Immunochemical localization of ribulose-1,5-bisphosphate carboxylase in the symbiont-containing gills of
            <i>Solemya velum</i>
            (Bivalvia: Mollusca)

Cavanaugh, Colleen M.; Abbott, Marilyn S.; Veenhuis, Marten

doi:10.1073/pnas.85.20.7786

Cited by 28 publications

(22 citation statements)

References 15 publications

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“…The phylogenetic placement of the S. velum symbionts, to date limited to sequence analysis of the 5S rRNA, indicates that these symbionts also fall in the Proteobacteria gamma subdivision (31 The strong amplification from gill tissue DNA and lack of amplification from foot tissue DNA (Fig. 1) supports the conclusions from studies of enzyme activity, electron microscopy (9), and 5S rRNA sequences (31) 16S rRNA gene sequence. Amplified DNA, purified using low-melting-point agarose (29), was sequenced directly using synthetic oligonucleotide primers (19,36) and the U.S. Biochemical Sequenase Kit with glycerol (34% final concentration) added to the DNA denaturation step (37).…”

supporting

confidence: 61%

“…In this investigation we sought to establish the phylogenetic relationships and the species specificities of the symbionts of the protobranch bivalve Solemya velum Say, an Atlantic coast clam which has been studied as a shallowwater model of invertebrate-chemoautotroph associations (7,9,10). The phylogenetic placement of the S. velum symbionts, to date limited to sequence analysis of the 5S rRNA, indicates that these symbionts also fall in the Proteobacteria gamma subdivision (31 The strong amplification from gill tissue DNA and lack of amplification from foot tissue DNA (Fig.…”

mentioning

confidence: 99%

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Phylogenetic relationships of chemoautotrophic bacterial symbionts of Solemya velum say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis

1992

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The protobranch bivalve Solemya velum Say (Mollusca: Bivalvia) houses chemoautotrophic symbionts intracellularly within its gills. These symbionts were characterized through sequencing of polymerase chain reaction-amplified 16S rRNA coding regions and hybridization of an Escherichia coli gene probe to S. velum genomic DNA restriction fragments. The symbionts appeared to have only one copy of the 16S rRNA gene. The lack of variability in the 16S sequence and hybridization patterns within and between individual S. velum organisms suggested that one species of symbiont is dominant within and specific for this host species. Phylogenetic analysis of the 16S sequences of the symbionts indicates that they lie within the chemoautotrophic cluster of the gamma subdivision of the eubacterial group Proteobacteria.Procaryote-eucaryote associations in which marine invertebrates harbor chemoautotrophic bacteria as endosymbionts appear to be widespread in marine habitats such as deep-sea hydrothermal vents and coastal sediments (8,15). In such symbioses, the procaryotes utilize the energy released by the oxidation of reduced inorganic substrates, such as hydrogen sulfide, to fix carbon dioxide via the CalvinBenson cycle (7, 13). The hosts appear to derive nutrition from their endosymbionts and in turn provide the symbionts simultaneous access to the substrates from anoxic and oxic environments which are necessary for energy generation. Maintenance of such intracellular symbionts presents a novel metazoan acquisition of procaryotic energy generation and autotrophic carbon fixation.While the existence of chemoautotroph-invertebrate symbioses is now generally accepted, little is actually known about the symbionts observed in the tissues of any of the hosts because none have been cultured. Comparison of rRNA sequences has greatly facilitated the identification of bacteria, including unculturable microorganisms, and the elucidation of their natural relationships (38). Phylogenetic analysis of 16S rRNA sequences enabled Distel et al. (12) to establish that the chemoautotrophic symbionts of the hydrothermal vent tubeworm and five species of bivalves of the subclass Lamellibranchia are related and cluster in the gamma subdivision of the Proteobacteria (formerly purple photosynthetic bacteria), one of the 11 major groups of eubacteria (30).In this investigation we sought to establish the phylogenetic relationships and the species specificities of the symbionts of the protobranch bivalve Solemya velum Say, an Atlantic coast clam which has been studied as a shallowwater model of invertebrate-chemoautotroph associations (7, 9, 10). The phylogenetic placement of the S. velum symbionts, to date limited to sequence analysis of the 5S rRNA, indicates that these symbionts also fall in the Proteobacteria gamma subdivision (31). However, the small size of * Corresponding author. t Present address:

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confidence: 61%

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confidence: 99%

Phylogenetic relationships of chemoautotrophic bacterial symbionts of Solemya velum say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis

1992

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“…RubisCO activity is high in S. velum gills (5); further, this enzyme has been localized within the cytoplasm of the symbiotic bacteria by immunocytohistochemistry (6). Enzymes consistent with the oxidation of reduced inorganic sulfur compounds are present in the gills (7), and carbon fixation by intact gills is stimulated by the presence of sulfide and thiosulfate (5), indicating that the symbionts are sulfur-oxidizing chemoautotrophs.…”

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confidence: 96%

CO ₂ Uptake and Fixation by Endosymbiotic Chemoautotrophs from the Bivalve Solemya velum

