Surviving the dark ocean Adaptation and cross-feeding between Prochlorococcus and heterotrophic bacteria

The cyanobacterium Prochlorococcus is the smallest and most abundant photosynthetic microorganism in the ocean surface layer. It has also been found in the deep ocean where sunlight is absent, yet it is unknown whether those cells are viable. This PhD thesis explores Prochlorococcus survival in extended darkness and how this is influenced by the heterotrophic bacterium Alteromonas. Experiments revealed that in isolation, Prochlorococcus survives only 1 day in darkness, but with Alteromonas, it survives 11 days. The heterotroph reduces oxidative stress and releases organic substrates, shifting Prochlorococcus metabolism toward heterotrophy and extending its survival. Transcriptomic evidence revealed increased expression of genes involved in organic compound degradation and transport.
Prochlorococcus is common near the base of the euphotic zone, where it likely experiences mixing in and out of extended darkness. To simulate this, Prochlorococcus and Alteromonas co-cultures were subjected to repeated dark exposures, which led to the evolution of a stable and heritable dark-tolerant phenotype of Prochlorococcus. This phenotype is thought to be epigenetic in nature. Dark-tolerance resulted in both physiological and metabolic changes in Prochlorococcus, including a reduced entrainment to the diel light:dark cycle and switch from autotrophic to heterotrophic growth through the use of sugars produced by Alteromonas. In turn, Alteromonas switched from using sugars to reduced organic acids produced by Prochlorococcus, revealing enhanced carbon exchange and increased metabolic coupling between the two species. This work highlights how interactions of the photosynthetic Prochlorococcus with heterotrophic bacteria mediate its survival in the dark ocean.