Net uptake of CO2 driven by sulphide and thiosulphate oxidation in the bacterial symbiont-containing clam Solemya reidi

• Published in: Journal of experimental biology Vol. 133; no. 1; pp. 1 - 31
• Main Authors: ANDERSON, A. E, CHILDRESS, J. J, FAVUZZI, J. A
• Format: Journal Article
• Language: English
• Published: Cambridge Company of Biologists 01-11-1987
• Subjects: Biological and medical sciences; Fundamental and applied biological sciences. Psychology; Invertebrates; Mollusca; Physiology. Development; Marine environment; Symbiosis; Sulfides; Energy metabolism; Bivalvia; Bacteria; Chemoautotrophy; Oxidation; Invertebrata; Mollusca; Respiration
• ISSN: 0022-0949; 1477-9145
• DOI: 10.1242/jeb.133.1.1

ABSTRACT
Solemya 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 chromatography and analysis of thiosulphate, sulphite (and sulphide) by HPLC using mono-bromobimane-derivatized discrete samples. Net CO2 uptake was shown to occur with exposure to 50–100 μmol l−1 sulphide and greater than 225 μmoll−1 thiosulphate; sulphide oxidation and thiosulphate uptake were also demonstrated. 45CaCO3 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 μmol l−1) 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 μmoll−1) 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 2·5 mmol l−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 of reduced sulphur compounds suggests that this intact symbiosis may be able to meet its organic carbon needs through autotrophy.