Response of Prochlorococcus to varying CO2:O2 ratios

Carbon fixation has a central role in determining cellular redox poise, increasingly understood to be a key parameter in cyanobacterial physiology. In the cyanobacterium Prochlorococcus-the most abundant phototroph in the oligotrophic oceans-the carbon-concentrating mechanism is reduced to the bare essentials. Given the ability of Prochlorococcus populations to grow under a wide range of oxygen concentrations in the ocean, we wondered how carbon and oxygen physiology intersect in this minimal phototroph. Thus, we examined how CO2: O-2 gas balance influenced growth and chlorophyll fluorescence in Prochlorococcus strain MED4. Under O-2 limitation, per-cell chlorophyll fluorescence fell at all CO2 levels, but still permitted substantial growth at moderate and high CO2. Under CO2 limitation, we observed little growth at any O-2 level, although per-cell chlorophyll fluorescence fell less sharply when O-2 was available. We explored this pattern further by monitoring genome-wide transcription in cells shocked with acute limitation of CO2, O-2 or both. O-2 limitation produced much smaller transcriptional changes than the broad suppression seen under CO2 limitation and CO2/O-2 co-limitation. Strikingly, both CO2 limitation conditions initially evoked a transcriptional response that resembled the pattern previously seen in high-light stress, but at later timepoints we observed O-2-dependent recovery of photosynthesis-related transcripts. These results suggest that oxygen has a protective role in Prochlorococcus when carbon fixation is not a sufficient sink for light energy.