A Novel Photosynthetic Strategy for Adaptation to Low Iron Environments

Abstract

Iron availability is a major limiting factor for photosynthesis and hence for life in most of the aquatic environments on earth. Cyanobacteria are important primary producers and prevail over Fe- deficiency by de-repressing the isiAB operon, which codes for the antenna protein IsiA and flavodoxin. We demonstrate that under nanomolar iron concentrations, a giant IsiA-Photosystem I supercomplex is formed, consisting of a Photosystem I trimer encircled by two complete IsiA rings with 18 and 25 copies in the inner ring and outer ring, respectively. The IsiA-Photosystem I supercomplex contains more than 850 chlorophylls and has a mass of 3.2 MDa, making it the most complex membrane protein that has been isolated to date. Ultrafast fluorescence spectroscopic results show fast and efficient excitation transfer and trapping in the supercomplex. The electron transfer throughput of Photosystem I is increased by 300%, an evolutionary adaptation that has allowed cyanobacteria to avoid oxidative stress. This adaptation of the photosynthetic apparatus confers an enormous, as-yet unrecognized, evolutionary advantage to cyanobacteria living under conditions of severe Fe stress and thereby have adapted to the modern low iron concentration in aquatic environments.1. Eldridge, M. et al. Aquatic Microbial Ecology 35, 79-91 (2004).2. Martin, J. & Fitzwater, S. Nature 331, 341-343 (1988).3. Wilhelm, S. Aquatic Microbial Ecology 9, 295-303 (1995).4. Bibby, T. S., Nield, J. & Barber, J. Nature 412, 743-5 (2001).5. Boekema, E. J. et al. Nature 412, 745-8 (2001).6. Singh, A., McIntyre, L. & Sherman, L. Plant Physiology 132, 1825 (2003).