Inorganic Carbon Assimilation via Chloroplasts in the Aphotic-Dwelling Kleptoplastidic Foraminifer Nonionella stella

The benthic foraminifer Nonionella stella dominates the abundant foraminiferal community inhabiting laminated, oxygen depleted and sometimes sulfidic sediments of the Santa Barbara Basin, comprising up to ~80% of the living assemblage, with densities sometimes exceeding 200 specimens per cubic cm. N. stella sequesters diatom chloroplasts even though the abundant population exists at >500-m water depth, which is clearly in the aphotic zone. Given that the light levels are thought to be too low to fuel photosynthesis, it remains unclear whether the chloroplasts provide other means to augment the cells’ metabolic or biochemical potential. We developed a de novo metatranscriptome assembly to identify metabolic functions of the foraminiferal host and their kleptoplast endosymbionts. Our results revealed that genes associated with the chloroplast Calvin-Benson-Bassham cycle (i.e., ribulose-bisphosphate carboxylase, phosphoglycolate phosphatase) are expressed among all of the studied samples including wild isolates as well as populations that were incubated in the lab exposed to different environmental conditions (oxic, anoxic, euxinic, with amendments of nitrate and/or hydrogen peroxide). These data suggest the presence of a functional pathway for inorganic carbon assimilation, providing a potential explanation for the puzzling existence of kleptoplasty in an aphotic organism. In addition to kleptoplasts, N. stella has a proliferation of peroxisomes that appear to play critical roles in hydrogen peroxide metabolism and free radical scavenging in their naturally low oxygen to anoxic and sulfidic environment. Funded by NSF BIO IOS 1557430 and 1557566.