Integrated multi-approaches reveal unique metabolic mechanisms of Vestimentifera to adapt to deep-sea hydrothermal vents

Vestimentiferans (Siboglinidae, Polychaeta) thrive in deep-sea hydrothermal vents and depend on chemosynthetic symbiosis for nutrition. Currently, the central carbon metabolisms, especially the sugar synthesis pathways, of vestimentiferans remain obscure. In this study, the genome of the vestimentiferan Arcovestia ivanovi was obtained. Comparative genomics revealed that, unlike other Polychaeta, vestimentiferans possessed trehaloneogenesis and lacked gluconeogenesis. Transcriptome and metabolome detected the expression of trehalose-6-phosphate synthase (TPS), the key enzyme of trehaloneogenesis, and trehalose in vestimentiferan tissues, especially trophosome, suggesting the possibility of trehalose as the main blood sugar in vestimentiferans. Vestimentiferan TPS was most closely related to arthropod TPS and may be transferred from arthropods via transposons that existed in high densities around the vestimentiferan and arthropod TPS loci. Electron microscopy observed vestimentiferan symbionts with packed glycogen granules. Consistently, glycogen biosynthesis was present in vestimentiferan symbionts but absent in other Siboglinidae symbionts. Together this study revealed that vestimentiferans have evolved unique metabolic mechanisms to adapt to hydrothermal vents by utilizing trehaloneogenesis as the major sugar-synthesizing pathway, which produces trehalose to facilitate tolerance of the stresses (such as high temperature and H2S) of the vents. This study also indicated a critical role of bacterial glycogen biosynthesis in the highly efficient symbiont-vestimentiferan cooperation.