The hydrocarbon seep tubeworm Lamellibrachia luymesi primarily eliminates sulfate and hydrogen ions across its roots to conserve energy and ensure sulfide supply

Abstract

SUMMARY Lamellibrachia luymesi (Polychaeta, Siboglinidae) is a deep-sea vestimentiferan tubeworm that forms large bush-like aggregations at hydrocarbon seeps in the Gulf of Mexico. Like all vestimentiferans, L. luymesi obtains its nutrition from sulfide-oxidizing endosymbiotic bacteria, which it houses in an internal organ called the trophosome. This tubeworm has a lifespan of over 170 years and its survival is contingent upon the availability of sulfide during this long period. In sediments underlying L. luymesi aggregations, microbes produce sulfide by coupling sulfate reduction with hydrocarbon oxidation. L. luymesi acquires sulfide from the sediment using a root-like posterior extension of its body that is buried in the sediment. Its symbionts then oxidize the sulfide to produce energy for carbon fixation, and release sulfate and hydrogen ions as byproducts. It is critical for the tubeworm to eliminate these waste ions, and it could do so either across its vascular plume or across its root. In this study, we measured sulfate and proton elimination rates from live L. luymesi and found that they eliminated approximately 85% of the sulfate produced by sulfide oxidation, and approximately 67% of the protons produced by various metabolic processes, across their roots. On the basis of experiments using membrane transport inhibitors, we suggest that L. luymesi has anion exchangers that mediate sulfate elimination coupled with bicarbonate uptake. Roots could be the ideal exchange surface for eliminating sulfate and hydrogen ions for two reasons. First, these ions might be eliminated across the root epithelium using facilitated diffusion, which is energetically economical. Second, sulfate and hydrogen ions are substrates for bacterial sulfate reduction, and supplying these ions into the sediment might help ensure a sustained sulfide supply for L. luymesi over its entire lifespan.