Oxygenic and anoxyegenic Photosynthesis

Photosynthesis is a highly complex, multistep process. Only the first step, a photochemical electron transfer reaction, is driven by light. All the subsequent reaclions are thermodynamically spontaneous and can therefore in principle rake place in the dark, but do so rapidly under physiological conditions only because they are facilitated by sophisticated enzyme catalysts within the photosynthetic organism. Several chapters in this book are devoted to the intricate architecture of the photosynthetic apparatus and the different organisms that carry out photosynthesis, and here we shall provide no more than a brief introduction.
 

Complex though the mechanisms of photosynthesis are, the overall chemical reactions are quite simple and fall into two categories: oxygenic photosynthesis is photosynthesis in which oxygen is produced, and anoxygenic photosynthesis is a simpler type of photosynthesis in which oxygen is not produced. Oxygenic photosynthesis occurs in plants, algae, oxyphotobacteria (including cyanobacteria) and anoxygenic photosynthesis occurs in green and purple photosynthetic bacteria. The overall chemical reaction of oxygenic photosynthesis is the sunlight-driven, chlorophyll-sensitised transformation of water and atmospheric carbon dioxide to make energy-storing carbohydrates, which have the empirical formula [CH;?O], and oxygen as a by-product.

This crucially important reaction, also shown in Fig. 1.1, produces essentially all of the Earth’s biomass, and this book is primarily concerned with its mechanism and consequences.

The photosynthetic apparatus of plants and algae is located in organelles called chloroplasts. In leaves of higher plants they are mostly found in the palisade layer of cells under the waxy sun-facing surface of the leaves. Each cell contains up to 100 chloroplasts. These are disk-like bodies 5-10 pm in diameter containing a colourless supporting matrix known as the stroma in which double-layer lipid membranes about 50-70 8, across provides support for the pigment-proteins involved in the capture of light energy. These membranes are known as thylakoids and, as can be seen in Fig.l.3, in chloroplasts of plants they are partly stacked in dense regions known as grana and partly more loosely arranged in the stroma as unstacked larnellae. The intrathylakoid region between the thylakoid double membranes is known as the lumen. In the chloroplasts of algae, the thylakoid membranes do not tend to have such an extensive separation of stacked and unstacked regions. In the case of red algae and cyanobacteria, there is no differentiation into stacked and unstacked regions. Anoxygenic photosynthesis occurs in purple and green sulphur photosynthetic bacteria. Here the overall reaction does not involve the oxidation of water to oxygen. Instead, these anoxygenic organisms obtain the reducing equivalents they need to fix COP from a range of electron sources such as H2S and organic acids, which we denote H2A. Bacteriochlorophylls are the light-absorbing pigments in these organisms, and the overall process can be written

A11 modern anoxygenic photosynthetic bacteria are oxygen-intolerant prokaryotic4 organisms that thrive only in reducing conditions, for example in the anaerobic environment of mud, soil and stagnant ponds where their particular electron donor H2A is available. Depending on the nature of H2A, reaction 1.2 may be exergonic or mildly endergonic.
 

Photosynthetic bacteria play an important ecological role, but in terms of biomass creation they are insignificant. In scientific terms, however, they have been very important experimental systems. Indeed, as explained in Chapter 3 by Leibl and Mathis, they have provided valuable clues to the structure of the more complex photosynthetic apparatus of green plants. There are probably many thousands of different species of photosynthetic bacteria yet to be discovered, but to date detailed studies have focussed on just a few: the purple photosynthetic bacteria Rhodopseudomonas viridis, Rhodobacter sphaeroides, Rhodobacter capsulatus, Rhodospirillum rubrum and Rhodopseudomonas acidophila and the related green, non-sulphur bacterium ChloroJlexus aurantiacus; and the green sulphur bacteria Chlorobium limicola, Prostherochloris aestuarii and the related Heliobacillus mobilis.

