Photoacclimation

Photoacclimation is a complex light-response that changes cellular activities on many time scales. The aquatic environment presents a highly variable irradiance (E) field with changes occurring over a wide range of time scales. For example, changes in E on short time scales can result from focusing and defocusing of radiation by waves at the surface. Longer time scale changes can result from variable cloud cover or turbulent motion that transports phytoplankton across the exponential E gradient of the surface mixed layer. In a well-mixed surface layer, phytoplankton experiences long periods of low E interspersed by short periods of saturating or even supersaturating E. The diurnal solar cycle causes changes in E on even longer time scales. To cope with the highly variable radiation environment, phytoplankton has developed numerous strategies to optimize photosynthesis, while minimizing susceptibility to photodamage. Photosynthetic acclimation to E over time scales of hours to days proceeds through changes in cellular pigmentation or structural characteristics, for example, size and number of photosynthetic units. On shorter time scales, cells adjust photon utilization efficiencies by changing the distribution of harvested energy between photosystems (state transitions) or by dissipating excess energy through non-photochemical processes, for example, xanthophyll cycle or photoinhibition.

Therefore, photoacclimation involves change in macromolecular composition in photosynthetical apparatus. It is relatively easy to observe acclimation in unicellular algae and seeweeds, where chlorophylls per cell or per unit surface can increase five- to ten-fold as irradiance decreases. The response is not a linear function of irradiance; rather at extremely low light levels, cells often become a bit chlorotic, and on exposure to slightly higher (but still low) irradiance, chlorophyll reaches a maximum. Increase in irradiance leads to a decrease in the cellular complement of chlorophylls until a minimum value is reached. The absolute irradiance levels that induce these effects are species specific and chlorotic response is not universal. The changes in pigmentation resulting from photoacclimation have profound consequences for light absorption properties of the cells. First, cells acclimated to high irradiance levels generally have high carotenoids concentration relative to chlorophyll a. Carotenoids such as β-carotene and zeaxanthin do not transfer excitation energy to the reaction centers and consequently act to screen the cell from excess light. Some xantophylls such as lutein, transfer excitation energy but with reduced efficiency, and therefore effectively reduce the functional absorption cross-section of the associated photosystem.

Because these carotenoids absorb light without a concomitant increase in the functional cross-section of PSII, organisms acclimated to high irradiance levels often have lower maximum quantum yield of photosynthetic O₂ evolution. Second, when cells acclimate to low irradiance levels, the subsequent increase in pigmentation is associated with a decrease in functional optical absorption section normalized to chlorophyll a. This effect is due primarly to the self-shading of the chromophores between layers of thylakoids membranes, and is an inverse function of the number of membranes in the chloroplast, that is, the more the membranes, the lower the optical cross-section. Thus, as cells accumulate chlorophyll, each chlorophyll molecule becomes less effective in light absorption; a doubling of cellular chlorophyll does not produce a doubling in the rate of light absorption. The reduction in the chlorophyll-specific optical absorption cross-section can be visualized considering the fate of photons incident on two stacks of thylakoid membranes: one is a thin stack from a cell acclimated to high irradiance levels and the second is a thick stack from a cell acclimated to low irradiance levels. The probability of a photon passing through a thick stack of membranes without being absorbed is small compared with a thin stack of membranes. This so-called “package effect” reduces the effectiveness of increased pigmentation in harvesting light and has important implications for the capital costs of light harvesting, that is, the investments in the physical structures of the organism required for the metabolic processes. The diminution in the optical absorption cross-section with increased chlorophyll is also a function of cell size: the larger the cell the more important is this effect. At some point a cell is, for most practical purposes, optically black and further increases in pigment levels confer no advantage in light absorption.

There are two basic photoacclimation responses in algae. In one, acclimation is accomplished primarily by changes in the number of photosynthetic reaction centers, while the effective absorption cross-section of the reaction centers remains relatively constant. The second is characterized by relatively large changes in the functional size of the antennae serving the reaction centers, while the number of reaction centers remains relatively constant. Complementary changes in either of the responses produce the same effect on the initial slope of the photosynthesis–irradiance curve. As the functional size of the antennae serving PSII, and not the number of rection centers, determines the light-saturation parameter, organisms that vary the cross-section would tend to have more control over this parameter, as long as the turnover time remains constant.