An extremely dense layer of the purple sulfur bacterium Amoebobacter purpureus in the chemocline of meromictic Mahoney Lake (British Columbia) was investigated over a 2-yr period. Within this layer, sulfide, elemental sulfur, and polysulfides were the main species of reduced sulfur. The oxidative part of the sulfur cycle was dominated by anoxygenic photosynthesis of A. purpureus. During summer, when sulfide concentrations in the layer were limiting, intracellular sulfur became the main electron donor for photosynthesis. delta-34S determinations revealed that the intracellular sulfur reacts chemically with dissolved sulfide to form polysulfides. Polysulfide concentrations decreased over summer, accompanied by an increase in numbers of sulfur-reducing bacteria. Sulfate reduction was the major pathway of sulfide formation. The annual carbon requirement of sulfate-reducing bacteria in the chemocline (22.5 g C M-2 yr-1) was met by the photosynthetic C fixation of A. purpureus (33.5 g C m-2 yr-1). Carbon demand exceeded the concomitant C fixation temporarily in summer, however. The activities of biomass-degrading enzymes and the formation of volatile fatty acids were sufficient to provide the carbon substrates. Our data indicate that in Mahoney Lake, anoxygenic photosynthesis and sulfate reduction are only indirectly coupled via degradation and autolysis of photosynthetically formed biomass.