Nitrogen isotopic composition of amino acids reveals a variety of trophic ecology of organisms inhabiting chemosynthesis-based ecosystems

Abstract To understand the trophic interactions between various organisms in chemosynthesis-based ecosystems (CBEs) and the metabolic interaction between host animal and its symbiont, we estimated the trophic position (TP) using the stable nitrogen isotopic compositions of glutamic acid and phenylalanine. We demonstrated that estimating TP based on the isotopic composition of amino acids is a valuable tool for understanding photosynthetic prey-predator interactions among marine organisms, and it can also be applied to chemosynthesis-based food webs involving host-symbiont interactions. In CBEs, the nitrogen isotope ratio of phenylalanine ranged from − 15‰ to + 13‰, suggesting a wide variety of nutritional sources for organisms. Our results revealed that organisms in CBEs can be categorized into two main groups: those that depend on chemosynthetic organic matter and those that depend on photosynthetic organic matter from the ocean surface. Furthermore, although not clearly distinguishable, there was an intermediate group that depends on both, such as demersal fishes. CBE-endemic organisms, particularly bivalves, were notably depleted in 15 N. Interestingly, two nutritional types of chemosymbiotic bivalves were identified: vesicomyid clams showed an increase in the nitrogen isotope ratio of glutamic acid and a higher TP relative to symbiotic bacteria, while Bathymodiolus and Gigantidas mussels exhibited no change in the nitrogen isotope ratio of glutamic acid and maintained a TP of ~ 1 across all tissues, including gill samples mainly composed of symbiotic bacteria. Different forms of trophic dependence on chemosynthetic bacteria were observed even among closely related bivalve species, regardless of whether the symbiotic relationship is ecto- or endo-symbiosis. Consequently, among species preying on chemosymbiotic bivalves, the TP may reach 3 or more when preying on vesicomyid clams but remains around 2 when preying on Bathymodiolus and Gigatidas mussels. The organisms inhabiting the CBE of Sagami Bay display diverse patterns of resource use.