Aquatic Photosynthesis – Second Edition - Softcover

Falkowski, Paul G.; Raven, John A; Raven, John A.

Softcover

ISBN 10: 0691115516 ISBN 13: 9780691115511

Publisher: Princeton University Press, 2007

Synopsis

Aquatic Photosynthesis is a comprehensive guide to understanding the evolution and ecology of photosynthesis in aquatic environments. This second edition, thoroughly revised to bring it up to date, describes how one of the most fundamental metabolic processes evolved and transformed the surface chemistry of the Earth. The book focuses on recent biochemical and biophysical advances and the molecular biological techniques that have made them possible.


In ten chapters that are self-contained but that build upon information presented earlier, the book starts with a reductionist, biophysical description of the photosynthetic reactions. It then moves through biochemical and molecular biological patterns in aquatic photoautotrophs, physiological and ecological principles, and global biogeochemical cycles. The book considers applications to ecology, and refers to historical developments. It can be used as a primary text in a lecture course, or as a supplemental text in a survey course such as biological oceanography, limnology, or biogeochemistry.

About this title

About the Author

Paul G. Falkowski is Board of Governors Professor in Environmental Biophysics and Molecular Ecology in the Institute of Marine and Coastal Sciences and the Department of Geological Sciences at Rutgers University. He has published numerous articles in "Science, Nature", and "Scientific American". John A. Raven is Boyd Baxter Professor of Biology at the University of Dundee, Scotland. His books include "Energetics and Transport in Aquatic Plants".

From the Back Cover

"Aquatic Photosynthesis is an excellent reference text for undergraduate-level courses and is a good text for specialist courses (advanced undergraduate and postgraduate). Everyone who works on aquatic photosynthesis should own this text and most people entering the field at the postgraduate or professional level will purchase it."--Richard J. Geider, University of Essex

"It's a great book. It will be very useful for all biologists and oceanographers."--Govindjee, University of Illinois, Urbana-Champaign

Excerpt. © Reprinted by permission. All rights reserved.

Aquatic Photosynthesis

By Paul G. Falkowski John A. Raven

Princeton University Press

Copyright © 2007 Princeton University Press
All right reserved.
ISBN: 978-0-691-11551-1

Chapter One

An Introduction to Photosynthesis in Aquatic Systems

Photosynthesis is the biological conversion of light energy to chemical bond energy that is stored in the form of organic carbon compounds. Approximately 45% of the photosynthesis on Earth each year occurs in aquatic environments (Falkowski 1994; Field et al. 1998). However, because we live on land and the aggregate biomass of aquatic plants amounts to less than 1% of the total photosynthetic biomass on our planet, terrestrial plants are much more a part of the human experience (Table 1.1). Consequently, the role and importance of aquatic photosynthetic organisms in shaping the ecology and biogeochemistry of Earth often is not appreciated by most students of photosynthesis.

In virtually all aquatic ecosystems, including the open ocean, lakes, continental margins, rivers, and estuaries, photosynthesis supplies the primary source of organic matter for the growth and metabolic demands of all the other organisms in the ecosystem. Hence, the rate of photosynthesis places an upper bound on the overall biomass and productivity of ecosystems and constrains the overall biological flow of energy on the surface of this planet. Over two billion years ago, aquatic photosynthetic organisms permanently altered Earth's atmosphere through the addition of a highly reactive gas, oxygen (Farquhar et al. 2000; Bekker et al. 2004), a phenomenon that ultimately permitted multicellular animals, including humans, to evolve (Knoll 2003). A small fraction of the fossilized organic remains of aquatic photosynthetic organisms would become petroleum and natural gas that simultaneously fuels contemporary civilization and serves as chemical feedstocks for innumerable industries, including plastics, dyes, and pharmaceuticals. The fossilized remains of calcareous nanoplankton, deposited over millions of years in ancient ocean basins, are mined for building materials. Siliceous oozes are used as additives for reflective paints, polishing materials, abrasives, and insulation. Aquatic photosynthetic organisms are key sources of vitamins and other high-quality biochemicals. This list could go on, but our point is that an understanding aquatic photosynthesis is not merely an academic exercise. Rather it provides a vantage point from which to explore how living and fossil aquatic photosynthetic organisms have influenced the biological and geochemical history and dynamics of Earth.

