New PhytoL (19S3) 93, 157-191 157 ADAPTATION OF UNICELLULAR ALGAE TO IRRADIANCE: AN ANALYSIS OF STRATEGIES BY K. RICHARDSON, J. BEARDALL* AND J. A. RAVEN Department of Biological Sciences, University of Dundee, Dundee DDI 4HN, Scotland, U.K. (Accepted 1 October 1982) CONTENTS SUMMARY 157 INTRODUCTION 158 AN.^LYTICAL METHODS 159 LIGHT HARVESTING BY MICROALGAE 160 RANGE OF PHOTON FLUX DENSITIES ALLOWING GROWTH AND PHOTOSYNTHESIS IN PHOTOTHOPHIC MICROALGAE (GENOTYPIC ADAPTATION) 163 Growth 163 Photosynthesis 165 Photoinhibition 165 PHENOTYPIC ADAPTATION 168 Changes in amounts of pigments 168 Interpretation of the effects of pigment changes: models 169 Observed changes in P vs I curves 170 ENERGETIC CONSIDERATIONS 174 General 174 Reduction of capital costs 175 Reduction of maintenance costs 175 Energetic costs of changing the photosyothetic apparatus 177 S2-S3 decay 177 Proton leakage due to passive uniport 178 PHYLOGENETIC ASPECTS OF DIFFERENCES IN LIGHT RESPONSES OF MICROALGAL PHOTOSYNTHESIS AND PHOTOLITHOTROPHIC GROWTH 178 Phylogenetic diflerences in photosynthetic structures 178 Comparison of tbe photosynthetic characteristics of green algae and other pbototrophs 180 ECOLOGICAL CONSIDERATIONS 182 ACKNOWLEDGEMENTS 185 REFERENCES 185 SUMMARY Analysis of data in the literature relating to micrcalgal adaptations to different photon flux densities indicates that different algal classes have significantly different ligbt requirennents for growth and photosynthesis. Although there is some variability within each class, dinoflagellates and 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 species has been reported at less than 1 fi.E m"' s~'). Comparison of the photon flux densities at which photoinhibition occurs in dinoflagellates and diatoms suggests that the former often experience photoinhibition at comparatively low irradiances. In contrast, diatoms often can tolerate relatively high light environments. This tolerance of a large absolute range of photon flux densities 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 6 ANj" 93 158 K. RICHARDSON eZ a/. tend to exhibit higher light compensation points than the other common microalgal classes and can tolerate very high light environments. The photosynthesis vs irradiance curves of high and low light adapted microalgae are discussed in relation to the theoretical models that other workers have put forward to describe phytoplankton photoadaptation as a function of either an increased number or an increase in the size of photosynthetic units in a cell. We conclude that while the models form a useful starting point for the study of photoadaptation, they cannot explain all of the strategies observed. Microalgal photoadaptation is discussed in terms of the possible mechanisms by which a cell could reduce its capital and maintenance costs under conditions of limiting energy supply. Phylogenetic aspects of the differences in light responses of tbe various microalgal classes and the ecological implications of different photoadaptive strategies are also considered. INTRODUCTION By comparison with most vascular plants, unicellular microalgae occupy habitats characterized by very low photon flux densities. Most microalgae live in aquatic environments where light is attenuated exponentially with depth according to the Lambert-Beer Law: where d is depth, !„ is the incident radiation upon the surface of the vifater, I^ is the photon flux density at depth, d, and k is an extinction coefficient. Typically, clear temperate coastal waters exhibit a k for photosynthetically active radiation (PAR), 400 to 700 nm of about 0-15 while in the clearest oceanic waters k may be in the region of 0"04. In addition to attenuating light, water selectively filters the light passing through it and although the quality of light penetrating to depth varies in different water types, in all types red light (> 600 nm) is essentially undetectable at depths of 10 m or more. (For detailed discussions of light and the underwater environment, see Jerlov, 1968, 1976; Wheeler and Neushal, 1981). The ability of microalgae to survive and grow in habitats where they nnay experience exposure to very low photon flux densities must result from the interaction of structural, behavioural, physiological and biochemical factors. Unlike macroscopic algae and vascular plants, unicellular phytoplankton do not have large amounts of non-photosynthetic tissue to support. This structural difference between unicellular algae and higher plants tnust certainly make the former more suited to life at low photon fiux densities. Furthermore, although most macroscopic algae