Scott

Cavanaugh

2007

Appl Environ Microbiol

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Chemoautotrophic symbioses, in which endosymbiotic bacteria are the major source of organic carbon for the host, are found in marine habitats where sulfide and oxygen coexist. The purpose of this study was to determine the influence of pH, alternate sulfur sources, and electron acceptors on carbon fixation and to investigate which form(s) of inorganic carbon is taken up and fixed by the gamma-proteobacterial endosymbionts of the protobranch bivalve Solemya velum. Symbiont-enriched suspensions were generated by homogenization of S. velum gills, followed by velocity centrifugation to pellet the symbiont cells. Carbon fixation was measured by incubating the cells with 14 C-labeled dissolved inorganic carbon. When oxygen was present, both sulfide and thiosulfate stimulated carbon fixation; however, elevated levels of either sulfide (>0.5 mM) or oxygen (1 mM) were inhibitory. In the absence of oxygen, nitrate did not enhance carbon fixation rates when sulfide was present. Symbionts fixed carbon most rapidly between pH 7.5 and 8.5. Under optimal pH, sulfide, and oxygen conditions, symbiont carbon fixation rates correlated with the concentrations of extracellular CO 2 and not with HCO 3 ؊ concentrations. The half-saturation constant for carbon fixation with respect to extracellular dissolved CO 2 was 28 ؎ 3 M, and the average maximal velocity was 50.8 ؎ 7.1 mol min ؊1 g of protein ؊1 . The reliance of S. velum symbionts on extracellular CO 2 is consistent with their intracellular lifestyle, since HCO 3 ؊ utilization would require protein-mediated transport across the bacteriocyte membrane, perisymbiont vacuole membrane, and symbiont outer and inner membranes. The use of CO 2 may be a general trait shared with many symbioses with an intracellular chemoautotrophic partner.

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“…The symbiont cycle may be complex as bacterial shape is variable from coccoid-to rod-shaped, and dividing stages are rarely seen, suggesting strong host control. Carbon is fixed via the Calvin cycle (Cavanaugh, 1983;Cavanaugh et al, 1988), using energy derived from the oxidation of reduced sulfur, most likely through the APS pathway for which they possess enzymes (Kleiner et al, 2012;Stewart and Cavanaugh, 2006). Ammonia is the nitrogen source assimilated via a host-encoded glutamine synthetase (Lee et al, 1999).…”

Section: Solemyidaementioning

confidence: 99%

An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea

et al. 2013

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Deep-sea bivalves found at hydrothermal vents, cold seeps and organic falls are sustained by chemosynthetic bacteria that ensure part or all of their carbon nutrition. These symbioses are of prime importance for the functioning of the ecosystems. Similar symbioses occur in other bivalve species living in shallow and coastal reduced habitats worldwide. In recent years, several deep-sea species have been investigated from continental margins around Europe, West Africa, eastern Americas, the Gulf of Mexico, and from hydrothermal vents on the Mid-Atlantic Ridge. In parallel, numerous, more easily accessible shallow marine species have been studied. Herein we provide a summary of the current knowledge available on chemosymbiotic bivalves in the area ranging west-to-east from the Gulf of Mexico to the Sea of Marmara, and north-to-south from the Arctic to the Gulf of Guinea. Characteristics of symbioses in 53 species from the area are summarized for each of the five bivalve families documented to harbor chemosynthetic symbionts (Mytilidae, Vesicomyidae, Solemyidae, Thyasiridae and Lucinidae). Comparisons are made between the families, with special emphasis on ecology, life cycle, and connectivity. Chemosynthetic symbioses are a major adaptation to ecosystems and habitats exposed to reducing conditions. However, relatively little is known regarding their diversity and functioning, apart from a few "model species" on which effort has focused over the last 30 yr. In the context of increasing concern about biodiversity and ecosystems, and increasing anthropogenic pressure on oceans, we advocate a better assessment of the diversity of bivalve symbioses in order to evaluate the capacities of these remarkable ecological and evolutionary units to withstand environmental change

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Immunochemical localization of ribulose-1,5-bisphosphate carboxylase in the symbiont-containing gills of Solemya velum (Bivalvia: Mollusca)

Abstract: The distribution of the Calvin cycle enzyme ribulose-1,5-bisphosphate carboxylase (RbuP2Case; EC 4.1

Cited by 28 publications

References 15 publications

Phylogenetic relationships of chemoautotrophic bacterial symbionts of Solemya velum say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis

Phylogenetic relationships of chemoautotrophic bacterial symbionts of Solemya velum say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis

CO ₂ Uptake and Fixation by Endosymbiotic Chemoautotrophs from the Bivalve Solemya velum

An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea

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Immunochemical localization of ribulose-1,5-bisphosphate carboxylase in the symbiont-containing gills of Solemya velum (Bivalvia: Mollusca)

Abstract: The distribution of the Calvin cycle enzyme ribulose-1,5-bisphosphate carboxylase (RbuP2Case; EC 4.1

Cited by 28 publications

References 15 publications

Phylogenetic relationships of chemoautotrophic bacterial symbionts of Solemya velum say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis

Phylogenetic relationships of chemoautotrophic bacterial symbionts of Solemya velum say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis

CO 2 Uptake and Fixation by Endosymbiotic Chemoautotrophs from the Bivalve Solemya velum

An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea

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CO ₂ Uptake and Fixation by Endosymbiotic Chemoautotrophs from the Bivalve Solemya velum