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C H A P T E R

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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 old, and for the past 4.3 billion years or so there has been a persistent film of liquid water on its surface (Watson and Harrison 2005). The original source of the water is not known with certainty (Robert 2001; Drake and Righter 2002); however, it is one of the most important features that distinguishes this planet from all others in our solar sys-tem. A second distinguishing feature is the abundance of molecular oxygen in the atmosphere. Based on the isotopic fractiona-tion of sulfur, it would appear that oxygen began to accumulate in the atmosphere and surface ocean between 2.4 and 2.3 billionyears ago (Ga) (Farquhar et al. 2000; Bekker et al. 2004), and in this case, the source is known: the oxidation, or “splitting,” of liquid water in oceans and/or lakes by a group of organisms that evolved to utilize the energy

of the sun to catalyze the reaction (Knoll et al., Chapter 8, this volume). All complex life ultimately came to be dependent on oxygenic photosynthesis (Falkowski 2006; Raymond and Segre 2006). How and when this metabolic capacity evolved remains one of the great unsolved scientific ques-tions (Blankenship et al., Chapter 3, this volume). Once it did evolve, however, the genetic imprint spread via horizon-tal gene transfer and a series of symbiotic associations to form a diverse photosyn-thetic biota that would prove resilient to planetary catastrophes including global glaciations, meteorite bombardments, and massive volcanic eruptions while pro-foundly and irreversibly altering Earth’s chemistry.

In this book, we examine both the molec-ular biological issue of how water came to

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be oxidized and the ecological and evolu-tionary issues of this process, once evolved, which were appropriated and perpetuated by a wide variety of organisms living in the oceans. As in all complex stories, there remain many unanswered questions.

I. WHAT IS PRIMARY PRODUCTION?

On Earth, six major elements, H, C, O, N, P, and S overwhelmingly comprise the ingredients of life (Schlesinger 1997). With the single exception of P, the elements that form the major biopolymers, including pro-teins, lipids, polysaccharides, and nucleic acids, are incorporated primarily in reduced form; that is, they have received electrons and/or protons from some source. Indeed, electron or hydrogen transfer (redox) reac-tions form the backbone of biological chem-istry (Mauzerall, Chapter 2, this volume).

Earth’s early atmosphere is thought to have been mildly reducing, containing CO2, N2, H2O, and possibly CO in significant amounts but probably not much CH4, H2S, or NH3 and almost certainly very little if any O2 (Kasting 1993). The addition of H2 to inor-ganic carbon (i.e., CO2) to form organic mat-ter (e.g., sugars, [CH2O]n) is endothermic, requiring an input of energy. Hence, this reaction does not occur spontaneously on Earth’s surface at temperatures and pressures compatible with the co-occurrence of liquid water. Conversely, the oxidation of organic carbon compounds produces energy that can be used by organisms to make biopoly-mers. The ability to reduce inorganic carbon to organic matter is restricted to a relatively small subset of metabolic pathways. Some bacteria and archaea exploit nonphoto-chemical reactions to reduce inorganic car-bon, but by far, photosynthesis is the most efficient, familiar, and widespread means of accomplishing this end (Falkowski and Raven 2007). Because the organisms capable of this metabolic feat provide organic matter for all other organisms in the ecosystem, they

are called “primary producers.” Although not all primary producers are photosyn-thetic, all photosynthetic organisms are pri-mary producers. The rate of production of organic matter by the ensemble of primary producers determines the rate of energy flow, and hence production, of all other trophic levels in nearly every ecosystem (Lindeman 1942).

Photosynthesis uses the energy of the sun to catalyze a redox reaction. The pro-cess requires an electron donor/acceptor pair. The electron donor is coupled to a photoreceptor, such that upon absorption of a single quantum at the appropriate wavelength, a single electron is transferred to the acceptor. This process takes approxi-mately 1 picosecond. The primary accep-tor, in turn, rapidly donates the electron in a stepwise fashion to other, lower energy acceptors, thereby both preventing a direct backreaction with the donor (which would lead to a useless, Sisyphean electron cycle) and allowing the electron transfers to slow down to millisecond time scales, thereby accommodating the kinetics of biochemi-cal reactions (Blankenship 2002). Ultimately the electron, accompanied by a proton, is used to reduce CO2 to the equivalent of a carboxyl group, COOH. Further electron transfers yield increasingly reduced forms of organic carbon: the carboxyl group is reduced to an aldehyde and/or ketone (intermediate metabolites), then to an alco-hol (found in sugars and polysaccharides), and ultimately to an alkane (C-H, found in lipids). The donor is rereduced by an elec-tron ultimately extracted from a substrate external to the cell, such as H2S, CH2O, Fe2+, or H2O. Of these potential substrates, H2O is the most abundant on Earth’s surface, but it also requires the most energy to oxidize.

