Photosynthetic adaptation to low iron, light, and temperature in Southern Ocean phytoplankton

Abstract

Phytoplankton productivity in the polar Southern Ocean (SO) plays an important role in the transfer of carbon from the atmosphere to the ocean’s interior, a process called the biological carbon pump, which helps regulate global climate. SO productivity in turn is limited by low iron, light, and temperature, which restrict the efficiency of the carbon pump. Iron and light can colimit productivity due to the high iron content of the photosynthetic photosystems and the need for increased photosystems for low-light acclimation in many phytoplankton. Here we show that SO phytoplankton have evolved critical adaptations to enhance photosynthetic rates under the joint constraints of low iron, light, and temperature. Under growth-limiting iron and light levels, three SO species had up to sixfold higher photosynthetic rates per photosystem II and similar or higher rates per mol of photosynthetic iron than temperate species, despite their lower growth temperature (3 vs. 18 °C) and light intensity (30 vs. 40 μmol quanta⋅m2⋅s−1), which should have decreased photosynthetic rates. These unexpectedly high rates in the SO species are partly explained by their unusually large photosynthetic antennae, which are among the largest ever recorded in marine phytoplankton. Large antennae are disadvantageous at low light intensities because they increase excitation energy loss as heat, but this loss may be mitigated by the low SO temperatures. Such adaptations point to higher SO production rates than environmental conditions should otherwise permit, with implications for regional ecology and biogeochemistry.