A globally abundant marine primary producer relies on microbial interactions to survive long-term stress

Many microorganisms produce resting cells with very low metabolic activity that allow them to survive prolonged stress conditions. In cyanobacteria and some eukaryotic microalgae, this process is accompanied by a loss of photosynthetic pigments (chlorosis). Here, we show that a chlorosis-like process occurs under multiple stress conditions in lab cultures of Prochlorococcus, the dominant phytoplankton linage in large regions of the oligotrophic ocean and a global key player in ocean biogeochemical cycles. Chlorotic cells are smaller than non-chlorotic ones and, on average, show reduced metabolic activity, measured at the single-cell level as C and N uptake by NanoSIMS. However, unlike many other cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not re-grow under axenic conditions when transferred to new media. Instead, co-culture with a heterotrophic bacterium, Alteromonas HOT1A3, enables Prochlorococcus to survive up to three months under nutrient starvation. Single-cell measurements of carbon and nitrogen uptake rates from Prochlorococcus cells in the deep photic zone of the Eastern Mediterranean suggest an important role for microbial interactions also in supporting the carbon demand of these photosynthetic organisms under low-light conditions. We propose that reliance on co-occurring heterotrophic bacteria or on the dissolved organic matter they produce (“The Black Queen Hypothesis”), rather than the ability to survive long periods of stress as resting cells, underlies the ecological success of Prochlorococcus in the oligotrophic ocean.