A new regulatory model can describe acclimation of phytoplankton growth rate (p), chlorophyll a : carbon ratio and nitrogen: carbon ratio to irradiance, temperature and nutrient availability. The model uses three indices of phytoplankton biomass-phytoplankton carbon (C), phytoplankton nitrogen (N), and chlorophyll a (Chl). The model links the light-saturated rate of photosynthesis to N: C, requires that Chl a synthesis be coupled to nitrogen assimilation, and includes several regulatory features. These include feedback inhibition of the nitrogen assimilation rate by increases in the N: C ratio, as well as regulation of Chl a synthesis by the balance between light absorption and photosynthetic carbon fixation. The model treats respiration as the sum of the maintenance metabolic requirement and the cost of biosynthesis. In addition, the model can account for accumulation and mobilization of energy reserves (i.e. variability of N: C) and photoacclimation (i.e. variability of Chl : N and Chl : C) in response to variations in irradiance and nutrient availability. The assumptions of the model are shown to be in agreement with experimental observations and the model output compares favorably with data for cultures in balanced and unbalanced growth. The light-, nutrient-, and temperature-dependencies of phytoplankton growth rate have often been modeled separately. Phytoplankton growth rate has been treated as a function of the dissolved nutrient concentration using the Monod equation or as a function of the cellular content (or quota) of limiting nutrient using the Droop equation (McCarthy 1980; Droop 1983; Morel 1987). Under conditions of balanced growth, the Droop and Monod equations are consistent with each other and with Michaelis-Menten nutrient uptake kinetics (Morel 1987). The temperature-dependence of growth rate has been treated as an exponential dependence or an Arrhenius equation, although other functions have also been used (Eppley 1972; Li 1980; Ahlgren 1987). The lightdependencies of growth and photosynthesis rates have been treated by a number of equations, including a modification of the Monod equation, a hyperbolic tangent, and a Poisson function

https://aslopubs.onlinelibrary.wiley.com/doi/pdf/10.4319/lo.1998.43.4.0679

A dynamic regulatory model of phytoplanktonic acclimation to light, nutrients, and temperature

SUMMARY 157INTRODUCTION 158AN.^LYTICAL METHODS 159LIGHT HARVESTING BY MICROALGAE 160RANGE OF PHOTON FLUX DENSITIES ALLOWING GROWTH AND PHOTOSYNTHESIS INPHOTOTHOPHIC MICROALGAE (GENOTYPIC ADAPTATION) 163 Growth 163Photosynthesis 165Photoinhibition 165 PHENOTYPIC ADAPTATION 168 Changes in amounts of pigments 168Interpretation of the effects of pigment changes: models 169Observed changes in P vs I curves 170 ENERGETIC CONSIDERATIONS 174 General 174Reduction of capital costs 175Reduction of maintenance costs 175Energetic costs of changing the photosyothetic apparatus 177S2-S3 decay 177Proton leakage due to passive uniport 178 PHYLOGENETIC ASPECTS OF DIFFERENCES IN LIGHT RESPONSES OF MICROALGALPHOTOSYNTHESIS AND PHOTOLITHOTROPHIC GROWTH 178 Phylogenetic diflerences in photosynthetic structures 178Comparison of tbe photosynthetic characteristics of green algae and otherpbototrophs 180 ECOLOGICAL CONSIDERATIONS 182ACKNOWLEDGEMENTS 185REFERENCES 185 SUMMARY Analysis of data in the literature relating to micrcalgal adaptations to different photon fluxdensities indicates that different algal classes have significantly different ligbt requirennents forgrowth and photosynthesis. Although there is some variability within each class, dinoflagellatesand blue-green algae generally photosynthesize and grow best at low photon flux densities.Diatoms also tend to be able to grow at very low photon flux densities (growth for some specieshas been reported at less than 1 fi.E m"' s~'). Comparison of the photon flux densities at whichphotoinhibition occurs in dinoflagellates and diatoms suggests that the former often experiencephotoinhibition at comparatively low irradiances. In contrast, diatoms often can toleraterelatively high light environments. This tolerance of a large absolute range of photon fluxdensities may, in part, explain why diatoms are often associated with spring blooms. Green algae* New address; Department of Botany, La Trobe University, Bundoora, Victoria, 3083 Australia.0028-646X/83/020157 + 35 S03.00/0 © 1983 The New Phytologist

https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/j.1469-8137.1983.tb03422.x