Historically, most of the detailed biochemical, biophysical, and molecular biological information about photosynthetic processes comes from studies of higher plants and a few model algae, including Synechocystis, Chlamydomonas, Chlorella, and Phaeodactylum (Kaplan and Reinhold 1999; Harris 1989; Rochaix 1995; Grossman 2000). Traditionally, most model organisms have been chosen because they are easily grown or can be genetically manipulated rather than because they are ecologically important. There are significant differences between terrestrial and aquatic environments that affect and are reflected in photosynthetic processes. These differences have led to a variety of evolutionary adaptations and physiological acclimations of the photosynthetic apparatus in aquatic organisms that are without parallel in terrestrial plants. Moreover, there is sufficient knowledge of the basic mechanisms and principles of photosynthetic processes in aquatic organisms to provide a basic understanding of how they respond to changes in their environment. Such interpretations form the foundation of aquatic ecophysiology and are requisite to understanding both community structure and global biogeochemical cycles in marine and freshwater environments.

We strive here to describe some of the basic concepts and mechanisms of photosynthetic processes, with the overall goal of developing an appreciation of the adaptations and acclimations that have led to the abundance, diversity, and productivity of photosynthetic organisms in aquatic ecosystems. In this introductory chapter we briefly examine the overall photosynthetic process, the geochemical and biological evidence for the evolution of oxygenic photosynthetic organisms, and the concepts of life-forms and nutritional modes. Many of these themes are explored in detail in subsequent chapters.

A Description of the Overall Photosynthetic Process

The biological economy of Earth is based on the chemistry of carbon. The vast majority of carbon on Earth is in an oxidized, inorganic form; that is, it is combined with molecular oxygen and is in the form of the gas carbon dioxide (C[O.sub.2]) or its hydrated or ionic equivalents, namely bicarbonate (HC[O.sup.-.sub.3]) and carbonate (C[O.sup.2-.sub.3]). These inorganic forms of carbon are interconvertible but thermodynamically stable. They contain no biologically usable energy, nor can they be used directly to form organic molecules without undergoing a chemical or biochemical reaction. To extract energy from carbon or to use the element to build organic molecules, the carbon must be chemically reduced, which requires an investment in free energy. There are only a handful of biological mechanisms extant for the reduction of inorganic carbon; on a global basis photosynthesis is the most familiar, most important, and most extensively studied.

Photosynthesis can be written as an oxidation-reduction reaction of the general form Pigment

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] (1.1)

Note that in this representation of photosynthesis light is specified as a substrate; the energy of the absorbed light is stored in the products. All photosynthetic bacteria, with the important exceptions of the cyanobacteria (including the prochlorophytes) and a group of aerobic photoheterotrophs (Kolber et al. 2000), are capable of fixing carbon only under anaerobic conditions and are incapable of evolving oxygen. In these organisms compound A is, for example, an atom of sulfur and the pigments are bacteriochlorophylls (Blankenship et al. 1995; van Niel 1941). All other photosynthetic organisms, including the cyanobacteria, prochlorophytes, eukaryotic algae, and higher plants, are oxygenic; that is, Eq. 1.1 can be modified to

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] (1.2)

where Chl a is the ubiquitous plant pigment chlorophyll a. Equation 1.2 implies that somehow chlorophyll a catalyzes a reaction or a series of reactions whereby light energy is used to oxidize water:

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] (1.3)

yielding gaseous, molecular oxygen. Equation 1.3 represents the so-called "light reactions" of oxygenic photosynthesis. The processes that constitute the light reactions are discussed in chapters 2 and 3.

Equation 1.3 describes an oxidation process. Specifically, it is a partial reaction, where electrons are extracted from water to form molecular oxygen. This process is the heart of one of two groups of reactions in oxygenic photosynthesis. The other reaction, the reduction of C[O.sub.2], also can be described by

C[O.sub.2] + 4[H.sup.+] + 4[e.sup.-] [right arrow] C[H.sub.2]O + [H.sub.2]O (1.4)

As free electrons are normally not found in biological systems, the reaction described by Eq. 1.3 and 1.4 requires the formation of an intermediate reducing agent that is not shown explicitly. The form of, and mechanism for, the generation of reductants is discussed in chapter 4.

