Sulfur and nitrogen metabolisms in the aphotic kleptoplastidic foraminifer Nonionella stella: results from metatranscriptomics

Certain deep-sea benthic foraminiferal species survive and are extremely abundant in anoxic (lacking oxygen) and/or euxinic (sulfidic) marine sediments. These foraminifera present diverse cell biology, where some have endobionts, others have ectobionts, and others even lack any putative symbionts. One type of specialized endosymbiosis is represented by the sequestered chloroplasts within hosts living in the aphotic zone. We obtained de novo metatranscriptomes of the holobiont of Nonionella stella, a species that sequesters chloroplasts and inhabits euxinic marine sediments in the aphotic zone (~590 m), in order to identify the metabolic pathways, and their origins, that allow N. stella to survive such an “extreme” environment. We exposed N. stella to different environmental conditions (oxic, hypoxic, anoxic, or euxinic amended with nitrate, hydrogen peroxide, both, or none). Our metatranscriptomic analyses demonstrated that the nitrate and ammonium assimilatory pathways are linked to the foraminiferal host and kleptoplasts, while assimilatory sulfate reduction appears to be linked to kleptoplasts of the dark-dwelling N. stella. We also obtained complete denitrification pathways linked partly to the N. stella host and partly to the associated bacteria. Benthic foraminifera present unique and environmentally relevant model organisms for exploring the mechanisms and evolutionary drivers allowing their adaptations in oxygen-depleted environments. Supported by NSF BIO IOS 1557430 and 1557566.