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Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection1

Authors

  • Allen J. Milligan,

    1. Institute of Marine and Coastal Studies, Rutgers, The State University of New Jersey, New Brunswick, New Jersey, USA
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    • 2

      Author for correspondence: e-mail allen.milligan@science.oregonstate.edu.

    • 3

      Present address: Department of Botany and Plant Pathology, 2082 Cordley Hall, Oregon State University, Corvallis, Oregon 97331-2902, USA.

  • Ilana Berman-Frank,

    1. Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, 52900, Israel
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  • Yoram Gerchman,

    1. Department of Chemistry, Princeton University, Princeton, New Jersey 08544, USA
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    • 4

      Present address: Department of Environmental and Evolutionary Biology, University of Haifa, Haifa 31905, Israel; and Department of Biology, University of Haifa at Oranim, Tivon 36006, Israel.

  • G. Charles Dismukes,

    1. Institute of Marine and Coastal Studies and Department of Geology, Rutgers, The State University of New Jersey, New Brunswick, New Jersey, USA
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  • Paul G. Falkowski

    1. Institute of Marine and Coastal Studies, Rutgers, The State University of New Jersey, New Brunswick, New Jersey, USA
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  • 1

    Received 16 August 2006. Accepted 7 May 2007.

Abstract

All colonial diazotrophic cyanobacteria are capable of simultaneously evolving O2 through oxygenic photosynthesis and fixing nitrogen via nitrogenase. Since nitrogenase is irreversibly inactivated by O2, accommodation of the two metabolic pathways has led to biochemical and/or structural adaptations that protect the enzyme from O2. In some species, differentiated cells (heterocysts) are produced within the filaments. PSII is absent in the heterocysts, while PSI activity is maintained. In other, nonheterocystous species, however, a “division of labor” occurs whereby individual cells within a colony appear to ephemerally fix nitrogen while others evolve oxygen. Using membrane inlet mass spectrometry (MIMS) in conjunction with tracer 18O2 and inhibitors of photosynthetic and respiratory electron transport, we examined the light dependence of O2 consumption in Trichodesmium sp. IMS 101, a nonheterocystous, colonial cyanobacterium, and Anabaena flos-aquae (Lyngb.) Bréb. ex Bornet et Flahault, a heterocystous species. Our results indicate that in both species, intracellular O2 concentrations are maintained at low levels by the light-dependent reduction of oxygen via the Mehler reaction. In N2-fixing Trichodesmium colonies, Mehler activity can consume ∼75% of gross O2 production, while in Trichodesmium utilizing nitrate, Mehler activity declines and consumes ∼10% of gross O2 production. Moreover, evidence for the coupling between N2 fixation and Mehler activity was observed in purified heterocysts of Anabaena, where light accelerated O2 consumption by 3-fold. Our results suggest that a major role for PSI in N2-fixing cyanobacteria is to effectively act as a photon-catalyzed oxidase, consuming O2 through pseudocyclic electron transport while simultaneously supplying ATP in both heterocystous and nonheterocystous taxa.

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