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

Abstract Background Vestimentiferan tubeworms are deep-sea colonizers, in which chemoautotrophic symbiosis was first observed. These animals are gutless and depend on endosymbiotic bacteria for organic compound synthesis and nutrition supply. Taxonomically, vestimentiferans belong to Siboglinidae and Annelida. Compared with other siboglinids, vestimentiferans are distinguished by high tolerance of the prevailing hydrogen sulfide in hydrothermal vents, rapid growth in local habitats, and a physical structure consisting of a thick chitinous tube. The metabolic mechanisms contributing to these features remain elusive. Results Comparative genomics revealed that unlike other annelids, vestimentiferans possessed trehaloneogenesis and lacked gluconeogenesis. Transcriptome and metabolome analyses detected the expression of trehalose-6-phosphate synthase/phosphatase (TPSP), the key enzyme of trehaloneogenesis, and trehalose production in vestimentiferan tissues. In addition to trehaloneogenesis, glycogen biosynthesis evidenced by packed glycogen granules was also found in vestimentiferan symbionts, but not in other Siboglinidae symbionts. Data mining and analyses of invertebrate TPSP revealed that the TPSP in Vestimentifera, as well as Cnidaria, Rotifera, Urochordata, and Cephalochordata, likely originated from Arthropoda, possibly as a result of transposon-mediated inter-phyla gene transfer. Conclusion This study indicates a critical role of bacterial glycogen biosynthesis in the highly efficient symbiont − vestimentiferan cooperation. This study provides a new perspective for understanding the environmental adaptation strategies of vestimentiferans and adds new insights into the mechanism of metabolic evolution in Metazoa. Video Abstract