Do phytoplankton require oxygen to survive? A hypothesis and model synthesis from oxygen minimum zones

Abstract

It is commonly known that phytoplankton have a pivotal role in marine biogeochemistry and ecosystems as carbon fixers and oxygen producers, but their response to deoxygenation has scarcely been studied. Nonetheless, in the major oceanic oxygen minimum zones (OMZs), all surface phytoplankton groups, regardless of size, disappear and are replaced by unique cyanobacteria lineages below the oxycline. To develop reasonable hypotheses to explain this pattern, we conduct a review of available information on OMZ phytoplankton, and we re-analyze previously published data (flow cytometric and hydrographic) on vertical structure of phytoplankton communities in relation to light and O 2 levels. We also review the physical constraints on O 2 acquisition as well as O 2 -dependent metabolisms in phototrophs. These considerations, along with estimates of the photosynthetic capacity of phytoplankton along OMZ depth profiles using published data, suggest that top-down grazing, respiratory demand, and irradiance are insufficient to fully explain the vertical structure observed in the upper, more sunlit portions of OMZs. Photorespiration and water-water cycles are O 2 -dependent pathways with low O 2 affinities. Although their metabolic roles are still poorly understood, a hypothetical dependence on such pathways by the phytoplankton adapted to the oxic ocean might explain vertical patterns in OMZs and results of laboratory experiments. This can be represented in a simple model in which the requirement for photorespiration in surface phytoplankton and O 2 -inhibition of OMZ lineages reproduces the observed vertical fluorescence profiles and the replacement of phytoplankton adapted to O 2 by lineages restricted to the most O 2 -deficient waters. A high O 2 requirement by modern phytoplankton would suggest a positive feedback that intensifies trends in OMZ extent and ocean oxygenation or deoxygenation, both in Earth's past and in response to current climate change.Deoxygenation in oceans is a growing phenomenon associated with anthropogenic climate change with several interacting causes that include changes in circulation and mixing, decreased solubility of oxygen (O 2 ) as temperature increases, and possibly biogeochemical changes (Ito et al., 2017;Schmidtko et al. 2017;Oschlies et al. 2018). The first evidence of a decline in dissolved O 2 was recorded in the 1980s (Horak et al. 2016;Ito et al. 2017). Oxygen minimum zones (OMZs) are naturally occurring zones where O 2 in sub-surface waters drops below a threshold that varies among authors but is