Sulfide oxidation and carbon fixation by the gutless clamSolemya reidi: an animal-bacteria symbiosis

Abstract

Solemya reidi, a protobranch clam lacking a digestive system and found exclusively in habitats rich in hydrogen sulfide (HS−), contains high densities of gram-negative bacteria within certain cells (“bacteriocytes”) of its large gills (Fig. 1). These bacteria are proposed to be responsible for the capacity ofS. reidi to oxidize HS− (Fig. 2) and produce sulfate. Some of the energy released during HS− oxidation could provide the necessary ATP and reducing power for the net fixation of CO2 via the reactions of the Calvin-Benson cycle, which have been found in the gills, but in no other tissues, of this clam.Solemya reidi exhibited a rapid fixation of H14CO3− compared to other clams and a fast transfer of label into a variety of metabolites, the labeling pattern varying with time of incubation (Tables 2–3). The CO2 fixation mechanism inS. reidi appears to involve an initial trapping of CO2 into a four-carbon compound (Table 2), which subsequently is decarboxylated to generate CO2 for the ribulose-1,5-bisphosphate carboxylase reaction of the Calvin-Benson cycle. Aspartate and malate were the major sites of14C during short-term incubations of intact clams or isolated gills; longer incubation periods led to appearance of radioactivity in a variety of amino acids and carboxylic acids. Of several carboxylating enzymes tested, only pyruvate carboxylase was found in gill tissue.Solemya reidi is capable of absorbing dissolved organic molecules from seawater (Tables 4 and 5). These findings indicate thatS. reidi may be nourished by reduced carbon and nitrogen compounds synthesized by symbiotic bacteria housed within its gills, and by dissolved organic material present in the muds in which the animal lives. The metabolic organization of this species is discussed in relation to the animal-bacteria symbioses recently discovered at the deep-sea hydrothermal vent sites where HS− may play an important role in driving primary productivity.