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. 1994). the chlorarachniophytes, the photosynthetic Job Name: 203043t

4 1. AN INTRODUCTION TO PRIMARY PRODUCERS IN THE SEA euglenids, and certain dinoflagellates. None (Falkowski et al. 2003); however, it appears are ecologically prominent in the oceans. that the trace element composition of these Red algae are diverse and ecologically organisms differs significantly from that of important as seaweeds, but they do not at green algae (Quigg et al. 2003), potentially present play a significant role in the phyto- reflecting the redox conditions of the oceans, plankton. In contrast, photosynthetic clades especially from the end-Permian extinction containing plastids that originated as red algal to present. It has been hypothesized that red symbionts dominate primary production in plastids originated once, early in the history many parts of the oceans. The heterokonts, of the so-called chromalveolate clade, and surely one of evolution’s great success stories, spread during the radiation of these diverse include both abundant and diverse seaweeds protists (a group that includes dinoflagel- (e.g., the kelps) and the ubiquitous diatoms lates, heterokonts, and haptophytes, all of found on land and in the sea as microb- which contain heterotrophic lineages in their enthos and phytoplankton (see Kooistra et al., basal branches) (Cavalier-Smith 2002). This Chapter 11, this volume). Another ecologically “Chromalveolate hypothesis” implies that important group in the marine phytoplankton the extant heterotrophic species in this is the haptophyte algae, especially the calcite- group had plastids but somehow lost them precipitating coccolithophorids (see de Vargas for unknown reasons. The hypothesis has et al., Chapter 12, this volume). Like photo- some support from molecular phylogeny synthetic heterokonts, haptophytes capable (see Hackett et al., Chapter 7; Delwiche, of photosynthesis have red-algal–derived Chapter 10; de Vargas et al., Chapter 12, this plastids. volume) but remains controversial (Grzebyk About half of known dinoflagellate spe- et al. 2003). Regardless of whether red sec- cies are photosynthetic, and most of these ondary plastids were incorporated into host also contain plastids derived from the red cells once or multiple times, organisms pos- algal line (see Delwiche, Chapter 10, this sessing this type of plastid have generally volume). Dinoflagellates are photosynthet- extremely large absorption cross sections ically promiscuous, however. In addition for light, and red plastids appear to be to the red and green plastids already men- well suited for photosynthesis at very low tioned, they include species with plastids photon fluxes (see Green, Chapter 4, this derived from a tertiary endosymbiosis that volume). incorporated a haptophyte alga. The phylogenetic diversity of marine pho- toautotrophs correlates with observed ecolog- III. WHAT IS THE ical heterogeneity of primary producers, with EVOLUTIONARY HISTORY OF green, red, and brown seaweeds along coasts PRIMARY PRODUCTION IN (and the remarkable floating brown alga THE OCEANS? Sargassum proliferating far from shore); dia- toms, dinoflagellates, and coccolithophorids The distribution of photosynthesis on dominating shelf phytoplankton; and cyano- the tree of life implies a complex history of bacterial and green picoplankton in oligo- photosynthesis in the oceans, and the geo- trophic mid-ocean environments. logical record confirms that this is the case. What biological or environmental con- The present structure—both ecological and ditions drove the spread of photosynthesis phylogenetic—of autotrophy in marine through the Eucarya? And why did green ecosystems originated only about 200 mil- algae come to cover the land, whereas algae lion years ago (Ma) (see Katz et al., Chapter with “red” plastids dominate many parts of 18, this volume). What governed the succes- the oceans? The factors that selected for pri- sive Mesozoic radiations of dinoflagellates, marily red secondary endosymbiotic algae coccolithophorids, and diatoms, and what in the modern ocean are not well understood did earlier oceans look like? It appears that Job Name: 203043t

