Florida Escarpment. Marine Biology. 100:411-418.   10.1007/bf00391157   AbstractWebsite

The biological community that surrounds the hypersaline cold water brine seeps at the base of the Florida Escarpment is dominated by two macrofaunal species: an undescribed bivalve of the family Mytilidac and a vestimentiferan worm, Escarpia laminata. These animals are apparently supported by the chemoautotrophic fixation of carbon via bacterial endosymbionts. Water column and sediment data indicate that high levels of both sulfide and methane are present in surface sediments around the animals but absent from overlying waters. Stable isotopic analyses of pore water indicate that there are two sources of sulfide: the first is geothermal sulfide carried in groundwater leaching from the base of the escarpment, and the second is microbial sulfide produced in situ. The vestimentiferan E. laminata, and the mytilid bivalve (seep mussel) live contiguously but rely on different substrates for chemoautotrophy. Enzyme assays, patterns of elemental sulfur storage and stable isotopic analyses indicate that E. laminata relies on sulfide oxidation and the seep mussel on methane oxidation for growth.

1988
Fisher, CR, Childress JJ, Arp AJ, Brooks JM, Distel D, Favuzzi JA, Felbeck H, Hessler R, Johnson KS, Kennicutt MC, Macko SA, Newton A, Powell MA, Somero GN, Soto T.  1988.  Microhabitat variation in the hydrothermal vent mussel, Bathymodiolus thermophilus, at the Rose Garden vent on the Galapagos Rift. Deep-Sea Research Part a-Oceanographic Research Papers. 35:1769-1791.   10.1016/0198-0149(88)90049-0   AbstractWebsite

Clumps of Bathymodiolus thermophilus were collected from three discrete areas at the ‘Rose Garden’ site on the Galapagos Rift using the deep submersible Alvin. Two mussel collections were made from the central Riftia mass, an area associated with very active venting, and three other collections were of two different peripheral mussel clumps. Before collection the clumps were extensively photographed and the water at two of the ‘microhabitats’ was analysed in situ for oxygen silica, sulfide and temperature. Sulfide levels of up to 300 μM were recorded at the central collection site, while the highest sulfide level recorded at the peripheral site assayed was 35 μM. Levels of RuBP carboxylase activity in the gills were significantly higher in mussels collected from the central ‘Riftia site’ than in either peripheral site. ATP sulfurylase was significantly higher in the gills of mussels from the central clump than in one of the peripheral clump collections. The chemical composition (% water, protein, carbohydrate, lipid and ash) and stable carbon isotope ratios (δ13C) of the mussels showed the same trends, with highest lipid and carbohydrate and the lowest water content and δ13C in the central site mussels. Similarly, the mussels from the central site were significantly depleted in stable nitrogen (δ15N) when compared with the peripheral site mussels. Variations between sites and tissues of the same animal may be indicative of differential utilization of inorganic or dissolved molecular nitrogen sources. The condition index (CI = soft tissue dry mass / internal shell volume) was similar for all animals collected at Rose Garden. The presence of a commensal polychaete, Branchipolynoe symmytilida, in the mantle cavity of the mussels was also correlated with the collection site, with the highest incidence of occurrence in the central clump.Levels of the enzyme RuBP carboxylase are quite variable in B. thermophilus and are on the average much lower (0.001 international units) than either Calyptogena magnifica (0.006 I.U.) or Riftia pachyptila (0.16 I.U.). We conclude that the mussels are able to thrive over a wider range of conditions than either C. magnifica or R. pachypila and that this is due to a lesser reliance on their symbiotic bacteria as a source of nutrition.

Fisher, CR, Childress JJ, Arp AJ, Brooks JM, Distel DL, Dugan JA, Felbeck H, Fritz LW, Hessler RR, Johnson KS, Kennicutt MC, Lutz RA, Macko SA, Newton A, Powell MA, Somero GN, Soto T.  1988.  Variation in the hydrothermal vent clam, Calyptogen magnifica, at the Rose Garden vent on the Galapagos spreading center. Deep-Sea Research Part a-Oceanographic Research Papers. 35:1811-1831.   10.1016/0198-0149(88)90051-9   AbstractWebsite

Calyptogena magnifica occupy a relatively restricted habitat at the Rose Garden hydrothermal vent site on the Galapagos Rift. These clams are found in areas with very low flow of vent water and gain exposure to hydrogen sulfide by inserting their well-vascularized foot into cracks that contain this flow. Vent water is undetectable around the siphons of many of the individuals, and they therefore probably take up sulfide through their foot, and oxygen and inorganic carbon through their gills. Age estimates indicate that the bulk of the recruitment of C. magnifica occured between 1971 and 1976. Isotopic evidence indicates that symbionts are the main source of both nutritional carbon and nitrogen for the clams, and that the symbionts assimilate both of these substrates from inorganic sources. Carbohydrate and protein in the clam soft tissues, as well as the elemental sulfur content of their gills, decrease with increasing clam size. There is only slight variation in most of the parameters measured, and none of the parameters show nearly the variation seen in the other hydrothermal vent bivalve, Bathymodiolus thermophilus. However, several parameters, such as δ13C, condition index, and some bacterial enzyme activities, vary significantly with habitat.

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.

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.

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.

Felbeck, H, Childress JJ.  1988.  Riftia pachyptila, a highly integrated symbiosis. Oceanologica Acta. 8:131-138. Abstract
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1987
Childress, JJ, Felbeck H, Somero GN.  1987.  Symbiosis in the Deep-Sea. Scientific American. 256:114-121. AbstractWebsite
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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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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.

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.