The light-absorbing pigments and cofactors5 in a photosynthetic organism are arranged in protein structures whose architecture depends on the type of organism, generically known as photosynthetic units. We discuss these structures in Section 1.3. For now, we note that each photosynthetic unit has two principal components: a reaction centre (RC), where the early, light-driven events of photosynthesis take place, and a light-harvesting (LH) antenna system, which contains most of the photosynthetically active pigments. In plants and green algae, the principal photosynthetic pigments are the chlorophylls (Chl a and b). Other types of algae (e.g. brown algae) can contain Chl c and Chl d as well as Chl a. Red algae and cyanobacteria, have only Chl a but also contain pigments known as phycobilins. In anoxygenic photosynthetic bacteria, the main pigments are the bacteriochlorophylls a and b (BChl), which are doubly-reduced chlorophylls that absorb at longer wavelengths than Chl a or Chl b so are more suited to aquatic organisms. All photosynthetic organisms contain carotenoids, of which there are many different types. They are involved in light harvesting but also play an important role in photoprotection. Figure 1.4 shows the structures of the main photosynthetic pigments. The LH systems absorb the photosynthetically active radiation (PAR) of incoming sunlight and channel it to the RCs. These are of two types, known as Type I and Type 11, that seem to have a common evolutionary origin. However, they differ in the nature of their cofactors and thermodynamic properties. Photosynthetic bacteria fall into two classes, distinguished by their RC type: green sulphur bacteria and heliobacteria have Type I RCs, while purple photosynthetic bacteria and filamentous green, non-sulphur photosynthetic bacteria have Type I1 RCs. Cyanobacteria, algae and higher plants have one RC of each type, known as Photosystem I (PSI) and Photosystem I1 (PSII), which act in series to drive oxygenic photosynthesis.6 Within the reaction centre lie two closely spaced Chl or BChl molecules usually known as the special pair,’ and given the symbol P (for pigment) followed by a number. This is the wavelength in nanometres where maximum bleaching is observed during photosynthesis, and lies close to the absorption maximum of the particular chlorophyll dimer. Because of the dimeric or quasi-dimeric character of P, its absorption maximum lies to longer wavelengths than that of the monomeric antenna pigment molecules. This significant shift to the red makes P an efficient trap for the excitation energy from the many surrounding LH antenna pigment molecules.

Figure 1.5 shows a highly schematic energy-level diagram of the photosynthetic units and overall photosynthetic reactions in anoxygenic (bacterial) and oxygenic (green-plant) photosynthesis. Photosynthetic bacteria possess either Type I or Type I1 RCs, and Fig. 1.5a shows P870, the Type IT RC of purple photosynthetic bacteria, as an example. When P870 receives excitation from its LH system, the electronically
excited state P870* is formed. Like all ‘special pairs’ of (bacterio)chlorophylls in photosynthesis, P870* acts as a reducing agent, and transfers an electron to a primary electron acceptor and thence to a series of secondary acceptors that take the electron outside the RC. In this way a chain of dark (thermal) events are initiated culminating in the reduction of C02 to carbohydrate. Meanwhile, the ‘hole’ (positive charge) on P870’ is transferred to a nearby primary acceptor, and thence to secondary acceptors in a chain of events that culminates in the oxidation of H2A. The bacterial RC is thus regenerated in an active state, ready to receive the next excitation from its LH system. A minimum of four absorbed photons is required to reduce one molecule of C02 although in many photosynthetic bacteria, cyclic electron flow also occurs which generates metabolic energy (ATP) without fixing COz.
 

In cyanobacteria, algae and higher plants, the Type I and Type I1 reaction centres PSI and PSII act in series, so that two photons now drive each electron through the electron-transfer chain, and a minimum of eight photons is required to reduce each C02 molecule. Excitation of P700, the ‘special pair’ of Chl a molecules in PSI, generates a strong reductant, P700*, capable of reducing C02, while the Chls of P680 in PSII generate an unusually strong oxidant, P680’, capable of oxidising water to oxygen. The overall electron-transfer sequence is completed by the transfer of an electron from P680* to P700’ (see Fig 1.5b).