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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.
II.
III.
IV.
What Is Primary Production?
How Is Photosynthesis Distributed in the Oceans?
What Is the Evolutionary History of Primary Production in the Oceans?
Concluding Comments
References
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 questions (Blankenship et al., Chapter 3, this
volume). Once it did evolve, however,
the genetic imprint spread via horizontal gene transfer and a series of symbiotic
associations to form a diverse photosynthetic biota that would prove resilient to
planetary catastrophes including global
glaciations, meteorite bombardments, and
massive volcanic eruptions while profoundly and irreversibly altering Earth’s
chemistry.
In this book, we examine both the molecular biological issue of how water came to
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 system. A second distinguishing feature is
the abundance of molecular oxygen in the
atmosphere. Based on the isotopic fractionation of sulfur, it would appear that oxygen
began to accumulate in the atmosphere and
surface ocean between 2.4 and 2.3 billion
years 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
1
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1. AN INTRODUCTION TO PRIMARY PRODUCERS IN THE SEA
be oxidized and the ecological and evolutionary 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 proteins, 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) reactions form the backbone of biological chemistry (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 inorganic carbon (i.e., CO2) to form organic matter (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 biopolymers. The ability to reduce inorganic carbon
to organic matter is restricted to a relatively
small subset of metabolic pathways. Some
bacteria and archaea exploit nonphotochemical reactions to reduce inorganic carbon, 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 photosynthetic, all photosynthetic organisms are primary 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 process 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 approximately 1 picosecond. The primary acceptor, 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 biochemical 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 alcohol (found in sugars and polysaccharides),
and ultimately to an alkane (C-H, found in
lipids). The donor is rereduced by an electron 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 complex energy transduction system in nature.
In all oxygenic photosynthetic organisms,
there are two photochemical reactions connected by a cytochrome. Molecular structural analyses clearly indicate that the two
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II. HOW IS PHOTOSYNTHESIS DISTRIBUTED IN THE OCEANS?
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 composed of two different polypeptides (i.e.,
heterodimers) embedded within and spanning a nonphospholipid bilayer membrane.
The amino acid sequences of the proteins
in the two reaction centers are very different, however. Both structural and amino
acid sequence homologies strongly suggest that one of the reaction center dimers,
designated photosystem II, is derived from
purple bacteria, a group of anaerobic photosynthetic 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 analogue elsewhere in nature. The second photosystem (photosystem I) is derived from
green sulfur bacteria and uses a set of iron
sulfur clusters as primary electron acceptors. 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) potentials, where ultimately the electron is used to
reduce ferridoxin. Although both photosystems (like their anoxygenic, bacterial counterparts) 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 photosystem 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).
3
II. HOW IS PHOTOSYNTHESIS
DISTRIBUTED IN THE OCEANS?
This question has two answers, one ecological 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 photosynthesis. 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 grazers (see Hamm and Smetacek, Chapter 14,
this volume), and in mid-gyre phytoplankton.
The group has attained far greater distribution, 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 hundreds 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 picoplankton. Secondary endosymbioses, involving
green algae as the autotrophic partner, have
resulted in three further groups of algae:
the chlorarachniophytes, the photosynthetic
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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 phytoplankton. 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 microbenthos and phytoplankton (see Kooistra et al.,
Chapter 11, this volume). Another ecologically
important group in the marine phytoplankton
is the haptophyte algae, especially the calciteprecipitating coccolithophorids (see de Vargas
et al., Chapter 12, this volume). Like photosynthetic heterokonts, haptophytes capable
of photosynthesis have red-algal–derived
plastids.
About half of known dinoflagellate species are photosynthetic, and most of these
also contain plastids derived from the red
algal line (see Delwiche, Chapter 10, this
volume). Dinoflagellates are photosynthetically promiscuous, however. In addition
to the red and green plastids already mentioned, they include species with plastids
derived from a tertiary endosymbiosis that
incorporated a haptophyte alga.
The phylogenetic diversity of marine photoautotrophs correlates with observed ecological heterogeneity of primary producers, with
green, red, and brown seaweeds along coasts
(and the remarkable floating brown alga
Sargassum proliferating far from shore); diatoms, dinoflagellates, and coccolithophorids
dominating shelf phytoplankton; and cyanobacterial and green picoplankton in oligotrophic mid-ocean environments.
What biological or environmental conditions 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 primarily 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 dinoflagellates, 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 secondary plastids were incorporated into host
cells once or multiple times, organisms possessing 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 geological record confirms that this is the case.
The present structure—both ecological and
phylogenetic—of autotrophy in marine
ecosystems originated only about 200 million years ago (Ma) (see Katz et al., Chapter
18, this volume). What governed the successive Mesozoic radiations of dinoflagellates,
coccolithophorids, and diatoms, and what
did earlier oceans look like? It appears that
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REFERENCES
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 coccolithoporids constitute a major sink for calcium 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 evolutionary trajectories of heterotrophs such as radiolarians 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 accompanied by the flux of organic matter into the
ocean interior. The degradation and oxidation 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 coevolution 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 photoautotrophs has a long and venerable history
but, perhaps surprisingly, has been largely overlooked by both students and scholars of biological oceanography. We hope that this book
will give suchstudents access to a new understanding of the organisms responsible for half
of the primary production on the planet. Our
understanding of evolution of marine photoautotrophs has been greatly enriched in recent
years as information in the fields of molecular
biology, algal physiology and biophysics, paleontology, genomics, and Earth systems history
have been more integrated. The chapters in
this volume are an attempt at such an integration. 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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