A model of photosynthesis and photo-protection based on reaction center damage and repair

Phytoplankton photosynthesis under the rapidly fluctuating irradiance which results from turbulent mixing through the vertical light gradient is poorly understood. Ship-based measurements often apply the fast repetition rate fluorescence (FRRF) technique in situ or in vivo to gauge the physiological state of the phytoplankton community and infer some of the physical properties of the water column (such as mixing time scales). We describe the development and validation of a model of photosynthetic electron turnover at photosystem II with consideration of downstream limitation, based on the redox state of photosystem II. We also include empirical formulations for slower processes such as photo-protection (from nonphotochemical quenching) and photo-inhibition. By confronting the simple model with laboratory data for Dunaliella tertiolecta, we were able to refine the model so that it faithfully produced rates of photosynthetic electron transfer determined by FRR fluorescence. Further, we were able to validate the model estimates of linear photosynthetic electron transfer rates against completely independent measurements obtained using 14C-bicarbonate assimilation in photosynthesis-light curves. The light dependence of phytoplankton photosynthesis is one of the most intensively studied aspects of phytoplankton physiology (Jassby and Platt 1976; Cullen 1990; Falkowski and Raven 2007). Nonetheless, most commonly used incubation procedures (e.g., Knap et al. [1996] p. 159) do not resolve photosynthesis rates on the time scales of variability in photon flux density (PFD) that are experienced by the phytoplankton in situ. It has long been recognized that variability in the light environment due to vertical mixing can affect the accuracy of estimates of in situ photosynthesis (Marra 1980; MacIntyre et al. 2000). Higher frequency variability, such as that caused by wavefocusing in the upper euphotic zone (Dera and Gordon 1970), does not appear to affect photosynthetic physiology in those eukaryotes studied (Stramski et al. 1993; Mouget et al. 1995a, b) but has been shown to induce an acclimative change in a cyanobacterium (MacKenzie and Campbell 2005). Numerous approaches have been made to mimic variability in the light regime in incubation experiments. These include manual (Yoder and Bishop 1985; Randall and Day 1987) or automated (Kirkpatrick et al. 1990; Gocke and Lenz 2004) movement of incubation bottles through the water column; circulation of the sample through a light gradient in a deck incubator (Jewson and Wood 1975; Gallegos et al. 1977); and imposing variable attenuation on a static sample through mechanical rotation of multiple filters (Mallin and Paerl 1992; Bertoni and Balseiro 2005). Empirical approaches may fail to match the variability (both magnitude and frequency) imposed by the experimenter in the incubation to the variability that is experienced by phytoplankton in the natural environment. Accurately reproducing the natural light regime requires a priori knowledge of both the dynamic range and rate of change of irradiance. These can be derived from three parameters (the attenuation coefficient, the depth of the mixed layer, and the vertical diffusivity) for deck incubations and two (mixed-layer depth and diffusivity) for in situ incubations. Each of these input variables can vary within the duration of an hours-long incubation. Methods that have been tested or proposed for providing a match between the natural variability and the imposed regime include analysis of dye diffusion (Mallin and Paerl 1992), incorporation of motion sensors on a submersible incubator (Kirkpatrick et al. 1990) and parallel estimation of diffusivity, using an acoustic Doppler current profiler (Bertoni and Balseiro 2005). Incubations that use submerged samples account for changes in both the magnitude and spectral dependence of the attenuation coefficient. This is not the case for deck incubations, in which the use of filters with fixed optical characteristics imposes a defined 1 Present address: National Oceanography Centre, University of Southampton, Southampton SO14 3ZH, United Kingdom. Acknowledgments ONR and RJG gratefully acknowledge financial support from the MarQUEST initiative as part of the Natural Environment Research Council funded QUEST consortium. DJS and CMM were supported by Natural Environment Research Council postdoctoral fellowships. HLM was supported by National Science Foundation grant OCE-9907702. We are also grateful to K. Oxborough for useful discussions of the manuscript and to M. Behrenfeld for providing a helpful and thorough review. 2 Corresponding author ([email protected]). Limnol. Oceanogr., 53(5), 2008, 1835–1852 E 2008, by the American Society of Limnology and Oceanography, Inc.