REFERENCES 5 green algae were more abundant in the References Paleozoic oceans (see Payne and van de Schootbrugge, Chapter 9; Knoll et al., Chapter Bekker, A., Holland, H.D., Wang, P.-L., Rumble III, D., Stein, H.J., Hannah, J.L., Coetzee, L., and Beukes, N.J. 8, this volume). (2004). Dating the rise of atmospheric oxygen. Nature Neither do the environmental influences 427: 117–120. of the algae stop with the carbon cycle (see Bhattacharya, D., and Medlin, L. (1998). Algal phyl- Guidry et al., Chapter 17, this volume). The ogeny and the origin of land plants. Plant Physiol. calcitic coccoliths precipitated by coccol- 116: 9–15. Blankenship, R.E. (1992). Origin and early evolution of ithoporids constitute a major sink for cal- photosynthesis. Photosyn. Res. 33: 91–111. cium carbonate, for the first time providing Blankenship, R.E. (2002). Molecular Mechanisms of Pho- a significant flux of carbonate to the deep tosynthesis. Oxford, Blackwell Science. seafloor (Litchman, Chapter 16, this volume). Blankenship, R.E., Sadekar, S., and Raymond, J. (2007). Diatoms, in turn, have come to dominate the The evolutionary transition from anoxygenic to oxy- genic photosynthesis. Evolution of Primary Produc- oceans’ silica cycle, influencing the evolution- ers in the Sea. P.G. Falkowski and A.H. Knoll, eds. ary trajectories of heterotrophs such as radi- Boston, Elsevier, pp. 21–35. olarians and siliceous sponges. The fluxes of Cavalier-Smith, T. (2002). Chloroplast evolution: sec- these “hard parts,” which probably evolved ondary symbiogenesis and multiple losses. Curr. as a protective mechanism against grazing Biol. 12(2): R62–R64. Delwiche, C.F. (2007). The origin and evolution of (see Hamm and Smetacek, Chapter 14; Finkel, dinoflagellates. Evolution of Primary Producers in the Chapter 15, this volume), were also accom- Sea. P.G. Falkowski and A.H. Knoll, eds. Boston, panied by the flux of organic matter into the Elsevier, pp. 191–205. ocean interior. The degradation and oxida- de Vargas, C., Aubry, M.-P., Probert, I., and Young, tion of this organic matter has “imprinted” J. (2007). Origin and evolution of coccolithophores: From coastal hunters to oceanic farmers. Evolution the ocean interior with a nitrogen–phosphate of Primary Producers in the Sea. P.G. Falkowski and ratio that is unique to that ecosystem and is an A.H. Knoll, eds. Boston, Elsevier, pp. 251–285. example of an “emergent” property of the co- Drake, M.J., and Righter, K. (2002). Determining the evolution of the chemistry of the sea and the composition of the Earth. Nature 416(6876): 39–44. organisms that live in it (Falkowski 2001). Falkowski, P.G. (2001). Biogeochemical cycles. Encyclo- pedia of Biodiversity 1: 437–453. Falkowski, P.G. (2006). Tracing oxygen’s imprint on IV. CONCLUDING COMMENTS Earth’s metabolic evolution. Science 311: 1724–1725. Falkowski, P.G., Katz, M., van Schootenbrugge, B., The study of the evolution of marine pho- Schofield, O., and Knoll, A.H. (2003). Why is the land green and the ocean red? Coccolithophores—From toautotrophs has a long and venerable history Molecular Processes to Global Impact. J. Young and but, perhaps surprisingly, has been largely over- H.R. Thierstein, eds. Berlin, Springer-Verlag. looked by both students and scholars of bio- Falkowksi, P.G., and Raven J.A. (2007). Aquatic Photo- logical oceanography. We hope that this book synthesis. Princeton, Princeton University Press. will give suchstudents access to a new under- Farquhar, J., Bao, H., and Thiemens, M. (2000). Atmos- pheric influence of Earth’s earliest sulfur cycle. standing of the organisms responsible for half Science 289(5480): 756–758. of the primary production on the planet. Our Fehling, J., Stoecker, D., and Baldauf, S.L. (2007). Pho- understanding of evolution of marine photo- tosynthesis and the eukaryote tree of life. Evolution autotrophs has been greatly enriched in recent of Primary Producers in the Sea. P. G. Falkowski and years as information in the fields of molecular A.H. Knoll, eds. Boston, Elsevier, pp. 75–107. Ferreira, K.N., Iverson, T.M., Maghlaoui, K., Barber, J., biology, algal physiology and biophysics, pale- and Iwata, S. (2004). Architecture of the photosyn- ontology, genomics, and Earth systems history thetic oxygen-evolving center. Science 303: 1831–1838. have been more integrated. The chapters in Finkel, Z.V. (2007). Does phytoplankton cell size this volume are an attempt at such an integra- matter? The evolution of modern marine food tion. It is our hope that the readers of this book webs. Evolution of Primary Producers in the Sea. P.G. Falkowski and A.H. Knoll, eds. Boston, Elsevier, will not only find the information useful but pp. 333–350. also, that students especially will be inspired to Green, B.R. (2007). Evolution of light-harvesting identify and address new questions. antennas in an oxygen world. Evolution of Primary Job Name: 203043t

