Abstract

Chlorophyll fluorescence from phytoplankton provides a tool to assess iron limitation in the oceans, but the physiological mechanism underlying the fluorescence response is not understood. We examined fluorescence properties of the model cyanobacterium Synechocystis PCC6803 and a ΔisiA knock-out mutant of the same species grown under three culture conditions which simulate nutrient conditions found in the open ocean: (1) nitrate and iron replete, (2) limiting-iron and high-nitrate, representative of natural high-nitrate, low-chlorophyll regions, and (3) iron and nitrogen co-limiting. We show that low variable fluorescence, a key diagnostic of iron limitation, results from synthesis of antennae complexes far in excess of what can be accommodated by the iron-restricted pool of photosynthetic reaction centers. Under iron and nitrogen co-limiting conditions, there are no excess antennae complexes and variable fluorescence is high. These results help to explain the well-established fluorescence characteristics of phytoplankton in high-nutrient, low-chlorophyll ocean regions, while also accounting for the lack of these properties in low-iron, low-nitrogen regions. Importantly, our results complete the link between unique molecular consequences of iron stress in phytoplankton and global detection of iron stress in natural populations from space.

Highlights

  • Proliferation of oxygenic photosynthesis approximately 2.3 billion years ago dramatically reduced iron solubility in the surface ocean and created a ‘physiological crisis’ for phytoplankton that continues today [1,2,3,4,5]

  • The fraction of absorbed light lost as fluorescence increases under low iron conditions, which is indicative of decreased efficiency in energy transfer for photosynthesis

  • We conducted experiments with the model cyanobacterium, Synechocystis sp PCC 6803, under three steady-state nutrient regimes: (1) nitrate and iron replete, (2) limiting-iron and high-nitrate, representative of natural highnitrate, low-chlorophyll (HNLC) regions, and (3) iron and nitrogen co-limiting, simulating conditions found in regions of the central

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Summary

Introduction

Proliferation of oxygenic photosynthesis approximately 2.3 billion years ago dramatically reduced iron solubility in the surface ocean and created a ‘physiological crisis’ for phytoplankton that continues today [1,2,3,4,5]. We conducted experiments with the model cyanobacterium, Synechocystis sp PCC 6803, under three steady-state nutrient regimes: (1) nitrate and iron replete, (2) limiting-iron and high-nitrate, representative of natural highnitrate, low-chlorophyll (HNLC) regions, and (3) iron and nitrogen co-limiting, simulating conditions found in regions of the central In this simulation of natural HNLC conditions, iron limitation caused a 60% increase in the PSII:PSI ratio and an 8fold increase in IsiA protein abundance (Fig. 1), consistent with previous iron-starvation results [19,20,35,36].

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