Membrane organisation of photosystem I complexes in the most abundant phototroph on Earth

Prochlorococcus is a major contributor to primary production, and globally the most abundant photosynthetic genus of picocyanobacteria because it can adapt to highly stratified low-nutrient conditions that are characteristic of the surface ocean. Here, we examine the structural adaptations of the photosynthetic thylakoid membrane that enable different Prochlorococcus ecotypes to occupy high-light (HL), low-light (LL) and nutrient-poor ecological niches. We used atomic force microscopy (AFM) to image the different photosystem I (PSI) membrane architectures of the MED4 (HL) Prochlorococcus ecotype grown under high-light and low-light conditions in addition to the MIT9313 (LL) and SS120 (LL) Prochlorococcus ecotypes grown under low-light conditions. Mass spectrometry quantified the relative abundance of PSI, photosystem II (PSII) and cytochrome b(6)f complexes and the various Pcb proteins in the thylakoid membrane. AFM topographs and structural modelling revealed a series of specialised PSI configurations, each adapted to the environmental niche occupied by a particular ecotype. MED4 PSI domains were loosely packed in the thylakoid membrane, whereas PSI in the LL MIT9313 is organised into a tightly-packed pseudo-hexagonal lattice that maximises harvesting and trapping of light. There are approximately equal levels of PSI and PSII in MED4 and MIT9313, but nearly two-fold more PSII than PSI in SS120, which also has a lower content of cytochrome b(6)f complexes. SS120 has a different tactic to cope with low-light levels, and SS120 thylakoids contained hundreds of closely packed Pcb-PSI supercomplexes that economise on the extra iron and nitrogen required to assemble PSI-only domains. Thus, the abundance and widespread distribution of Prochlorococcus reflect the strategies that various ecotypes employ for adapting to limitations in light and nutrient levels.