Abstract
Cyanobacteria dominate the world's oceans where iron is often barely detectable. One manifestation of low iron adaptation in the oligotrophic marine environment is a decrease in levels of iron-rich photosynthetic components, including the reaction center of photosystem I and the cytochrome b 6f complex [R.F. Strzepek and P.J. Harrison, Photosynthetic architecture differs in coastal and oceanic diatoms, Nature 431 (2004) 689–692.]. These thylakoid membrane components have well characterised roles in linear and cyclic photosynthetic electron transport and their low abundance creates potential impediments to photosynthetic function. Here we show that the marine cyanobacterium Synechococcus WH8102 exhibits significant alternative electron flow to O 2, a potential adaptation to the low iron environment in oligotrophic oceans. This alternative electron flow appears to extract electrons from the intersystem electron transport chain, prior to photosystem I. Inhibitor studies demonstrate that a propyl gallate-sensitive oxidase mediates this flow of electrons to oxygen, which in turn alleviates excessive photosystem II excitation pressure that can often occur even at relatively low irradiance. These findings are also discussed in the context of satisfying the energetic requirements of the cell when photosystem I abundance is low.
Highlights
Synechococcus sp. dominate phytoplankton populations over much of the world's oceans and are important contributors to global primary productivity [2]
Diatoms have adapted to low Fe levels by significantly lowering the cellular content of the Fe-rich photosynthetic electron transport components, which include cytochrome b6f and photosystem I (PSI) [1]
Most cyanobacteria in terrestrial and freshwater environments maintain ratios of photosystem II (PSII):PSI that are below unity [4]
Summary
Synechococcus sp. dominate phytoplankton populations over much of the world's oceans and are important contributors to global primary productivity [2]. The availability of Synechococcus WH8102 in pure culture and the sequencing of its genome make this cyanobacterium an ideal model for integrating genomic, molecular and physiological information Such studies are vital for addressing key issues in oceanic. Freshwater cyanobacteria respond to Fe depletion by lowering the relative abundance of PSI and forming an additional light harvesting antenna around the remaining PSI [6,7]. Based on full genome sequencing, the marine, open-ocean cyanobacterium Synechococcus WH8102 contains neither isiA nor pcb genes, making it likely that this organism has evolved other mechanisms for surviving the ironpoor oceanic environment, where PSI levels may be depleted. We show that the model marine cyanobacterium, Synechococcus WH8102 compensates for low relative levels of PSI by enlisting O2 as a major electron acceptor downstream of PSII, at the level of the intersystem electron transport chain. The enzyme responsible for mediating this alternative electron flow is an oxidase with characteristics of PTOX
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