Photosystem II function under extreme low light and low temperatures; polar vs. temperate phytoplankton

Polar phytoplankton achieve slow, but ecologically significant, productivity under exceptionally low light, where the sequential arrivals of photons at Photosystem II complexes are widely spaced in time. We hypothesized that maintaining photosynthesis under such low growth light involves suppression of energetically wasteful photochemical ‘misses’ in Photosystem II. Under full darkness Photosystem II relaxes predominantly to the S1 oxidation state of the oxygen evolving complex. After such dark relaxation we applied series of single turnover, saturating, flashes to advance Photosystem II through sequential photochemical charge separations, progressively oxidizing the oxygen evolving complex through sequential increments through the S-States, resulting in four-step changes in Photosystem II chlorophyll fluorescence yield. We tracked these oscillations in chlorophyll fluorescence to measure the persistence of synchronized S-States across the Photosystem II populations in diatoms and green algae, in response to changing measurement temperatures and extremely low effective light levels, which we emulated by increasing the spacing between photon deliveries. Prolonged synchronous S-State cycling indicates fewer desynchronizations from wasteful photochemical misses and, thus, potentially more efficient photosynthetic energy conversion under low growth light. We observed that colder temperatures result in more sustained cycling at longer photon spacings, within taxa. Further, polar taxa maintained synchronized cycles for longer than did temperate taxa, even under comparable measurement conditions. Our findings support our hypothesis that diverse lineages of polar phytoplankton can suppress energetically wasteful photochemical misses under low temperature, to help sustain photosynthesis even under extremely low growth light. Therefore, ambient temperature interacts with the lower-light limitation on photosynthesis.