Although the biological reduction of C[O.sub.2] may be thermodynamically permitted on theoretical grounds by, for example, mixing a biological reducing agent such as NADPH with C[O.sub.2], the reaction will not spontaneously proceed. Enzymes are required to facilitate the reduction process. Given the substrates and appropriate enzymes, the reactions that lead to carbon reduction can proceed in the dark as well as the light. These so-called "dark reactions" are coupled to the light reactions by common intermediates and by enzyme regulation. Although there are variations on the metabolic pathways for carbon reduction, the initial dark reaction, whereby C[O.sub.2] is temporarily "fixed" to an organic molecule, is highly conserved throughout all photosynthetic organisms. We examine the dark reactions in chapter 5.

An Introduction to Oxidation-Reduction Reactions

The term oxidation was originally proposed by chemists in the latter part of the 18th century to describe reactions involving the addition of oxygen to metals, forming metallic oxides. For example,

3Fe + 2[O.sub.2] [right arrow] [Fe.sub.3][O.sub.4] (1.5)

The term reduction was used to describe the reverse reaction, namely, the removal of oxygen from a metallic oxide, for example, by heating with carbon:

[Fe.sub.3][O.sub.4] + 2C [right arrow] 3Fe + 2C[O.sub.2] (1.6)

Subsequent analysis of these reactions established that the addition of oxygen is accompanied by the removal of electrons from an atom or molecule. Conversely, reduction is accompanied by the addition of electrons. In the specific case of organic reactions that involve the reduction of carbon, the addition of electrons is usually balanced by the addition of protons. For example, the reduction of carbon dioxide to formaldehyde requires the addition of four electrons and four [H.sup.+]-that is, the equivalent of four hydrogen atoms:

O = C = O + 4[e.sup.-] + 4[H.sup.+] [right arrow] C[H.sub.2]O + [H.sub.2]O (1.7)

Thus, from the perspective of organic chemistry, oxidation may be defined as the addition of oxygen, the loss of electrons, or the loss of hydrogen atoms (but not hydrogen ions, [H.sup.+]); conversely, reduction can be defined as the removal of oxygen, the addition of electrons, or the addition of hydrogen atoms.

Oxidation-reduction reactions only occur when there are pairs of substrates, forming pairs of products:

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] (1.8)

In oxygenic photosynthesis, C[O.sub.2] is the recipient of the electrons and protons, and thus becomes reduced (it is the A in Eq. 1.8). Water is the electron and proton donor, and thus becomes oxidized (it is the B in Eq.1.8).The oxidation of two moles of water (Eq. 1.3) requires the addition of 495 kJ. The reduction of C[O.sub.2] to the simplest organic carbon molecule, formaldehyde, adds 176 kJ of energy. The energetic efficiency of photosynthesis can be calculated by dividing the energy stored in organic matter by that required to split water into molecular hydrogen and oxygen. Thus, the maximum overall efficiency of photosynthesis, assuming no losses at any intermediate step, is 176/495 or about 36%. We discuss the thermodynamics of oxidation-reduction reactions more fully in chapter 4.

The Photosynthetic Apparatus

The light reactions and the subsequent movement of protons and electrons through the photosynthetic machinery to form chemical bond energy and reductants are reactions associated with, or occurring in, membranes (Anderson and Andersson 1988; Staehelin 1986). The fixation and subsequent biochemical reduction of carbon dioxide to organic carbon compounds are processes occurring in the aqueous phase, that is, not in membranes. The ensemble of the biochemical elements that facilitate these processes constitute the photosynthetic apparatus. In most anaerobic photosynthetic bacteria and cyanobacteria, the photosynthetic light reactions are organized on membranes that are arranged in sheets or lamellae adjacent to the periplasmic membrane (Blankenship et al. 1995; Bryant 1994) (Fig. 1.1a). The dark reactions are generally localized in the center of the cell. In eukaryotic cells, the photosynthetic apparatus is organized in special organelles, the chloroplasts, which contain alternating layers of lipoprotein membranes and aqueous phases (Staehelin 1986) (Fig. 1.1b).

