A COST‐BENEFIT ANALYSIS OF PHOTON ABSORPTION BY PHOTOSYNTHETIC UNICELLS

Summary An attempt is made to provide a cost-benefit analysis of light harvesting by microalgal cells. The costs relate to the number of mol photons which the cell must absorb to produce a quantity of light-harvesting apparatus containing 1 mol of chromophore; the fraction of the dry weight which is devoted to the light-harvesting machinery containing 1 mol of chromophore; and the number of mols of nitrogen which are used in producing the light-harvesting machinery containing one mol of chromophore. These costs relate to resources (photons; fraction of cell biomass; nitrogen) which may restrict the growth of microalgae in low-light environments (co-limitation by light and nitrogen in the case of nitrogen). The benefits relate to the photon absorption rate in a given light field (photon flux density and spectral distribution) per mol chromophore. Maximum photon absorption rate per mol chromophore requires that the specific absorption coefficient (e) of the pigment shall be high in the wavelength range to which the organism is exposed, and that self-shading (the ‘package’ effect) be minimized by having a large area of cell exposed to the incident photons per mol of chromophore. The costs of the light-harvesting machinery were estimated in terms of photons absorbed by the cell per mol of chromophore (plus associated protein and lipid) synthesized, using known biochemical pathways from carbon dioxide, nitrogen source (ammonium or nitrate) and photons to the light-harvesting apparatus. The fraction of the cell dry weight occupied by light-harvesting apparatus containing one mol of chromophore was deduced from the mass of protein and lipid associated with one mol of the various chromophores. The nitrogen cost was derived from the mols of nitrogen found in the light-harvesting machinery containing 1 mol of each of the various chromophores. These estimates show that, for all three criteria enumerated above, the cheapest tight-harvesting apparati are integral complexes containing chlorophylls a + b + carotenoids in chlorophytes and chlorophylls a+c2 (± C1) + carotenoids in Chromophytes, and the most expensive are the phycocyanins and allophycocyanins of Phycobiliphytes. The benefits of the various kinds of light-harvesting machinery were estimated in terms of the number of photons which were absorbed from a given light field per unit chromophore in solution and, more realistically, in vivo in cells of various sizes. The mean specific coefficient over the blue-green waveband characteristic of ‘aquatic shade’ showed that (in the absence of self-shading) the light-harvesting machinery characteristic of Chlorophytes and Chromophytes was generally superior to that of algae containing phycobilins and, especially, phycocyanin and allophycocyanin. When this disadvantage of the phycocyanins in terms of photon absorption rate per mol chromophore is compounded by considering the high energy (and fraction of biomass, and nitrogen) costs of synthesis of the phycocyanins, these pigments would appear to be contra-indicated as light-harvesting pigments for shade-adapted microalgae. Nevertheless, the phycocyanins occur in Cyanobacterial and Cryptophycean phytoplankters. A partial offset of the high costs of synthesis of the peripheral (phycobilin) light-harvesting complexes may derive from reduced H+ leakage through thylakoid membranes of organisms containing these complexes since the lipid bilayer area per mol chromophore is lower in Phycobiliphytes. A mismatch between prediction and reality analogous to that found for Phycobiliphyte exploitation of extreme shade environments is found when we examine the surface area of organism exposed to incident photons per mol chromophore. While many shade-adapted phytoplankters are small spheres up to a few tens of μm3 in volume or, if of larger volume, are cylinders of small radius or are flattened, there are also phytoplankters of shaded habitats with small projected areas per mol chromophore and hence with an inefficient use of light-harvesting machinery due to self-shading. It would appear that, while cost-benefit analyses of light-harvesting provide a partial answer to the problem of how microalgal cells can grow at very low photon flux densities, there are many exceptions to the generalisations which the cost-benefit analysis generates. These exceptions demand further study.