Anaerobic metabolism of Foraminifera thriving below the seafloor

Foraminifera are single-celled eukaryotes (protists) of large ecological importance, as well as environmental and paleoenvironmental indicators and biostratigraphic tools. In addition, they are capable of surviving in anoxic marine environments where they represent a major component of the benthic community. However, the cellular adaptations of Foraminifera to the anoxic environment remain poorly constrained. We sampled an oxic-anoxic transition zone in marine sediments from the Namibian shelf, where the genera Bolivina and Stainforthia dominated the Foraminifera community, and use metatranscriptomics to characterize Foraminifera metabolism across the different geochemical conditions. The relative abundance of Foraminifera gene expression in anoxic sediment depths increased an order of magnitude, which was confirmed in a ten-day incubation experiment where the development of anoxia coincided with a 27-fold increase in the relative abundance of Foraminifera protein encoding transcripts. This indicates that many Foraminifera were not only surviving, but thriving under the anoxic conditions. The anaerobic energy metabolism of these active Foraminifera was characterized by fermentation of sugars and amino acids, dissimilatory nitrate reduction, fumarate reduction, and dephosphorylation of creatine phosphate. This was co-expressed alongside genes involved in production of reticulopodia, phagocytosis, calcification, and clathrin-mediated-endocytosis (CME). Thus, Foraminifera may use CME under anoxic conditions to utilize dissolved organic matter as a carbon and energy source, in addition to ingestion of prey cells via phagocytosis. These mechanisms help explain how some Foraminifera can thrive under anoxia, which would help to explain their ecological success documented in the fossil record since the Cambrian period more than 500 million years ago.