and vascular plants occupy a fixed topographic position and in order to survive must be able to tolerate all environmental extremes that that position experiences, some phytoplankton are able, at least to some extent, to regulate their position in the water column. This tneans that some species may be able to exert some control over their light environment as well. Microalgae are better suited for the study of photoadaptive strategies than macrophytes because the latter can adapt morphologically to changes in the light environment and, therefore, may be less reliant on cell-level changes than unicells. Also, terrestial macrophytes have more extreme thermo/water regulation prob- lems in 'sun' than in 'shade' environments. Thus, photoadaptive strategies may be difficult to differentiate from temperature or dessication responses. To date, a large number of physiological and biochemical investigations have been carried out on the problem of the relationship between irradiance and algal growth and photosynthesis. Adaptation of unicellular algae 159 Most such studies of phytoplankton photoadaptation have examined responses of an individual species confronted with a change in its light environment. By analogy with vascular plants, investigators have attempted to differentiate between ' sun' and ' shade' species. Although a number of different adaptive strategies have been described, no clear overall picture of phytoplankton adaptations to changes in photon flux density has, as yet, emerged. The problems associated with analysis of light adaptation in microalgae are considerable. In the field, natural water movements make description of a phytoplankter's light environment and light history very difficult. In the laboratory, description of the light environment is possible. However, results of investigations may be affected by changes in algal physiological state precipitated by the culturing conditions employed (see Griffiths, 1973; Morris and Glover, 1974; Beardall and Morris, 1976). Furthermore, laboratory cultures are normally maintained at greater cell densities than would normally be encountered in nature. Failure to consider the extent to which algal suspensions absorb incident light complicates the analysis of photosynthesis vs photon flux density (P vs I) and grovi^th rate vs photon flux density (p, vs I) curves. Finally, problems surrounding the measurement of light have complicated the algal physiologist's understanding of light adaptation by phytoplankton. In recent years, the convention of describing the light environment in units of illumination (lux, footcandles) has gradually been replaced by expressing light either in units of energy (joules, ergs, gram calories) or in quanta (Einsteins). As photosynthesis at its most basic level is controlled by the absorption of photons, the expression of light in quanta (einsteins) would seem particularly suited to investigations into phytoplankton photoadaptation. Knowledge of the spectral distribution of the quanta received then allows calculation of the energy input. Conversion between units can be complicated and owing to differences in the nature of the measurements is, at best, imprecise when converting between units of illumination and energy or quanta. Analysis of the available literature reveals that many investigators (and reviewers) remain confused about the units in use and what is actually being measured. (For discussion, see Incoll, Long and Ashmore, 1981.) Many appear to lack a feeling for 'reasonable' values and some quite unrealistic light measurement values have found their way into print. We believe that further understanding of light/shade adaptation by phytoplank- ton cannot be achieved until a synthesis of the available data pertaining to microalgal light adaptations has been made. Therefore,, the present work is an attempt to collate and analyse the literature relating to phytoplankton light adaptation. By doing so we hope to clarify the present understanding of photo- adaptation by phytoplankton and to identify the questions which should be asked in further research. ANALYTICAL METHODS Data pertaining to algal growth and photosynthesis at differing photon flux densities were compiled from the published literature and from personal com- munications. All values for light measurement were converted to /lE m~^ s''- according to the conversions shown below.* In these units, 'full sunlight' has a photon flux density of about 1700 fcE m~^ s'^ (400' to 700 nm). When cultures were • 2Wm-= = 10/(Em-'s-'; 1 klx = 16-5/tE m"'s"'; 1 ly min"'= 4-184 J cm^'min"i; 1 ly min-'= 697 W m-"; ] ly min"' = 3485 /iB