Adaptations of a tropical swamp worm, alma emini, for subsistence in a H2S-rich habitat: evolution of endosymbiotic bacteria, sulfide metabolizing bodies, and novel processes of elimination of neutralized sulfide complexes

Abstract

The epithelial cell lining of the respiratory groove of Alma emini, an oligochaete glossoscolecid worm that lives in a hydrogen sulfide (H2S)-rich tropical swamp, was investigated by transmission electron microscopy to determine the underlying structural adaptations which enable the worm to subsist in a highly inimical habitat. The epithelium of the respiratory groove is made up of squamous cells with a highly amplified free epithelial surface. The cells are tightly packed with electron dense sulfur metabolizing bodies (SMBs) and contain endosymbiotic bacteria. Presence of sulfur in the electron dense SMBs was confirmed by X-ray microanalysis. Certain eukaryotic cells with prominent filopodia-like cytoplasmic extensions were observed under the epithelial cells and in the muscle tissue. The cells contained numerous heteromorphic endosymbiotic bacteria and scattered SMBs. Both the SMBs and the bacteria are reckoned to be involved in scavenging and detoxifying H2S. The removal of sulfide complexes was observed to occur through excision of blebs formed by epithelial cell membrane elaborations and by exocytosis of crystalline-like particles. These adaptive stratagems generally correspond with those that have been adopted by many marine and hydrothermal vent organisms that occupy sulfide-rich biomes. The congruent adaptive stratagems and ultrastructural morphologies in such a diverse community of organisms have been imposed by a common need to neutralize the insidious effects of H2S in their environments.