The function of plastids in the deep-sea benthic foraminifer, Nonionella stella
Limnol. Oceanogr., 47(6), 2002, 1569-1580 | DOI: 10.4319/lo.2002.47.6.1569
ABSTRACT: Curiously, the benthic foraminifer, Nonionella stella, found in the upper 3 cm of sediments collected off California at a depth of ;600 m, retains chloroplasts. We examined the origin and physiological function of the organelles within the host cell. Transmission electron micrographs, fluorescence and absorption spectra, Western blots, and enzyme assays revealed that the chloroplasts were intact and retained functionality for up to 1 year after sample collection. 16S rDNA gene sequences established that the plastids were derived from diatoms closely related to Skeletonema costatum and Odontella sinensis. Western blots of three major chloroplast proteins (ribulose bisphosphate carboxylase oxygenase [RuBisCO], the D1 protein, and the fucoxanthin chlorophyll a protein complex) confirmed that the organelle retained both nuclear and chloroplast encoded proteins, which suggests that the turnover of the plastid machinery is extremely low. Moreover, the two carboxylating enzymes examined, RuBisCO and phosphoenol pyruvate carboxylase, retained catalytic activity. Three hypotheses regarding the function of sequestered chloroplasts in deep-sea foraminifera were considered: (1) the organelles are photosynthetic under extremely low irradiance levels, (2) the organelles utilize exogenous substrates to generate an electrochemical gradient that permits chemoautrophy in the dark, and (3) they are used for the assimilation of inorganic nitrogen. Our results suggest that the chloroplasts are used to meet the nitrogen requirements of the host. Immunolocalization of the nuclear encoded protein, nitrate reductase, supports this hypothesis. This protein is widely distributed in photoautotrophs but is not encoded in eukaryotic protists such as foraminifera.