Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalve-bacteria symbiosis

Abstract

Solemya borealis Totten was collected from anoxic sediments in Buzzards Bay, Massachusetts in April and July 1989 and examined for the presence of symbiotic, chemoautotrophic bacteria. In addition, sediment cores collected at the same site were analyzed throughout the year, to provide a detailed description of the S. borealis habitat. Here we present structural, enzymatic, biochemical, and stable isotope data which suggests that S. borealis, like the related species Solemya velum Say and Solemya reidi Bernard, contains high concentrations of symbiotic chemoautotrophic bacteria in gill bacteriocytes which play a significant role in nutrition. Transmission electron microscopy revealed the presence of rod-shaped cells, which resemble Gram-negative bacteria, within gill epithelial cells. Ribulose-1,5-bisphosphate carboxylase activity in cell-free extracts of S. borealis gill tissue was comparable with that found in other invertebrate-chemoautotroph symbioses. Very negative δ34S ratios (-32.6 to-15.7‰) suggest the utilization of porewater sulfides as both an energy and a sulfur source for the symbionts. Carbon and nitrogen stable isotope ratios were extremely negative (δ13C=-32 to-34.6‰, δ15N=-9.7 to-8.6‰), similar to those of other bivalve-chemoautotroph symbioses. High concentrations of cis-vaccenic acid, a fatty acid previously found in other invertebrate-chemoautotroph symbioses, were found in all the major lipid classes of the gills of S. borealis. The stable isotope ratios and lipid composition of S. borealis suggest that most of this bivalve's nutritional requirements are supplied by bacterial endosymbionts. High levels of taurine in the free amino acid pool of S. borealis suggest the existence of unusual amino acid metabolic pathways which may be the result of endosymbiont activity. The S. borealis specimens were found in relatively shallow water sediments dominated by silts and clays. The sediments contain high concentrations of organic carbon and nitrogen, exhibit limited oxygen penetration, and have high rates of ammonium and sulfide input from the anaerobic microbial community. Sediment C and N stable isotope ratios reflect the input of algal-derived nutrients to the sediments (δ13C=-20.7 to-20.9‰, δ15N=+7.7 to +20.8‰). Sediment δ34S ratios ranged from-18.7 to-25.1‰ demonstrating the presence of sulfur produced by bacterial dissimilatory sulfate reduction processes.