Prochlorococcus rely on microbial interactions rather than on chlorotic resting stages to survive long-term stress

Many microorganisms produce resting cells with very low metabolic activity that allows them to survive phases of prolonged stress conditions. Using axenic lab cultures, we show that Prochlorococcus, the dominant phytoplankton linage in large regions of the nutrient-poor ocean, cannot survive extended nutrient starvation alone. Under starvation conditions some cells retain metabolic activity, measured as single-cell C and N uptake, but these cultures do not re-grow when transferred into new media. Nevertheless, co-cultures with a heterotrophic bacterium enabled Prochlorococcus to survive nutrient starvation for months. We extend these observations to natural conditions, suggesting that up to 10% of the Prochlorococcus cells in the oceans live under conditions of light starvation, utilizing organic matter produced by other organisms. We propose that reliance on co-occurring heterotrophic bacteria or on the organic matter they produce, rather than the ability to survive extended starvation as resting cells, underlies the ecological success of Prochlorococcus.