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An Introduction to Primary Producers in the Sea: Who They Are, What They Do, and When They Evolved

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An Introduction to Primary Producers in the Sea: Who They Are, What They Do, and When They Evolved Job Name: 203043t CHAPTER 1 An Introduction to Primary Producers in the Sea: Who They Are, What They Do, and When They Evolved PAUL G. FALKOWSKI AND ANDREW H. KNOLL I. What Is Primary Production? II. How Is Photosynthesis Distributed in the Oceans? III. What Is the Evolutionary History of Primary Production in the Oceans? IV. Concluding Comments References Earth is approximately 4.6 billion years of the sun to catalyze the reaction (Knoll old, and for the past 4.3 billion years or so et al., Chapter 8, this volume). All complex there has been a persistent film of liquid life ultimately came to be dependent on water on its surface (Watson and Harrison oxygenic photosynthesis (Falkowski 2006; 2005). The original source of the water is not Raymond and Segre 2006). How and when known with certainty (Robert 2001; Drake this metabolic capacity evolved remains and Righter 2002); however, it is one of the one of the great unsolved scientific ques- most important features that distinguishes tions (Blankenship et al., Chapter 3, this this planet from all others in our solar sys- volume). Once it did evolve, however, tem. A second distinguishing feature is the genetic imprint spread via horizon- the abundance of molecular oxygen in the tal gene transfer and a series of symbiotic atmosphere. Based on the isotopic fractiona- associations to form a diverse photosyn- tion of sulfur, it would appear that oxygen thetic biota that would prove resilient to began to accumulate in the atmosphere and planetary catastrophes including global surface ocean between 2.4 and 2.3 billion glaciations, meteorite bombardments, and years ago (Ga) (Farquhar et al. 2000; Bekker massive volcanic eruptions while pro- et al. 2004), and in this case, the source is foundly and irreversibly altering Earth’s known: the oxidation, or “splitting,” of liquid chemistry. water in oceans and/or lakes by a group of In this book, we examine both the molec- organisms that evolved to utilize the energy ular biological issue of how water came to 1 Job Name: 203043t 2 1. AN INTRODUCTION TO PRIMARY PRODUCERS IN THE SEA be oxidized and the ecological and evolu- are called “primary producers.” Although tionary issues of this process, once evolved, not all primary producers are photosyn- which were appropriated and perpetuated thetic, all photosynthetic organisms are pri- by a wide variety of organisms living in mary producers. The rate of production of the oceans. As in all complex stories, there organic matter by the ensemble of primary remain many unanswered questions. producers determines the rate of energy flow, and hence production, of all other trophic levels in nearly every ecosystem I. WHAT IS PRIMARY (Lindeman 1942). PRODUCTION? Photosynthesis uses the energy of the sun to catalyze a redox reaction. The pro- On Earth, six major elements, H, C, O, cess requires an electron donor/acceptor N, P, and S overwhelmingly comprise the pair. The electron donor is coupled to a ingredients of life (Schlesinger 1997). With photoreceptor, such that upon absorption the single exception of P, the elements that of a single quantum at the appropriate form the major biopolymers, including pro- wavelength, a single electron is transferred teins, lipids, polysaccharides, and nucleic to the acceptor. This process takes approxi- acids, are incorporated primarily in reduced mately 1 picosecond. The primary accep- form; that is, they have received electrons tor, in turn, rapidly donates the electron in and/or protons from some source. Indeed, a stepwise fashion to other, lower energy electron or hydrogen transfer (redox) reac- acceptors, thereby both preventing a direct tions form the backbone of biological chem- backreaction with the donor (which would istry (Mauzerall, Chapter 2, this volume). lead to a useless, Sisyphean electron cycle) Earth’s early atmosphere is thought to and allowing the electron transfers to slow have been mildly reducing, containing CO2, down to millisecond time scales, thereby N2, H2O, and possibly CO in significant accommodating the kinetics of biochemi- amounts but probably not much CH4, H2S, cal reactions (Blankenship 2002). Ultimately or NH3 and almost certainly very little if any the electron, accompanied by a proton, is O2 (Kasting 1993). The addition of H2 to inor- used to reduce CO2 to the equivalent of a ganic carbon (i.e., CO2) to form organic mat- carboxyl group, COOH. Further electron ter (e.g., sugars, [CH2O]n) is endothermic, transfers yield increasingly reduced forms requiring an input of energy. Hence, this of organic carbon: the carboxyl group is reaction does not occur spontaneously on reduced to an aldehyde and/or ketone Earth’s surface at temperatures and pressures (intermediate metabolites), then to an alco- compatible with the co-occurrence of liquid hol (found in sugars and polysaccharides), water. Conversely, the oxidation of organic and ultimately to an alkane (C-H, found in carbon compounds produces energy that lipids). The donor