Beyond the single pathway: co-expression analysis reveals distinct roles of dual carbon fixation in Riftia pachyptila symbionts

Abstract

Biological carbon fixation is foundational to the biosphere. Most organisms possess one carbon fixation pathway. The hydrothermal vent tubeworm Riftia pachyptila’s chemoautotrophic symbionts, however, possess two functional pathways: the Calvin Benson-Bassham (CBB) and the reductive tricarboxylic acid (rTCA) cycles. Little is known about how Riftia’s symbionts and related organisms coordinate the functioning of these two pathways. Here we investigated net carbon fixation rates, transcriptional/metabolic responses, and transcriptional co-expression patterns of Riftia pachyptila’s endosymbionts by incubating tubeworms at environmental pressures, temperature, and geochemistry. Results showed that rTCA and CBB transcriptional patterns varied in response to different geochemical regimes and that each pathway is allied to specific metabolic processes, suggesting distinctive yet complementary roles in metabolic function. Net carbon fixation rates were also exemplary, and accordingly we propose that co-activity of CBB and rTCA may be an adaptation for maintaining high carbon fixation rates, conferring a fitness advantage in dynamic vent environments.