Metabolic adaptations of foraminifera to oxygen depletion and their role in marine nutrient cycling

Benthic foraminifera are ubiquitous marine protists that inhabit environments from the deepest part of the ocean to saltmarsh meadows slightly above sea-level. Various species of foraminifera have highly specific adaptations to the environmental conditions in their ecological niche. Their high abundances in oxygen depleted environments and their metabolic adaptations to anaerobic conditions make them key players in marine nutrient cycling.

Here I will review the recent advances in understanding those adaptations. Benthic foraminifera from oxygen depleted environments are a rare example of eukaryotes that are able to denitrify and thus an important sink for reactive nitrogen in the oceans. Several species even show a metabolic preference of nitrate over oxygen as an electron acceptor. Several enzymes that are involved in foraminiferal denitrification are transcribed by eukaryotic RNA. These denitrification steps are thus executed by the foraminifers themselves and use enzyme homologues that are known from bacterial denitrification. Still, the foraminiferal denitrification pathway is incomplete. Recent studies indicate that previously undescribed enzymes as well as bacterial symbionts might be responsible for the missing steps in the foraminiferal denitrification pathway.

Furthermore, there is a widespread occurrence of intracellular phosphate storage in benthic foraminifera, which encode genes required for both a creatine phosphate and a polyphosphate metabolism. Both dephosphorylation of creatine phosphate and hydrolysis of polyphosphates are likely also adaptations to oxygen depletion. The high intracellular phosphate storage in foraminifera has previously been overlooked in benthic phosphorous cycling. It constitutes an important mobile reservoir in benthic ecosystems and facilitates phosphogenesis in some environments.