6 1. AN INTRODUCTION TO PRIMARY PRODUCERS IN THE SEA

Producers in the Sea. P.G. Falkowski and A.H. Knoll, Primary Producers in the Sea. P.G. Falkowski and A.H. eds. Boston, Elsevier, pp. 37–53. Knoll, eds. Boston, Elsevier, pp. 351–375. Grzebyk, D., Schofield, O., Vetriani, C., and Falkowski, P.G. Martin, W. (2007). Eukaryote and mitochondrial ori- (2003). The Mesozoic radiation of eukaryotic algae: The gins: Two sides of the same coin and too much ado portable plastid hypothesis. J. Phycol. 39: 259–267. about oxygen. Evolution of Primary Producers in the Guidry, M.W., Arvidson, R.S., and Mackenzie, F.T. Sea. P.G. Falkowski and A.H. Knoll, eds. Boston, (2007). Biological and geochemical forcings to phan- Elsevier, pp. 55–73. erozoic change in seawater, atmosphere, and car- Mauzerall, D. (2007). Oceanic photochemistry and evo- bonate precipitate composition. Evolution of Primary lution of elements and cofactors in the early stages Producers in the Sea. P.G. Falkowski and A.H. Knoll, of the evolution of life. Evolution of Primary Producers eds. Boston, Elsevier, pp. 377–403. in the Sea. P.G. Falkowski and A.H. Knoll, eds. Hackett, J.D., Yoon, H.S., Butterfield, N.J., Sanderson, Boston, Elsevier, pp. 7–19. M.J., and Bhattacharya, D. (2007). Plastid endosym- O’Kelly, C.J. (2007). The origin and early evolution of biosis: Sources and timing of the major events. Evo- green plants. Evolution of Primary Producers in the Sea. lution of Primary Producers in the Sea. P.G. Falkowski P.G. Falkowski and A.H. Knoll, eds. Boston, Elsevier, and A.H. Knoll, eds. Boston, Elsevier, pp. 109–131. pp. 287–309. Hamm, C., and Smetacek, V. (2007). Armor: Why, Payne, J.L., and van de Schootbrugge, B. (2007). Life in when, and how. Evolution of Primary Producers in Triassic oceans: Links between planktonic and benthic the Sea. P. G. Falkowski and A. H. Knoll, eds. Boston, recovery and radiation. Evolution of Primary Producers Elsevier, pp. 311–332. in the Sea. P.G. Falkowski and A.H. Knoll, eds. Boston, Kasting, J.F. (1993). Earth’s early atmosphere. Science Elsevier, pp. 165–189. 259: 920–926. Quigg, A., Finkel, Z.V., Irwin, A.J., Rosenthal, Y., Ho, T.-Y., Katz, M.E., Fennel, K., and Falkowski, P.G. (2007). Reinfelder, J.R., Schofield, O., Morel, F., and Falkowski, Geochemical and biological consequences of phy- P.G. (2003). The evolutionary inheritance of elemental toplankton. Evolution of Primary Producers in the Sea. stoichiometry in marine phytoplankton. Nature 425: P.G. Falkowski and A.H. Knoll, eds. Boston, Elsevier, 291–294. pp. 405–429. Raymond, J., and Segre, D. (2006). The effect of oxygen Knoll, A.H., Summons, R.E., Waldbauer, J.R., and on biochemical networks and the evolution of com- Zumberge, J.E. (2007). The geological succession of plex life. Science 311: 1764–1767. primary producers in the oceans. Evolution of Pri- Robert, F. (2001). The origin of water on Earth. Science mary Producers in the Sea. P.G. Falkowski and A.H. 293: 1056–1058. Knoll, eds. Boston, Elsevier, pp. 133–163. Schlesinger, W.H. (1997). Biogeochemistry: An Analysis Kooistra, W., Gersonde, R., Medlin, L.K., and Mann, of Global Change. New York, Academic Press. D.G. (2007). The origin and evolution of diatoms: Watson, E.B., and Harrison, T.M. (2005). Zircon Their adaptation to a planktonic existence. Evolution thermometer reveals minimum melting conditions of Primary Producers in the Sea. P.G. Falkowski and on earliest Earth. Science 308: 841–844. A.H. Knoll, eds. Boston, Elsevier, pp. 207–249. Wolk, C.P., Ernst, A., and Elhai, J. (1994). Heterocyst Lindeman, R. (1942). The trophic-dynamic aspect of metabolism and development. The Molecular Biology ecology. Ecology 23: 399–418. of Cyanobacteria. E.D.E. Bryant, ed. Dordecht, Kluwer Litchman, E. (2007). Resource competition and the Academic Publishers: 769–823. ecological success of phytoplankton. Evolution of