Adaptation of unicellular algae to irradiance: an analysis of strategies

The dependence of phytoplankton photosynthesis on light intensity may be altered by the range and frequency of variations in light intensity recentlv experienced by the organisms. A major source of the fluctuations in light intensity experienced by phytoplankton in the upper ocean is vertical motion. We estimate time and space scales for \\Tertical displacements of phytoplankton caused by turbulent mixing, internal waves, Langmuir circulations, and double diffusive processes. In the surface layer, depending on windspeed, current shear and stratification, we find that time scales for cycling of phytoplankton by turbulent eddies and mixing vary from about 0.5 h to hundreds of hours for vertical displacements of the order of 10 m. In the seasonal thermocline, turbulent diffusive time scales for displacements as small as several meters are weeks to months, whereas similar displacements by internal waves occur over periods of several minutes to several hours, according to the strength of the density stratification, and are then dominant. Langmuir cells seem to scale as the large turbulent eddies and need not be treated separately, and double diffusive processes seem to be of minor importance. The formulation used here of a vertical turbulent diffusion coefficient K, as a function of observable quantities-e the rate of dissipation of turbulent kinetic energy, and N the local buoyancy frequency-should also be us&d for estimating vertical fluxes of nutrients. In addition, this formulation is reversible in time and can be used to estimate the recent depth and light history of phytoplankton taken from the upper ocean. Traditionally the dependence of the photosynthetic production rate of phytoplankton on light intensity has been described by “P vs. I” curves relating the rate of photosynthetic production, P, to increasing light intensity, I, determined usually from experiments where portions of the same sample are incubated at several different constant light intensities for the same period. The uptake of labeled carbon over that period is measured and considered to be an index of the photosynthetic production (Peterson 1980). Division by the time interval gives the photosynthetic rate. A smooth curve fitted through the data resembles one of the family of curves shown in Fig. 1 (which, for illustration, has been generated from the model equation of Platt et al. 1980): P(I) = aem”‘( 1 eeVr). (1) Several problems exist: different curves are often found at different times of day (provided the incubation period is sufficiently brief, say 2-4 h), at different depths, during different seasons, and with different organisms (Harris 1973; MacCaull and Platt 1977; Platt et al. 1980). Furthermore, time-course measurements of varying photosynthetic production P(t)

https://aslopubs.onlinelibrary.wiley.com/doi/pdf/10.4319/lo.1983.28.5.0801

Time and space scales of vertical mixing and advection of phytoplankton in the upper ocean

Macrotidal estuaries (mean tidal range >2m) generally exhibit a tolerance to pollution with nitrogen-containing nutrients despite high loadings originating from freshwater outflows. These systems, which are characterized by high tidal energy, generally exhibit lower levels of chlorophylla than systems with lower tidal energy. A comparative analysis of data from 40 microtidal and macrotidal estuaries shows that mean annual chlorophylla levels are significantly lower in systems with high tidal energy even when nitrogen concentrations are equal to nitrogen levels in the microtidal systems. Tidal range and associated processes (e.g., tidal mixing, current velocity, light penetration, and sediment resuspension) influence phytoplankton biomass in some estuaries.

Control of phytoplankton biomass in estuaries: A comparative analysis of microtidal and macrotidal estuaries

The photosynthetic responses to variations in photon flux density were determined for Symbiodinium microadriaticum, the symbiont of the Caribbean jellyfish Cassiopeia xamachana, S. kawagutii, the symbiont of the Indo-Pacific stony coral Montipora verrucosa, and S. pilosum, the symbiont of the Caribbean zoanthld Zoanthus sociatus. Photosynthetic responses were characterized in terms of cellular pigment content, photosynthesis versus irradiance (P-I) relationships, and number and size of the photosynthetic unit (PSU). Analyses of the responses under 2 Light regimes of 40 and 250 p 0 1 quanta m-' S-' indicate that: (1) the 3 different species cultured under identical conditions possess different photosynthetic characteristics; (2) the 3 species acclimate to low photon flux density by simultaneously increasing the number and size of their PSU; (3) PSU characteristics were not correlated with the parameters of their respechve P-lcurves; (4) the 3 species analyzed have different photoacclimatory capabilities which can be correlated with their respective ecological distribution as endosymbionts. As different species demonstrate characteristic responses, photo-acclunatory adjustment in symbiotic dinoflagellates may be under genetic constraints, and thus may represent photo-adaptation (sensu 0. Bjorkman). As a whole, the results suggest that symbiont photo-adaptation may constitute an important axis of niche diversification for the intact associations.

