Different Nitrogen Sources Fuel Symbiotic Mussels at Cold Seeps

Abstract

Cold seeps globally host dense unique oasis-type ecosystems, mainly fuelled by chemosynthetic microorganisms via reduced gases such as methane and hydrogen sulfide. However, the origin and pathway of nitrogen chemosynthesis in this widely distributed symbiont ecosystem remain poorly understood. Here, we explore biomarker methods (bulk stable isotope, amino acid (AA), fatty acid (FA) and compound-specific isotope analyses in gill tissues of mussels) to demonstrate the relative contributions of inorganic and organic nitrogen to symbiotic mussels at cold seeps in the South China Sea and their impact on the synthesis and metabolism of amino acids. Gigantidas platifrons (G. platifrons) symbioses with type II methanotrophs via the Serine pathway, and Bathymodiolus aduloides (B. aduloides) thrives with sulfur-oxidizing bacteria via the Calvin pathway, as revealed by bulk δ13C and δ13C of FAs. Based on the δ15N values in gill tissues of mussels, organic nitrogen from sediment is estimated as the dominant nitrogen source for B. aduloides (97-98%), in contrast, NH4+ was the main nitrogen source for G. platifrons. Different dominant nitrogen sources result in the δ15N of AAs in the gills of two mussel species having opposite trends, which might be related to synthesis and metabolism of AAs in symbiotic bacteria and host, respectively. Our findings reveal that the mechanism of nitrogen acquisition in cold seep systems is plastic and related to DIN sources/uptake and changing environmental conditions. These findings uncover novel biosynthesis of nitrogen in the deep sea, typically at cold seeps, and may have important implications for nitrogen biogeochemistry and deep-sea conservation.

Trophic diversity of chemosymbiont hosts in deep-sea hydrothermal vents using amino acid nitrogen isotopes

“…If symbiont hosts consume microbially resynthesized energy in addition to the energy newly synthesized by symbionts, this suggests that they play a dual role as primary consumers and detritivores, contributing to vent energy recycling. The use of d 15 N AA values as an indicator of chemosynthetic sources and mechanisms of nitrogen utilization has been proven in cold seeps (Vokhshoori et al, 2021;Wang et al, 2022) and shallow water hydrothermal vents (depth > 30m) (Chang et al, 2018), This study is the first to explore TP in deep-sea (> 2,000 m) hydrothermal vents with no or negligible contribution of photosynthetic OM. We believe that this study contributes to improving the interpretation of d 15 N AA values to better understand the function and energetics of deep-sea hydrothermal vent ecosystems.…”