Chlorophyll breakdown in aquatic ecosystems.

T he annual cycle of greening and degreening of plants is probably the most obvious sign of life on Earth. It is caused by the biosynthesis of ∼10 tons of chlorophylls (Chls) in spring and their degradation in fall. The biochemistry of Chl breakdown to linear tetrapyrroles has been worked out in land plants (1), but little was known about the process in marine organisms, which contribute a comparable share to global biomass production. In PNAS, Kashiyama et al. (2) now provide evidence for a rather different pathway that is widespread in aquatic ecosystems and relates to protist feeding on picoplankton. Chls are the pigments of photosynthesis, the process providing the basis for life on Earth, the oxygen in the atmosphere, and fossil fuels. These pigments have been optimized during evolution for the efficient harvesting of sunlight, and the subsequent energy transduction into high-energy compounds like ATP and NADPH. Chemically, Chls are cyclic tetrapyrroles. They share the basic carbon skeleton and large parts of their biosynthesis with hemes. The biophysical properties are nonetheless very different and reflect the different functions. Chls have, in particular, several properties that apparently render them indispensible for photosynthesis (3). They strongly absorb visible and near-infrared light, which is essential for light harvesting, and they have long-lived excited states that prevent loss of the transiently stored energy into heat. Chls are nonetheless a mixed blessing, because the very properties beneficial to photosynthesis also render them highly phototoxic. This is no problem as long as the system works perfectly. Under optimum conditions, the primary processes, the so-called “light reactions,” proceed with quantum efficiencies near the theoretical limit (4, 5). Whenever there are internal or external disturbances and the energy stored in the Chls’ excited states cannot be used productively within picoseconds, these pigments can, however, raise havoc. The long-lived excited states of Chls and reverse electron flow processes now allow the formation of triplet states, which, in turn, can react efficiently with molecular oxygen. The resulting reactive oxygen species are among the most aggressive agents in nature, capable of attacking almost any cellular component. Situations generating such overload are common in a changing light environment. Photosynthetic organisms therefore need to optimize photosynthesis continuously in competition with others without being scorched by excess energy (6). Sudden and unpredictable increases can occur, for example, under moving clouds or under a canopy of other plants. They can also arise from imbalances of electron flow or lack of electron donors or acceptors caused by environmental conditions and repair of the complexes