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

Abstract

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.