https://www.int-res.com/articles/meps/113/m113p163.pdf

Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density

Cultures of the marine dinoflagellate Glenodinium sp. were light-shifted and rates of photoadaptation determined by monitoring changes in cell volume, growth rate, pigmentation, parameters of the photosynthesisirradiance (P-I) curves and respiration. To approximate physiological conditions of field populations, cells were cultured on an alternating light-dark cycle of 12hL:12hD, which introduced a daily periodicity of photosynthesis. One result of the present study was to demonstrate how specific parameters of the P-I relationship influenced by periodicity of the light: dark cycle are distinguished from photosynthetic parameters influenced by changes in light level. Under steady-state conditions, rates of both light-saturated (Pmax) and light-limited photosynthesis changed in unison over the day; these changes were not related to pigmentation, and displayed their maxima midday. This close relationship between Pmax and the slope (a) of the cellular P-I curves in steadystate conditions was quickly adjusted when growth illumination was altered. Rates of light-limited photosynthesis were increased under low light conditions and the periodicity of cellular photosynthesis was maintained. The short-term responses of the P-I relationship to changing light level was different, depending on (1) whether the light shift was from high to low light or vice versa, and (2) whether the high light levels were sufficient to promote maximal photosynthesis rates. Major increases in the photosynthetic carotenoid peridinin, associated with a single type of light-harvesting chromo protein in the chloroplast, was observed immediately upon shifting high light cultures to low light conditions. Following pigment synthesis, significant increases in rates of light-limited photosynthesis were observed in about one-tenth the generation time, while cellular photosynthetic potential was unaffected. it is suggested that general results were consistent with suggested that general results were consistent with earlier reports that the major photoadaptive “strategy” of Glenodinium sp. is to alter photosynthetic unit (PSU) size. Photoadaptive response times to high light were light-dependent, but appeared to be shower than photoadaptive responses to low light. If light intensities were bright enough to maximize growth rates, photosynthetic response times were on the order of a generation period and pigmentation fell quickly as cells divided at a faster rate. If light-intensities were not sufficient to maximize growth rates, then pigment content did not decline, while rates of light-limited photosynthesis declined quickly. In all cases, photoadaptation was followed best by monitoring fast changes in half saturation constants for photosynthesis, rather than fluctuating changes in pigmentation. Results compared well with time-course phenomena reported for other groups of phytoplankton. Overall, results suggest phytoplankton can bring about photo-induced changes in photosynthesis very quickly and thus accommodate widely fluctuating light regimes over short periods of time.

Time-course of photoadaptation in the photosynthesis-irradiance relationship of a dinoflagellate exhibiting photosynthetic periodicity

Gonyaulax polyedra Stein was grown under bright light (330 μE m2 s-1) and then transferred to low light (80 μE m2 s-1), where the rates of photoadaptation were measured as a function of increasing cell density in increasingly nutrient-limited batch cultures. Photoadaptation required the synthesis of new pigment molecules for the photosynthetic units of the thylakoid membrane. However, as older bright-light cultures were shifted to low-light conditions, the onset of pigment synthesis was delayed, the rates of new chlorophyll synthesis slowed, and final yields of cell chlorophyll were sharply reduced. Moreover, photoadaptive capabilities of photosynthesis observed in log-phase cultures were lost in nutrient-limited stationary cultures. Addition of inorganic nutrients to stationary cultures at the time of transfer to low-light levels induced pigments synthesis at a rate and magnitude comparable to log-phase cultures and led to short-term increases in the rates of cell-and carbon-based photosynthesis. The nutrient status of the population also increased, as witnessed by increased carbon and nitrogen content and a large, but transient, increase in nitrate reductase activity. Improved photosynthetic status did not increase cell division rates over control populations. The study was made from December 1980 through March 1981.

H. A. Matlick

Papers

Time-course of photoadaptation in the photosynthesis-irradiance relationship of a dinoflagellate exhibiting photosynthetic periodicity

Nutrient-dependent low-light adaptation in the dinoflagellate Gonyaulax polyedra