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: 5.29). 03/1986; 227:227-247. DOI: 10.1098/rspb.1986.0021

ABSTRACT 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.

  • [Show abstract] [Hide abstract]
    ABSTRACT: Lucina pectinata is a large tropical Lucinidae which is characterized by abundant tissue hemoglobin in its deep-red gills. In the present paper, hemoglobin is described as being located in cytoplasmic dark patches of the bacteriocytes together with a cystine-rich protein. Large microbodies contain a non-hemoglobin heme-compound which is identified with a previously described non-protein-bound hematin; however, it has not been established whether this heme is involved in a sulphur-oxidizing system or represents a catabolic by-product of hemoglobin. Electron-lucent vesicles are associated with the basal microbodies but their function is, so far, unknown. In addition, the bacteriocytes have been observed to have direct contact with sea water, modulated by large intercalary cells which overlap the bacteriocytes on their margin. Such relationships between bacteriocytes and intercalary cells, as well as their cytological features, are different from those observed in lucinid species inhabiting sea-grass beds, but very similar to those observed in Calyptogena magnifica. From the congruence between the shallow-water Lucinidae L. pectinata, inhabiting mangrove swamps, and the deep-sea Vesicomyidae C. magnifica, found at hydrothermal vents, we conclude that such features are likely to be adaptative to high-sulphide environments, notwithstanding the phylogenetic distance.
    Marine Biology 01/1996; 125(3):511-524. · 2.39 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Spisula substruncata, a mactrid bivalve living in well-oxygenated sublittoral sandy bottoms, contains two types of intracellular bacteria in its gills. Chemoautotrophic metabolism of these bacteria was tested in different ways. Homogenates of gill tissues showed a slight ribulose — 1.5 — bisphosphate carboxylase activity. Fixation of 14C-labelled bicarbonate in S. subtruncata was higher than in Venus gallina, a clam without bacteria living in the same environment. Other experiments were performed with and without two reduced compounds (sodium thiosulphate and ammonium chloride) at different incubation times (45 to 300 min). With the two compounds, the levels of fixed carbon per g of gill tissue increased significantly after 60 min incubation. A possible ammonia utilization by gill bacteria is demonstrated and may be explained by the fact that the most abundant dissolved reduced compound available for chemoautotrophs is ammonia. The values obtained in this association were lower than those recorded for other bivalves with bacterial cells in their gills. These low values may be explained by the relatively small number of the two types of bacteria observed in the gills of S. subtruncata.
    Netherlands Journal of Sea Research 01/1989; 23(1):29-34.
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: SUMMARY Solemva reidi Bernard is a gutless clam that lives in burrows in reducing sediments, and harbours intracellular sulphur-oxidizing bacteria in its gills. Clams were incubated in various concentrations of sulphide and thiosulphate for up to 65 h in a flow-through respirometer. Fluxes were determined by continuous sampling of the respiratory medium with analysis of CO2, O2 and sulphide by gas chromatogra- phy and analysis of thiosulphate, sulphite (and sulphide) by HPLC using mono- bromobimane-denvatized discrete samples. Net CO2 uptake was shown to occur with exposure to 50—lOO^mol 1~' sulphide and greater than 225^moll~' thiosul- phate; sulphide oxidation and thiosulphate uptake were also demonstrated. 4S CaCO3 deposition in the shells of .S'. reidi was found to be insignificant compared to the net CO2 flux measured in the presence of low levels of sulphide. In experiments conducted under various O2 conditions, O2 limitation, produced by a combination of low (O2) and low water flow, was shown to inhibit sulphide oxidation and to prevent CO2 uptake. However, if O2 supply was not limited by low flow rates, in the presence of low (O2) (25-40 ^moll~') S. reidi showed rates of O2 and sulphide consumption and CO2 uptake near the maximum levels determined under high (O2) conditions, indicating the potential for net CO2 uptake in the low (O2) conditions presumed to exist in the animal's burrows. Thiosulphate levels in the blood of S. reidi were analysed and shown to increase rapidly during incubation in sulphide. These levels reached an apparent steady state (approx. 300|imoll~') in recently captured clams after 1 h of incubation. However, both O2 limitation and time in captivity (>43 days after capture) caused a marked increase in the blood thiosulphate levels, which exceeded 2 - 5mmoll~ 1 after 16 h of exposure to sulphide. These results indicate that blood thiosulphate is transported to the bacteria and further oxidized, and that sulphide and thiosulphate oxidation are oxygen-dependent. In analyses of gill tissues for elemental sulphur, we found a wide range in the levels of sulphur stores. Calculations indicated these to be a small fraction of the total flux of sulphur maintained during continuous sulphide oxidation. Estimates of CO2:O2: sulphide ratios suggest CO2 fixation efficiencies similar to those of chemolithoautotrophic bacteria. Assuming translocation and oxidation of symbiont-fixed organic compounds, the net uptake of CO2 by S. reidi in the presence