Deoxygenation is driving ecological shifts across vast oceanic volumes. To understand and predict future ocean ecosystem functioning and stability, it is critical to identify the eukaryotic metabolic repertoire that enables survival under anoxia. Foraminiferan protists are one of few eukaryotic lineages that can inhabit anoxic marine sediments, environments relevant today and in Earth's past. Here, we investigate the metabolic strategies employed by a representative of an early-evolving foraminiferan group to persist anoxia. A saccamminid foraminifer inhabiting an anoxic bathyal seafloor in the Santa Barbara Basin (CA, USA) was preserved in situ. (Meta)transcriptomic analyses revealed an aerotolerant mitochondrial metabolism lacking Cytochrome c Oxidase, but expressing alternative oxidase, potentially fueled by internally released oxygen during ROS detoxification, and utilizing a TCA reductive Complex II. This foraminifer uses glutamate oxidation and aspartate-malate shuttle to generate reducing equivalents, driving ATP production via an atypical anaerobic electron-transport chain. Energy metabolism is also tightly linked to phosphate availability, facilitating substrate-level phosphorylation of high-energy intermediates. This foraminifer's competitive advantage is its anaerobic energy metabolism combined with ability to detoxify and reduce oxygen, if present. These unusual capabilities confer a blueprint for understanding how early eukaryotes may have evolved during anoxia, remained resilient during the Neoproterozoic Oxygenation Event, and likely will be ecological winners amid ongoing ocean deoxygenation.
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