A huge IsiA-PSI supercomplex unravels photosynthetic strategies for adaptation to low iron environments

Abstract

Cyanobacteria are aquatic photoautotrophs and important primary producers in many areas of the ocean. Their ability to generate dioxygen by oxygenic photosynthesis resulted in one of the largest changes to the Earth's atmosphere. Iron, which is essential in aquatic ecosystems, is scarce in the ocean and is the major factor limiting growth of photosynthetic organisms in the open oceans. Cyanobacteria prevail over iron deficiency by expressing a number of genes including the iron stress induced gene, isiA , which encodes the 36 kDa membrane protein IsiA. The major aim of this work was the unraveling of strategies that allow cyanobacteria to adapt to low iron environments. Nanomolar concentrations of iron lead to the formation of a giant IsiADR-PSI supercomplex in the thermophilic cyanobacterium Thermosynechococcus elongatus. Electron microscopic projection maps at 15 Å resolution show that the IsiADR-PSI supercomplex consists of a Photosystem I (PSI)-trimer encircled by two complete rings of the IsiA protein with 18 copies in the inner ring and 25 copies in the outer ring. The supercomplex has a molecular weight of 3.2 MDa and the chlorophyll-a/P 700 ratio is 285 ± 5, which corresponds to 855 ± 15 chlorophyll-a/Photosystem I. It is thereby the largest PSI complex and membrane protein that has been isolated to date. The investigation of the complex by ultrafast florescence spectroscopy unrevealed that the IsiADR-PSI supercomplex is a functional light-harvesting system that shows efficient energy transfer in the chlorophyll antenna system and high rates of electron transfer from cytochrome c 6 to flavodoxin