The energy-efficient reductive tricarboxylic acid cycle drives carbon uptake and transfer to higher trophic levels within the Kueishantao shallow-water hydrothermal system

Abstract

Chemoautotrophic Campylobacteria utilize the reductive tricarboxylic acid (rTCA) cycle for carbon uptake, a metabolic pathway that is more energy-efficient and discriminates less against 13C than the Calvin–Benson–Bassham cycle. Similar to other hydrothermal systems worldwide, Campylobacteria dominate the microbial community of the shallow-water hydrothermal system off Kueishantao (Taiwan). Compound-specific carbon stable isotope analyses of lipid-derived fatty acids were performed to understand the importance of rTCA and the transfer of fixed carbon to higher trophic levels in the vent area. Of these, C16:1ω7c, C18:1ω7c, and C18:1ω9c fatty acids were strongly enriched in 13C, indicating the activity of rTCA utilizing Campylobacteria. Isotopic fractionation was close to 0, likely caused by pH values as low as 2.88. Characteristic fatty acids were present not only in the vent fluids but also in adjacent sediments and water filters 20 m away from the vent orifice, albeit with decreasing abundance and diluted 13C signal. Furthermore, δ13C analysis of fatty acids from the tissue of Xenograpsus testudinatus, a crab endemic to this particular vent system, identified the trophic transfer of chemosynthetically fixed carbon. This highlights the interrelationship between chemoautotrophic microbial activity and life opportunities of higher organisms under environmentally harsh conditions at shallow-water hydrothermal systems.