Why be Green in the Deep Sea?

All life forms oxidize and/or reduce carbon. The eukaryotic machinery for these processes originated from primitive relatives of the chloroplast and mitochondria, cyanobacteria and purple-sulfur bacteria, respectively. Coincidentally or not both cyanobacteria and purple sulfur bacteria can utilize hydrogen sulfide as an electron donor. Primitive mitochondrial and photosynthetic pathways may have evolved in sulfur biomes (Searcy 1992). Adaptations or reversions to ancient pathways by modern organelles such as mitochondria, peroxisomes and chloroplasts may provide clues as to how cells evolved oxidative and regenerative pathways. Extant organisms that live in primitive conditions may utilize ancient pathways hidden by evolution from a mildly reducing to oxidizing atmosphere about 2 billion years ago. Many of these adaptations are largely associated with prokaryotes, however certain eukaryotes thrive in severely oxygen-depleted sulfidic settings, an observation that is somewhat surprising considering most eukaryotic taxa require oxygen to survive and most aerobes are detrimentally affected by hydrogen sulfide. Obviously, these organisms have specialized mechanisms to allow survival in such an environment. Indeed, certain aerobes are known to even exploit sulfide. Recent observations suggest that as yet unknown mechanism(s) allow the dominant eukaryote of a sulfidic, deep-sea locale to exploit potentially toxic hydrogen sulfide in a novel manner. More specifically, in the Santa Barbara Basin, the protistan foraminifer Nonionella stella sequesters chloroplasts in its cytoplasm. Plastid sequestration by protists, including foraminifera, and metazoans is not uncommon in euphotic settings. The seafloor of the Santa Barbara Basin (SBB) lies, however, at a water depth of ~590 m, which is far below the even the deepest euphotic zone. Thus, a question arises: Why would a phagotroph bother to selectively engulf, but not digest, chloroplasts if they do not benefit the host?

The second unusual attribute of SBB N. stella is the presence of vast peroxisome fields. Although peroxisomes are typical cellular components, their functions and their density in mammalian cells can correspond to environmental and/or physiological perturbations (Masters & Crane 1995). Because foraminifera from aerated, non-sulfidic environs typically lack peroxisome fields while those from sulfidic, O2-depleted areas typically have them, it is likely that peroxisomes play a significant role in the success of N. stella in SBB. The major objective of this research is to elucidate the role(s), if any, of peroxisomes and sequestered chloroplasts in the benthic foraminifer Nonionella stella under dark, oxygen-depleted, sulfide-enriched conditions.