Carotenoids, versatile components of oxygenic photosynthesis

Abstract

Carotenoids (CARs) are a group of pigments that perform several important physiological functions in all kingdoms of living organisms. CARs serve as protective agents, which are essential structural components of photosynthetic complexes and membranes, and they play an important role in the light harvesting mechanism of photosynthesizing plants and cyanobacteria. The protection against reactive oxygen species, realized by quenching of singlet oxygen and the excited states of photosensitizing molecules, as well as by the scavenging of free radicals, is one of the main biological functions of CARs. X-ray crystallographic localization of CARs revealed that they are present at functionally and structurally important sites of both the PSI and PSII reaction centers. Characterization of a CAR-less cyanobacterial mutant revealed that while the absence of CARs prevents the formation of PSII complexes, it does not abolish the assembly and function of PSI. CAR molecules assist in the formation of protein subunits of the photosynthetic complexes by gluing together their protein components. In addition to their aforementioned indispensable functions, CARs have a substantial role in the formation and maintenance of proper cellular architecture, and potentially also in the protection of the translational machinery under stress conditions.

Introduction

CARs are ubiquitous protective agents in the membranes of all photosynthetic organisms. Although several aspects of CAR functions are still to be elucidated, a growing body of evidence suggests that they play important roles in cyanobacteria and the chloroplasts and other organelles of green plants. In cyanobacteria and plants that are capable of oxygenic photosynthesis the majority of CARs are found in thylakoid membranes where the light reactions of photosynthesis take place. Therefore it has been suggested that these compounds perform important functions in the primary processes of photosynthesis. Among CARs β-carotene and several xanthophylls serve as constituents of functional multiprotein complexes, such as photosystems I and II (PSI, PSII), cytochrome b₆/f complexes, and the light-harvesting complexes involved in photosynthetic electron transport. In these superstructures protein components are surrounded by and bound together by specific CARs, presumably by means of hydrophobic interactions.

The roles of various CARs in photosynthetic organisms have previously been studied using either biochemical or molecular genetic approaches. However, the information regarding their precise functions is still limited. The recent identification of genes encoding CAR biosynthetic enzymes in cyanobacteria and plants, and the subsequent isolation of mutants defective in these functions, have provided powerful molecular tools for studying the roles of individual CAR species in these organisms. It has become apparent that CARs are essential for the assembly and stabilization of protein complexes in thylakoid membranes, and also for some non-photosynthetic processes. In this review we summarize recent findings concerning the biosynthesis and functions of CARs in photosynthetic organisms, primarily in cyanobacteria and higher plants. We overview the effects of free, non-protein-bound CARs on membrane microviscosity and the ways how these molecules can modulate membrane dynamics via CAR-lipid–protein interactions. We also assess the structural changes observed in cyanobacterial CAR mutants and highlight the photoprotective roles of CARs, especially those of the orange carotenoid protein, in the defense mechanism against various stress effects. Furthermore, we also discuss a CAR-based mechanism that might have a role in protecting elongation factors of the translational machinery from oxidative damage.