The machinery that evolved to use water as a source of reductant is the most com-plex energy transduction system in nature. In all oxygenic photosynthetic organisms, there are two photochemical reactions con-nected by a cytochrome. Molecular struc-tural analyses clearly indicate that the two

2 1. AN INTRODUCTION TO PRIMARY PRODUCERS IN THE SEA

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photochemical reaction centers (each of which contains the primary donor and acceptors covalently bound to specific amino residues in a protein complex) have surprisingly similar structural topologies (Blankenship et al., Chapter 3, this volume). Both types of reaction centers are com-posed of two different polypeptides (i.e., heterodimers) embedded within and span-ning a nonphospholipid bilayer membrane. The amino acid sequences of the proteins in the two reaction centers are very differ-ent, however. Both structural and amino acid sequence homologies strongly sug-gest that one of the reaction center dimers, designated photosystem II, is derived from purple bacteria, a group of anaerobic photo-synthetic organisms incapable of oxidizing water. However, unlike in the purple sulfur bacteria, photosystem II contains a quartet of Mn atoms and a Ca atom bound to amino acids in the protein heterodimer on one side of the membrane (Ferreira et al. 2004). This metal center forms the heart of the water oxidizing machine; it has no known ana-logue elsewhere in nature. The second pho-tosystem (photosystem I) is derived from green sulfur bacteria and uses a set of iron sulfur clusters as primary electron accep-tors. The primary role of this photosystem is to use the energy of light to drive electrons extracted from water by photosystem II to lower (more electrically negative) poten-tials, where ultimately the electron is used to reduce ferridoxin. Although both photosys-tems (like their anoxygenic, bacterial coun-terparts) can operate in a cycle to generate transmembrane electrical fields that can be coupled to adenosine triphosphate (ATP) formation (Blankenship 1992), the efficiency of cyclic electron transport around photo-system I is extremely high. Indeed, in the biological reduction of N2 in some species of cyanobacteria, a special, differentiated cell, the heterocyst, loses all photosystem II activity (and hence no longer generates oxygen) but retains cyclic photochemically driven electron flow around photosystem I to provide energy (Wolk et al. 1994).

II. HOW IS PHOTOSYNTHESIS DISTRIBUTED IN THE OCEANS?

This question has two answers, one ecologi-cal and one phylogenetic. How and when the two photosystems of anoxygenic photobacteria fused into one remains poorly understood (see Martin, Chapter 5, this volume). What we do know is that it happened exactly once—in the common ancestor of extant cyanobacteria, the only prokaryotes capable of oxygenic photosyn-thesis. Today, cyanobacteria form a moderately diverse clade, with species attaining ecological importance in eutrophic fresh waters, in the peritidal benthos where salinity or migrating sands limit algal competitors and animal graz-ers (see Hamm and Smetacek, Chapter 14, this volume), and in mid-gyre phytoplankton. The group has attained far greater distribu-tion, however, as the plastids of photosynthetic eukaryotes (Bhattacharya and Medlin 1998). Oxygenic photosynthesis in eukaryotic cells originated via an endosymbiotic event in which cyanobacteria were incorporated as symbionts and subsequently reduced to metabolic slaves within their host cells. The progeny of this fusion not only diversified to become the hun-dreds of thousands of glaucophyte, red algal, green algal, and land plant species found today but also provided the autotrophic partner for six or more new rounds of endosymbiosis that spread photosynthesis widely throughout the eukaryotic domain (see Hackett et al., Chapter 7; Fehling et al., Chapter 6, this volume).

On land, photosynthesis is dominated by a single clade derived from the charophyte green algae, the embryophytic land plants (see O’Kelly, Chapter 13, this volume). A few vascular plants have secondarily recolonized coastal marine waters, but photoautotrophy in the oceans springs from much more diverse phylogenetic sources. Green algae play a role, especially small flagellates, common in coastal blooms and in open ocean picoplank-ton. Secondary endosymbioses, involving green algae as the autotrophic partner, have resulted in three further groups of algae: the chlorarachniophytes, the photosynthetic

II. HOW IS PHOTOSYNTHESIS DISTRIBUTED IN THE OCEANS? 3

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4 1. AN INTRODUCTION TO PRIMARY PRODUCERS IN THE SEA

euglenids, and certain dinoflagellates. None are ecologically prominent in the oceans.

Red algae are diverse and ecologically important as seaweeds, but they do not at present play a significant role in the phyto-plankton. In contrast, photosynthetic clades containing plastids that originated as red algal symbionts dominate primary production in many parts of the oceans. The heterokonts, surely one of evolution’s great success stories, include both abundant and diverse seaweeds (e.g., the kelps) and the ubiquitous diatoms found on land and in the sea as microb-enthos and phytoplankton (see Kooistra et al., Chapter 11, this volume). Another ecologically important group in the marine phytoplankton is the haptophyte algae, especially the calcite-precipitating coccolithophorids (see de Vargas et al., Chapter 12, this volume). Like photo-synthetic heterokonts, haptophytes capable of photosynthesis have red-algal–derived plastids.

