Anaerobic sulfur metabolism in thiotrophic symbioses

Abstract

Hydrogen sulfide is generally accepted to be the energy source for the establishment of sulfur-oxidizing symbiotic communities. Here, we show that sulfur-storing symbioses not only consume but also produce large amounts of hydrogen sulfide. The prerequisite for this process appears to be the absence of oxygen. Anaerobic sulfide production is widespread among different thiotrophic symbioses from vent and non-vent sites (Riftia pachyptila, Calyptogena magnifica, Bathymodiolus thermophilus, Lucinoma aequizonata and Calyptogena elongata). The extent of H2S generation correlates positively with the amount of elemental sulfur stored in the symbiont-bearing tissues of the hosts. Sulfide production starts a few hours after anoxia sets in, with H2S initially accumulating in the circulatory system before it is excreted into the surrounding environment. We propose that not sulfate but the elemental sulfur deposited in the symbionts serves as a terminal electron acceptor during anoxia and is reduced to sulfide. In anoxia-tolerant symbioses such as L. aequizonata, anaerobic sulfur respiration may be important for producing maintenance energy to help the species survive several months without oxygen. The increased levels of cysteine in the gills of L. aequizonata may be caused by a lack of reoxidation due to the absence of oxygen.