Molecular Mechanisms of Photosynthesis. Robert E. Blankenship
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have several well‐documented essential functions in photosynthetic systems. First, they are accessory pigments in the collection of light, absorbing light and transferring energy to a chlorophyll‐type pigment. Most antenna complexes contain carotenoids. Second, carotenoids function in a process called photoprotection. Carotenoids rapidly quench triplet excited states of chlorophylls before they can react with oxygen to form the highly reactive and damaging excited singlet state of oxygen. They also quench the singlet oxygen if it is somehow formed. Finally, carotenoids have recently been shown to be involved in the regulation of energy transfer in antennas. These processes, which avoid overexcitation of the photosynthetic system by safely dissipating excess energy, have different mechanisms in different organisms. We will discuss them in more detail in Chapter 5.
Carotenoids have very unusual energetic and spectroscopic properties. They usually exhibit an intense absorption band, typically in the 400–500 nm range, giving them their characteristic orange color. However, this transition is from the ground state (S0) to the second excited singlet state (S2), instead of to the first excited singlet state (S1). The transition from the ground state to the first excited singlet state is forbidden because of the symmetry of the carotenoid molecule. An energy level diagram typical of many carotenoids is shown in Fig. 4.12. The lifetime of S2 is very short, usually relaxing to S1 by internal conversion on a subpicosecond time scale. This short lifetime of S2 means that fluorescence of the S2 state is highly quenched and is not observed in most situations. From the S1 state, the excited carotenoid can relax to the ground state. However, this relaxation is also almost always nonradiative. The fluorescence decay rate constant of an excited state is related to the strength of the absorption that forms the excited state (Eq. A.68). If an absorption transition is extremely weak, such as the S0 to S1 carotenoid absorption, then the intrinsic fluorescence decay rate constant between these two states will be very small, and fluorescence will make a negligible contribution to the excited state decay (Eq. A.69). Internal conversion from S1 to S0 is typically very efficient, so the S1 state has a picosecond lifetime. Carotenoids with nine or more double bonds have additional dark states in addition to the three energy levels discussed here (Ostroumov et al., 2013).
Figure 4.12 Energy Level diagram typical of carotenoids.
The energy of the S1 state of the carotenoid is very difficult to measure directly, because of the forbidden nature of the S0 to S1 transition. One method that can be used to determine this energy is two‐photon spectroscopy, in which two photons are absorbed simultaneously, with the sum of their energies equal to the transition energy. The S0 to S1 transition is allowed under these conditions (Krueger et al., 1999).
With both the S2 and S1 states having exceptionally short excited state lifetimes, it is perhaps surprising that carotenoids are able to carry out energy transfer to chlorophylls before they decay to S0, releasing heat. Yet, in many cases, carotenoids are efficient antenna pigments, because the energy transfer process is even faster than the deactivation rate. We will explore some of the details of this energy transfer process in complexes where structural information is available in Chapter 5.
4.6 Bilins
Bilins are linear, open‐chain tetrapyrrole pigments found in the light‐harvesting antenna complexes known as phycobilisomes, which absorb in the spectral region from 550 to 650 nm. Phycobilisomes are well characterized structurally and spectroscopically and are one of the best understood of the various classes of antenna complexes. We will discuss them in more detail in Chapter 5.
Figure 4.13 Structures of two of the most common bilins: phycocyanobilin and phycoerythrobilin.
The bilins resemble a porphyrin that has been split open and twisted into a linear conformation. Indeed, the bilins are actually formed from heme groups in just this fashion, as described below. The structures of the two most commonly found bilins, phycocyanobilin, and phycoerythrobilin, are shown in Fig. 4.13. The bilins are bound to proteins known as biliproteins. The three main classes of biliprotein antenna complexes are allophycocyanin, phycocyanin, and phycoerythrin. Bilins are the only class of photosynthetic pigments that are covalently attached to proteins. They are linked by thioether bonds to specific cysteine amino acid residues. In most cases, a single thioether linkage on ring A is found, although a dual linkage at both ring A and ring D is found on some pigments in phycoerythrin (MacColl, 1998).
The open‐chain tetrapyrrole bilin chromophores are made by a surprisingly complex pathway (Bryant et al., 2020). First, the protoporphyrin IX molecule is synthesized, as described above in the description of chlorophyll biosynthesis. This molecule is converted into a heme by insertion of Fe. The heme is then split open by the action of the enzyme heme oxygenase. Heme oxygenase requires both O2 and NADPH as substrates, producing the molecule biliverdin, which is subsequently reduced, isomerized, and finally ligated to the apoprotein.
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