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University of Groningen Structures of Photosynthetic Membrane University of Groningen Structures of photosynthetic membrane complexes Semchonok, Dmitry Alexandrovich IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2016 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Semchonok, D. A. (2016). Structures of photosynthetic membrane complexes. Rijksuniversiteit Groningen. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 01-10-2021 Chapter 1. Introduction Photosynthesis is the processes whereby plants, algae and some other groups of organisms convert light into chemically fixed energy. The topic of this thesis deals with the primary steps in photosynthesis, which takes place in specialized photosynthetic membranes. Complex proteins inside photosynthetic membranes catalyse the primary steps. A number of such proteins were structurally characterised by electron microscopy. In this introduction chapter, we will discuss some basic aspects of both photosynthesis and electron microscopy analysis. Further, the proteins and the corresponding organisms that have been studied will be introduced. Some basic facts about photosynthesis Photosynthesis is the first main issue to be introduced. It is the process whereby green plants, algae, cyanobacteria, photosynthetic bacteria and certain other organisms transform light energy into chemical energy that can be later released to fuel the organisms' activities: namely to convert water, carbon dioxide and minerals into oxygen and energy-rich organic compounds in a direct or indirect way. The main organic compounds are carbohydrate molecules, sugars, lipids and proteins. Besides being vital for the life of the photosynthetic organisms, they serve as food for all other living creatures (Encyclopedia Britannica, 2010). Thus the meaning of the word “photosynthesis” – from the Greek φῶς, phōs, "light", and σύνθεσις, synthesis, "putting together" (Ke, 2001) has significance in the most broadest sense. Looking around and watching to fossils in old stones it seems that photosynthesis exists forever. However, how old is photosynthesis more precisely? It is generally believed the earth was formed around 4.54 billion years ago by accretion from the solar nebula and that life on earth began between 3.8 – 3.5 billion years ago (Noffke et al., 2013). In the Archean Era (3.9–2.5 billion years ago) the earliest photosynthetic activity was carried out by bacteria that did not evolve oxygen. These so-called anoxygenic photosynthetic bacteria are assumed to have used reductants such as H2, H2S, or ferrous iron, but not H2O. Oxygenic photosynthesis carried out by 6 cyanobacteria is thought to have been developed later (Olson, 2006). Evidences indicate that cyanobacteria evolved about 2 billion years ago leading to oxygen accumulation in the atmosphere. The presence of oxygen and the production of foodstuffs by higher plants made the existence of heterotrophs such as humans possible. Presently, the total biomass produced annually by plant photosynthesis amounts to about two hundred billion tons (Ke, 2001). Living creatures, including humans, consume the photosynthesised foodstuffs and gain energy from them by “respiration”, a process by which the organic compounds are oxidized back to carbon dioxide and water. Photosynthesis therefore serves as a vital link between the light energy of the sun and all living creatures (Ke, 2001). History of the study of photosynthesis Photosynthesis, as one of the most important processes on Earth, takes a central position in plant cell science. The first known scientific view on the process of photosynthesis was expressed by Aristotle (384 – 322 BC), the “father of biology”. He compared the soil (earth) to the stomach and assumed earth as the stomach of plants, as soon as they gain their nutrients directly from earth and water without having a “proper” digestive system. After observations of Aristotle, there is a big gap in the history of the research for 2000 years until the 17th century when the wave of interest to photosynthesis and plant science research arose with a new force. The next scientist who focused on photosynthesis was Jan Baptist van Helmont (1579 – 1644), an early modern period Flemish chemist, physiologist, and physician, who considered water to be the source of life and the basic nutrient for plants. Therefore, he devised an experiment by which he showed that small potted willows could thrive on soil and water alone while they gain their substance (weight) solely from the “water” as the weight of the soil in the pots did not decrease significantly. His works were collected and edited by his son Franciscus Mercurius van Helmont and the book “Ortus medicinae, vel opera et opuscula omnia” was published by Lodewijk Elzevir in Amsterdam in 1648 (NOYES, 1895) wherein the term “gas” (from the Greek word chaos) was used for the first time. After that time, the study of photosynthesis was slowly increasing. In our review, we cannot omit Marcello Malpighi (1628 – 1694), an Italian physician and biologist regarded as one of the fathers of microscopical anatomy and histology, who studied the anatomy of plants and insects concisely by making use of the 7 microscope. He claimed that plants take up nutrients which are dissolved in water via their roots. Overall, a pleiad of eminent scientists for over 300 years has made an invaluable contribution to the study of photosynthesis. Among them are persons as Robert Boyle, Joseph Priestley, Jan Ingenhousz, Julius Sachs, Kliment Arkadievich Timiryazev, Albert Einstein and many others. Between 1925–53, a number of novel techniques and methods enabled much more detailed research in plant physiology. It was the period that controlled growth in climatized growth chambers, ultracentrifugation, electron microscopy, x-ray-diffraction, thin layer and gas liquid chromatography and fluorescence spectrophotometry became available. Most of these techniques are still prevailing in modern research. Many of the central concepts of photosynthesis were established around the middle of the 20th century and at the same time, its basic mechanisms were clarified in more detail. For example, measurements of photosynthetic efficiency (quantum yield) at different wavelengths of light (Emerson and Lewis, 1943) led to the insight that two distinct forms of chlorophyll (Chl) must be excited in oxygenic photosynthesis. These results suggested the concept of two photochemical systems. The reaction centre pigments of photosystem II (PSII) and photosystem I (PSI) (P680 and P700, respectively) were found by studying changes in light absorbance in the red region (Kok, 1959), (Döring et al., 1969), (Tanaka and Makino, 2009). Chls with absorbance maxima corresponding to these specific wavelengths were proposed as the final light sink. These Chls were shown to drive electron transfer by charge separation. The linkage of electron transfer and CO2 assimilation was suggested by studies on Hill oxidant (Hill, 1937). A linear electron transport system with two light-driven reactions (Z scheme) was proposed based upon observations of the redox state of cytochromes (Hill and Bendall, 1960), (Duysens et al., 1961) and photophosphorylation was found to be associated with thylakoid fragments (Arnon et al., 1954). The metabolic pathway that assimilates carbon by fixation of CO2 was 14 discovered by Melvin Calvin's group, who used CO2 radioactive tracers in the 1950s (Bassham et al., 1950). This was the first significant discovery in biochemistry made using radioactive tracers, for which Calvin received the chemistry Noble prize in 1961. The primary reaction of CO2 fixation is catalyzed by ribulose-1,5-bisphosphate carboxylase/oxygenase, commonly known by the abbreviation Rubisco (Weissbach et al., 1956), initially called Fraction 1 protein (Wildman and Bonner, 1947). Rubisco is the most abundant protein in the world, largely because it is also the most inefficient 8 –1 one with the lowest catalytic turnover rate (1–3 s ). Another CO2 fixation pathway was found later in sugarcane (Hartt and Kortschak, 1964), (Hatch and Slack, 1966). It was named C4 photosynthesis (Tanaka and Makino, 2009) to discriminate it from the much more common C3 type of photosynthesis. One of the next breakthroughs to our understanding of photosynthesis was achieved by Hartmut Michel and Johann Deisenhofer. They made crystals of the photosynthetic reaction centre from Rhodopseudomonas viridis, an anaerobic photosynthetic bacterium,
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