The lipoprotein membranes of eukaryotic cell chloroplasts are called thylakoids, and contain two major lipid components, mono- and digalactosyldiacylglycerol (MGDG and DGDG, respectively), arranged in a bilayer approximately 4 nm thick (1 nm = [10.sup.-9] m = 10 ) in which proteins and other functional molecules are embedded (Singer and Nicolson 1972) (Fig. 1.2). Unlike most of the lipids associated with membranes in a cell, the lipids in thylakoid membranes are not phospholipids (Murphy 1986). Like most biological membranes, thylakoids are not symmetrical; that is, some of the components span the membrane completely, whereas others are embedded only partially (Cramer and Knaff 1990). The thylakoid membranes form closed vesicles around an aqueous, intrathylakoid space. This structure is analogous to the pocket in pita bread, the pocket being called the lumen. The proteins and pigments that constitute the two light reactions, as well as most of the electron transfer components that link them, and the catalysts involved in oxygen evolution and ATP synthesis are organized laterally along the membrane (Fig. 1.3). In addition, although there are some important exceptions, thylakoid membranes contain the major light-harvesting pigment-protein complexes; hence, when isolated from cells, thylakoids are characteristically colored (Larkum and Barrett 1983; Green and Durnford 1996).

Surrounding the thylakoids is an aqueous phase, the stroma. Soluble proteins in the stroma use chemical reductants and energy generated by the biochemical reactions in the thylakoid membranes to reduce C[O.sub.2], N[O.sup.-.sub.2], and S[O.sup.2-.sub.4], thereby forming organic carbon compounds, ammonium and amino acids, and organic sulfide compounds, respectively. The stroma also contains functional DNA (nucleoids), ribosomal (r), messenger (m), and transfer (t) RNAs, as well as all the associated enzymes for transcription and translation of the chloroplast genome (Kirk and Tilney-Bassett 1978; Reith and Munholland 1993; Grzebyk et al. 2003).

The stroma, in turn, is surrounded by two to four plastid envelope membranes (depending on the organism) that, in some organisms, are connected to the nucleus and separated from each other by an aqueous intermembrane compartment (Berner 1993). The inner envelope membrane has a number of integral membrane proteins, which selectively transport photosynthetic substrates into the stroma and photosynthetic products out of it. The outer envelope membrane also has integral membrane proteins, called porins, which permit nonselective transport of solutes less than about 800 Da, such as C[O.sub.2], [O.sub.2], inorganic phosphate, ATP, and so on (Raven and Beardall 1981b).

The Role of Membranes in Photosynthesis

The structure of the chloroplast illustrates some important features of photosynthetic processes. All photosynthetic organisms, whether they be prokaryotes, eukaryotic algae, or higher plants, use membranes to organize photosynthetic electron transport processes and separate these processes from carbon fixation (Bryant 1994; Drews 1985; Redlinger and Gantt 1983). Biological membranes serve many purposes. One is to control the fluxes of solutes between compartments within cells and between cells. A second is to separate electrical charges across the membrane. Finally, membranes facilitate spatial organization of chemical reactions. These three roles of membranes are related to each other.

Chemical reactions are scalar processes-they have no intrinsic relationship to their spatial environment. The orientation of proteins and prosthetic groups within membranes allows the coupling of scalar photochemical reactions to vectorial fluxes of electrons, ions, and neutral solutes (Cramer and Knaff 1990). In the context of the photosynthetic apparatus, "vectorial" refers to a process whereby specific products of biochemical reactions accumulate on only one side of a thylakoid membrane, thereby forming concentration gradients across the membrane. The vectorial translocation of ions and electrons helps establish an electrical field across the membrane. Because membranes allow for spatial organization of enzymes and other proteins, mechanical (vectorially oriented) actions, on a molecular scale, can be coupled to the dissipation of the electrochemical (scalar) energy. For example, protons can be transported from one side of a membrane to other at the expense of ATP hydrolysis, and vice versa. These processes, which would be energetically futile in solution, are highly profitable when employed by a membrane.

Evolution of Oxygenic Photosynthesis: Geochemical Evidence

The evolution of biological membranes is obscure, but must have been one of the earliest processes in the origins of life on Earth (Benner et al. 2002). The origins of photosynthesis are also obscure, but geochemical imprints and molecular biological inferences can be used to reconstruct some of the key events.

(Continues...)

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Edition details

• Publisher: Princeton University Press
• Publication date: 2007
• Language: English
• ISBN 10: 0691115516
• ISBN 13: 9780691115511
• Binding: Paperback
• Edition number: 2
• Number of pages: 488