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Science 16 November 2001:
Vol. 294. no. 5546, pp. 1534 - 1537
DOI: 10.1126/science.1064082
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Reports

Segregation of Nitrogen Fixation and Oxygenic Photosynthesis in the Marine Cyanobacterium Trichodesmium

Ilana Berman-Frank,1* Pernilla Lundgren,2 Yi-Bu Chen,1 Hendrik Küpper,345 Zbigniew Kolber,1 Birgitta Bergman,2 Paul Falkowski1

In the modern ocean, a significant amount of nitrogen fixation is attributed to filamentous, nonheterocystous cyanobacteria of the genus Trichodesmium. In these organisms, nitrogen fixation is confined to the photoperiod and occurs simultaneously with oxygenic photosynthesis. Nitrogenase, the enzyme responsible for biological N2 fixation, is irreversibly inhibited by oxygen in vitro. How nitrogenase is protected from damage by photosynthetically produced O2 was once an enigma. Using fast repetition rate fluorometry and fluorescence kinetic microscopy, we show that there is both temporal and spatial segregation of N2 fixation and photosynthesis within the photoperiod. Linear photosynthetic electron transport protects nitrogenase by reducing photosynthetically evolved O2 in photosystem I (PSI). We postulate that in the early evolutionary phase of oxygenic photosynthesis, nitrogenase served as an electron acceptor for anaerobic heterotrophic metabolism and that PSI was favored by selection because it provided a micro-anaerobic environment for N2 fixation in cyanobacteria.

1 Environmental Biophysics and Molecular Ecology Program, Institute of Marine and Coastal Sciences, Rutgers University, 71 Dudley Road, New Brunswick, NJ 08901, USA.
2 Department of Botany, Stockholm University, SE-106 91 Stockholm, Sweden.
3 Photosynthesis Research Center, Institute of Microbiology, Opatovický mlýn, CZ-37981 Třeboň, Czech Republic.
4 Laboratory of Biomembranes, University of South Bohemia, Branisovská 31, CZ-370 05 České Budejovice, Czech Republic.
5 University of Konstanz, Faculty of Sciences, Department of Biology, D-78457 Konstanz, Germany.
*   To whom correspondence should be addressed. E-mail: irfrank{at}imcs.rutgers.edu

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