About half of known dinoflagellate spe-cies are photosynthetic, and most of these also contain plastids derived from the red algal line (see Delwiche, Chapter 10, this volume). Dinoflagellates are photosynthet-ically promiscuous, however. In addition to the red and green plastids already men-tioned, they include species with plastids derived from a tertiary endosymbiosis that incorporated a haptophyte alga.

The phylogenetic diversity of marine pho-toautotrophs correlates with observed ecolog-ical heterogeneity of primary producers, with green, red, and brown seaweeds along coasts (and the remarkable floating brown alga Sargassum proliferating far from shore); dia-toms, dinoflagellates, and coccolithophorids dominating shelf phytoplankton; and cyano-bacterial and green picoplankton in oligo-trophic mid-ocean environments.

What biological or environmental con-ditions drove the spread of photosynthesis through the Eucarya? And why did green algae come to cover the land, whereas algae with “red” plastids dominate many parts of the oceans? The factors that selected for pri-marily red secondary endosymbiotic algae in the modern ocean are not well understood

(Falkowski et al. 2003); however, it appears that the trace element composition of these organisms differs significantly from that of green algae (Quigg et al. 2003), potentially reflecting the redox conditions of the oceans, especially from the end-Permian extinction to present. It has been hypothesized that red plastids originated once, early in the history of the so-called chromalveolate clade, and spread during the radiation of these diverse protists (a group that includes dinoflagel-lates, heterokonts, and haptophytes, all of which contain heterotrophic lineages in their basal branches) (Cavalier-Smith 2002). This “Chromalveolate hypothesis” implies that the extant heterotrophic species in this group had plastids but somehow lost them for unknown reasons. The hypothesis has some support from molecular phylogeny (see Hackett et al., Chapter 7; Delwiche, Chapter 10; de Vargas et al., Chapter 12, this volume) but remains controversial (Grzebyk et al. 2003). Regardless of whether red sec-ondary plastids were incorporated into host cells once or multiple times, organisms pos-sessing this type of plastid have generally extremely large absorption cross sections for light, and red plastids appear to be well suited for photosynthesis at very low photon fluxes (see Green, Chapter 4, this volume).

III. WHAT IS THE EVOLUTIONARY HISTORY OF

PRIMARY PRODUCTION IN THE OCEANS?

The distribution of photosynthesis on the tree of life implies a complex history of photosynthesis in the oceans, and the geo-logical record confirms that this is the case. The present structure—both ecological and phylogenetic—of autotrophy in marine ecosystems originated only about 200 mil-lion years ago (Ma) (see Katz et al., Chapter 18, this volume). What governed the succes-sive Mesozoic radia tions of dinoflagellates, coccolithophorids, and diatoms, and what did earlier oceans look like? It appears that

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green algae were more abundant in the Paleozoic oceans (see Payne and van de Schootbrugge, Chapter 9; Knoll et al., Chapter 8, this volume).

Neither do the environmental influences of the algae stop with the carbon cycle (see Guidry et al., Chapter 17, this volume). The calcitic coccoliths precipitated by coccol-ithoporids constitute a major sink for cal-cium carbonate, for the first time providing a significant flux of carbonate to the deep seafloor (Litchman, Chapter 16, this volume). Diatoms, in turn, have come to dominate the oceans’ silica cycle, influencing the evolution-ary trajectories of heterotrophs such as radi-olarians and siliceous sponges. The fluxes of these “hard parts,” which probably evolved as a protective mechanism against grazing (see Hamm and Smetacek, Chapter 14; Finkel, Chapter 15, this volume), were also accom-panied by the flux of organic matter into the ocean interior. The degradation and oxida-tion of this organic matter has “imprinted” the ocean interior with a nitrogen–phosphate ratio that is unique to that ecosystem and is an example of an “emergent” property of the co-evolution of the chemistry of the sea and the organisms that live in it (Falkowski 2001).

IV. CONCLUDING COMMENTS

The study of the evolution of marine pho-toautotrophs has a long and venerable history but, perhaps surprisingly, has been largely over-looked by both students and scholars of bio-logical oceanography. We hope that this book will give suchstudents access to a new under-standing of the organisms responsible for half of the primary production on the planet. Our understanding of evolution of marine photo-autotrophs has been greatly enriched in recent years as information in the fields of molecular biology, algal physiology and biophysics, pale-ontology, genomics, and Earth systems history have been more integrated. The chapters in this volume are an attempt at such an integra-tion. It is our hope that the readers of this book will not only find the information useful but also, that students especially will be inspired to identify and address new questions.

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