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BIOENERGETICS AND PHOTOSYNTHESIS

Traffic Lights in Trichodesmium. Regulation of Photosynthesis for Nitrogen Fixation Studied by Chlorophyll Fluorescence Kinetic Microscopy¹

Hendrik Küpper^*, Naila Ferimazova, Ivan etlík and Ilana Berman-Frank

Mathematisch-Naturwissenschaftliche Sektion, Fachbereich Biologie, Universität Konstanz, D–78457 Konstanz, Germany (H.K.); Faculty of Biological Sciences and Institute of Physical Biology, University of South Bohemia, CZ–370 05 Ceske Budejovice, Czech Republic (H.K., N.F., I.S.); Institute of Microbiology, Department of Autotrophic Microorganisms, Academy of Sciences of the Czech Republic, CZ–37981 Trebon, Czech Republic (N.F., I.S.); and Faculty of Life Sciences, Bar Ilan University, Ramat Gan 52900, Israel (I.B.-F.)

We investigated interactions between photosynthesis and nitrogen fixation in the non-heterocystous marine cyanobacterium Trichodesmium IMS101 at the single-cell level by two-dimensional (imaging) microscopic measurements of chlorophyll fluorescence kinetics. Nitrogen fixation was closely associated with the appearance of cells with high basic fluorescence yield (F₀), termed bright cells. In cultures aerated with normal air, both nitrogen fixation and bright cells appeared in the middle of the light phase. In cultures aerated with 5% oxygen, both processes occurred at a low level throughout most of the day. Under 50% oxygen, nitrogen fixation commenced at the beginning of the light phase but declined soon afterwards. Rapid reversible switches between fluorescence levels were observed, which indicated that the elevated F₀ of the bright cells originates from reversible uncoupling of the photosystem II (PSII) antenna from the PSII reaction center. Two physiologically distinct types of bright cells were observed. Type I had about double F₀ compared to the normal F₀ in the dark phase and a PSII activity, measured as variable fluorescence (F_v = F_m – F₀), similar to normal non-diazotrophic cells. Correlation of type I cells with nitrogen fixation, oxygen concentration, and light suggests that this physiological state is connected to an up-regulation of the Mehler reaction, resulting in oxygen consumption despite functional PSII. Type II cells had more than three times the normal F₀ and hardly any PSII activity measurable by variable fluorescence. They did not occur under low-oxygen concentrations, but appeared under high-oxygen levels outside the diazotrophic period, suggesting that this state represents a reaction to oxidative stress not necessarily connected to nitrogen fixation. In addition to the two high-fluorescence states, cells were observed to reversibly enter a low-fluorescence state. This occurred mainly after a cell went through its bright phase and may represent a fluorescence-quenching recovery phase.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.045963.

^* Corresponding author; e-mail hk282{at}cornell.edu; hendrik.kuepper{at}uni-konstanz.de; fax 607–255–2459.

Received May 8, 2004; returned for revision June 9, 2004; accepted June 9, 2004.