Chemoautotrophic Symbionts in the Gills of the Bivalve Mollusc Lucinoma borealis and the Sediment Chemistry of its Habitat

Proceedings of the Royal Society B: Biological Sciences (Impact Factor: 5.05). 03/1986; 227(1247):227-247. DOI: 10.1098/rspb.1986.0021


Lucinoma borealis has enlarged gills, which contain numerous prokaryotes in specialized cells (bacteriocytes) in the subfilamentar region. The gills also contain high concentrations of elemental sulphur and of a c-type cytochrome. Homogenates of gill tissue show ribulosebisphosphate carboxylase and phosphoribulokinase activity; they also show activity for adenylylsulphate reductase, an enzyme concerned in the oxidation of sulphur, and will phosphorylate ADP on the addition of sulphite or sulphide. Fixation of bicarbonate by gill tissue from starved animals is enhanced in the presence of 100 µM sulphide. The sediment in which the animals live contains 1-6 $\mu $g atoms per litre of dissolved iron and hence there is very little dissolved sulphide, 200 nM, or less (80 nmol dm-3 sediment). Thiosulphate concentrations are also low, 300 nM, or less (120 nmol dm-3 sediment). In contrast, there are acid-labile sulphide concentrations up to 14 mmol dm-3 and elemental sulphur concentrations up to 4 mg atom per cubic decimetre of sediment. The mean sulphate reduction rate in the sediment varied seasonally with temperature over the range 1640-4920 nmol sulphate reduced per hour per cubic decimetre. L. borealis was usually found below the region of maximum sulphate reduction. Hydrogen, methane and carbon monoxide concentrations were all 160 nmol dm-3, or less. Despite the low levels of dissolved sulphide the association between prokaryote and host appears to be able to exploit this habitat by the oxidation of reduced sulphur species; ways in which the bivalve may be able to extract these from the sediment are discussed. The bivalves may obtain half their carbon from the autotrophic prokaryotes.

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    • "Dando et al. (1985) have found that Lucinoma borealis, Myrtea spinifera (Montagu, 1803) and Thyasira flexuosa (Montagu, 1803), living in a community with the pogonophoran Siboglinum fiordicum Webb, had enzymes characteristic of the symbiosis in their ctenidia. Subsequentely, Dando et al. (1986) studied the gills of L. borealis and observed the presence of numerous prokaryotes in specialized cells (bacteriocytes) in the subfilamentar region of the gills, together with high concentrations of elemental sulphur and of a c-type cytochrome. Recently, Gros et al. (2000) "
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    ABSTRACT: Lucinoma kazani, a new deep-water species of Lucinidae from the Eastern Mediterranean Basin, is described and illustrated. The material was collected in the Anaximander Mountains, between Rhodes and Cyprus, Eastern Mediterranean. The first living specimens were collected during the Dutch ANAXIPROBE project in the Kazan volcano, at a depth of 1709 m. Later, during the MEDINAUT programme, both living specimens and shells were collected from several mud volcanoes at different depths in the Anaximander Mountains.This bivalve holds symbionts in the ctenidia, as do all previously studied Lucinidae. The type of habitat of this new species is gas-saturated mud, with high levels of methane, which diffuses upwards into a low-oxygen deep-water. Therefore, we consider this as evidence of a living cold seep community in the Eastern Mediterranean Sea.
    Deep Sea Research Part I Oceanographic Research Papers 06/2002; 49(6-49):991-1005. DOI:10.1016/S0967-0637(02)00010-9 · 2.57 Impact Factor
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    • "Cytoplasmic hemoglobin is characteristic ofthe gills of most bivalves housing sulfur-oxidizing symbionts (Dando et al., 1985; Wittenberg, 1985; Lucinoma bore a/is with symbionts may lack gill hemoglobin, Dando et al., 1986; Yoldia limatula with few or no symbionts has gill hemoglobin at high concentration, Wittenberg, 1985; Nucula proxima with no symbionts has gill hemoglobin at low concentrations, Doeller, Kraus, and Smith, un pub. data). "
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    ABSTRACT: Two different hemoglobins occur in nearly equal concentrations in the gill of the bivalve mollusc, Solemya velum (total hemoglobin concentration is 200 μM/kg wet weight gill). A spectrophotometric study of intact gill filaments demonstrates that in the absence of sulfide, the gill hemoglobin may be oxygenated and deoxygenated, with part (5-20%) in the aquoferric form. In the presence of sulfide, about half of the gill hemoglobin is rapidly and reversibly converted to ferric hemoglobin, which then binds sulfide to form ferric hemoglobin sulfide (ferric hemoglobin with sulfide ligated to the heme iron in the distal ligand position); the balance continues to bind oxygen as oxyhemoglobin. S. velum inhabits reduced marine sediments where oxygen and hydrogen sulfide meet, and houses a dense population of intracellular chemoautotrophic sulfur-oxidizing symbiotic bacteria in its gill. We suggest that gill hemoglobins may mediate sulfide and oxygen delivery to the bacterial symbiont. Because sulfide is the dominant electron donor to fuel the Solemya/bacteria symbiosis, a cytoplasmic sulfide-binding protein that prevents the spontaneous reaction of sulfide with oxygen may be of utility in the nutrition of the animal.
    Biological Bulletin 12/1988; 175(3):388. DOI:10.2307/1541730 · 1.64 Impact Factor
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    • "Within the shell, the foot and viscera of T. flexuosa and T. sarsi are flanked by two thick gills which range in colour from pinkish white in T. sarsi to purplebrown in T. flexuosa. The gill filaments are thick and contain numerous prokaryote cells between the cuticle and the cell membrane (Southward, 1986). These prokaryotes can be phagocytosed by the epidermal cells (Southward, "
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    ABSTRACT: The bivalves Thyasiraflexuosa and T. sarsi have enlarged gills which contain numerous prokaryotes. Gills from freshly collected animals contain high concentrations of elemental sulphur. Homogenates of gill tissue show activity for ribulosebisphosphate carboxylase, adenylylsulphate reductase, sulphate adenylyltransferase and sulphate adenylyltransferase (ADP), indicating that the prokaryotes are sulphur-oxidizing autotrophs. Both species can burrow to depths of 8 cm below the sediment surface and use their vermiform feet to construct channels penetrating deeper into the sediment. T.flexuosa and T. sarsi are scarce in sediments with high hydrogen sulphide concentrations and are not found in sediments where the sulphide zone is below their burrowing depth.
    Journal of the Marine Biological Association of the UK 11/1986; 66(04):915-929. DOI:10.1017/S0025315400048529 · 1.06 Impact Factor
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