is rereduced by an elec- can be used by organisms to make biopoly- tron ultimately extracted from a substrate 2+ mers. The ability to reduce inorganic carbon external to the cell, such as H2S, CH2O, Fe , to organic matter is restricted to a relatively or H2O. Of these potential substrates, H2O is small subset of metabolic pathways. Some the most abundant on Earth’s surface, but it bacteria and archaea exploit nonphoto- also requires the most energy to oxidize. chemical reactions to reduce inorganic car- The machinery that evolved to use water bon, but by far, photosynthesis is the most as a source of reductant is the most com- efficient, familiar, and widespread means plex energy transduction system in nature. of accomplishing this end (Falkowski and In all oxygenic photosynthetic organisms, Raven 2007). Because the organisms capable there are two photochemical reactions con- of this metabolic feat provide organic matter nected by a cytochrome. Molecular struc- for all other organisms in the ecosystem, they tural analyses clearly indicate that the two Job Name: 203043t II. HOW IS PHOTOSYNTHESIS DISTRIBUTED IN THE OCEANS? 3 photochemical reaction centers (each of II. HOW IS PHOTOSYNTHESIS which contains the primary donor and DISTRIBUTED IN THE OCEANS? acceptors covalently bound to specific amino residues in a protein complex) have This question has two answers, one ecologi- surprisingly similar structural topologies cal and one phylogenetic. How and when the (Blankenship et al., Chapter 3, this volume). two photosystems of anoxygenic photobacteria Both types of reaction centers are com- fused into one remains poorly understood (see posed of two different polypeptides (i.e., Martin, Chapter 5, this volume). What we do heterodimers) embedded within and span- know is that it happened exactly once—in the ning a nonphospholipid bilayer membrane. common ancestor of extant cyanobacteria, the The amino acid sequences of the proteins only prokaryotes capable of oxygenic photosyn- in the two reaction centers are very differ- thesis. Today, cyanobacteria form a moderately ent, however. Both structural and amino diverse clade, with species attaining ecological acid sequence homologies strongly sug- importance in eutrophic fresh waters, in the gest that one of the reaction center dimers, peritidal benthos where salinity or migrating designated photosystem II, is derived from sands limit algal competitors and animal graz- purple bacteria, a group of anaerobic photo- ers (see Hamm and Smetacek, Chapter 14, synthetic organisms incapable of oxidizing this volume), and in mid-gyre phytoplankton. water. However, unlike in the purple sulfur The group has attained far greater distribu- bacteria, photosystem II contains a quartet tion, however, as the plastids of photosynthetic of Mn atoms and a Ca atom bound to amino eukaryotes (Bhattacharya and Medlin 1998). acids in the protein heterodimer on one side Oxygenic photosynthesis in eukaryotic cells of the membrane (Ferreira et al. 2004). This originated via an endosymbiotic event in which metal center forms the heart of the water cyanobacteria were incorporated as symbionts oxidizing machine; it has no known ana- and subsequently reduced to metabolic slaves logue elsewhere in nature. The second pho- within their host cells. The progeny of this tosystem (photosystem I) is derived from fusion not only diversified to become the hun- green sulfur bacteria and uses a set of iron dreds of thousands of glaucophyte, red algal, sulfur clusters as primary electron accep- green algal, and land plant species found today tors. The primary role of this photosystem is but also provided the autotrophic partner for to use the energy of light to drive electrons six or more new rounds of endosymbiosis that extracted from water by photosystem II to spread photosynthesis widely throughout lower (more electrically negative) poten- the eukaryotic domain (see Hackett et al., tials, where ultimately the electron is used to Chapter 7; Fehling et al., Chapter 6, this reduce ferridoxin. Although both photosys- volume). tems (like their anoxygenic, bacterial coun- On land, photosynthesis is dominated by terparts) can operate in a cycle to generate a single clade derived from the charophyte transmembrane electrical fields that can be green algae, the embryophytic land plants coupled to adenosine triphosphate (ATP) (see O’Kelly, Chapter 13, this volume). A few formation (Blankenship 1992), the efficiency vascular plants have secondarily recolonized of cyclic electron transport around photo- coastal marine waters, but photoautotrophy system I is extremely high. Indeed, in the in the oceans springs from much more diverse biological reduction of N2 in some species phylogenetic sources. Green algae play a of cyanobacteria, a special, differentiated role, especially small flagellates, common in cell, the heterocyst, loses all photosystem coastal blooms and in open ocean picoplank- II activity (and hence no longer generates ton. Secondary endosymbioses, involving oxygen) but retains cyclic photochemically green algae as the autotrophic partner, have driven electron flow around photosystem I resulted in three further groups of algae: to provide energy (Wolk et al.
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