Photosynthesis Research 33: 91-111, 1992. © 1992 Kluwer Academic Publishers. Printedin the Netherlands. Minireview

Origin and early evolution of photosynthesis Robert E. Blankenship Department of Chemistry and Biochembtry, Center for the Study of Early Events in Photosynthesis, Arizona State University, Tempe A Z 85287-1604, USA Received 1 September 1991; accepted in revised form 12 March 1992

Key words: evolution, origin of life, reaction center, chlorophyll, bacteriochlorophyll, Chloroflexus aurantiacus, heliobacteria Abstract

Photosynthesis was well-established on the earth at least 3.5 thousand million years ago, and it is widely believed that these ancient organisms had similar metabolic capabilities to modern cyanobacteria. This requires that development of two photosystems and the oxygen evolution capability occurred very early in the earth's history, and that a presumed phase of evolution involving non-oxygen evolving photosynthetic organisms took place even earlier. The evolutionary relationships of the reaction center complexes found in all the classes of currently existing organisms have been analyzed using sequence analysis and biophysical measurements. The results indicate that all reaction centers fall into two basic groups, those with pheophytin and a pair of quinones as early acceptors, and those with iron sulfur clusters as early acceptors. No simple linear branching evolutionary scheme can account for the distribution patterns of reaction centers in existing photosynthetic organisms, and lateral transfer of genetic information is considered as a likely possibility. Possible scenarios for the development of primitive reaction centers into the heterodimeric protein structures found in existing reaction centers and for the development of organisms with two linked photosystems are presented.

Abbreviation: Gyr - gigayears

Introduction

Photosynthesis is the utilization of solar energy by plants, algae and certain bacteria for the synthesis of complex organic molecules (Staehelin and Arntzen 1986, Amesz 1987). For the energy of sunlight to be stored it must first be absorbed by the pigments of the organism. Several types of pigments, e.g., (bacterio)chlorophylls, carotenoids and bilin pigments serve this function in various photosynthetic organisms. A portion of the light energy absorbed by the photosynthetic pigments is eventually stored by forming chemical bonds. This conversion of energy from one form to another is a complex process that relies on cooperation between a

large number of pigment molecules and a group of electron transfer proteins. Collectively these are called a photosynthetic unit. Most of the pigments serve as an antenna, collecting light and transferring the energy to the reaction center, where the chemical reactions leading to long-term energy storage take place. The universal feature of all chlorophyll-based photosynthetic systems is an antenna system that collects light energy and transfers it to a reaction center complex where it is stored as redox energy. The only other group of photosynthetic organisms (in the literal sense) are the halobacteria, in which a retinal-containing protein known as bacteriorhodopsin directly pumps protons across a membrane upon light excitation

92 (Stoeckenius and Bogomolni 1982). These systems do not contain diversified antenna and reaction center structures, and do not carry out electron transfer reactions. It seems likely that there is no direct connection between these two types of photosynthesis, and that they therefore represent two independent evolutionary developments.

Geological constraints on dates of the origin and early development of photosynthesis Current thinking suggests that photosynthetic organisms may have been among the very earliest life forms on the primitive earth (Schopf 1983, Woese 1987, Olson and Pierson 1987a, Schidlowski 1988, de Duve 1991). Considerable evidence suggests that the earliest available evidence for life on Earth, fossil stromatolites dated to as far back as 3.5 thousand million years (Gyr) ago, are the remains of organisms that are morphologically similar to contemporary oxygenevolving cyanobacteria (Walter 1983, Awramik 1992). Isotopic evidence for autotrophic carbon fixation, likely photosynthetic in nature, extends even further back, to 3.8 Gyr ago (Schidlowski 1988). There is general agreement that the organisms that build the ancient stromatolites were photosynthetic. Whether they actually evolved oxygen is widely believed, but is not absolutely certain; a recent suggestion is that they may have been similar to the filamentous non-oxygen evolving green photosynthetic bacterium Chloroflexus aurantiacus (Oyzizu et al. 1987, Ward et al. 1989). The advent of oxygen-evolving photosynthesis permitted the development of advanced life, both by creating the ozone layer that shielded the earth from UV irradiation and also by providing a ubiquitous terminal oxidant for respiration. Geologic evidence clearly establishes that molecular oxygen began to accumulate in the atmosphere by approximately 2 Gyr ago, and it is virtually certain that this oxygen is of photosynthetic origin (Cloud 1973, Walker et al. 1983). Recent results have pushed this date back to 2.7 Gyr ago (Buick 1992). In addition, there are indications that oxygen was being produced as far back as 3.5 Gyr ago. The oxygen produced

by these early organisms may well have been consumed by chemical processes, possibly the oxidation of Fe 2+ to Fe 3÷, and so did not build up in the atmosphere until much later. This 'titration' of the reduced iron by oxygen has been proposed as a major source of the banded iron formations that date from this period, although other mechanisms have also been suggested (Cloud 1973, Walker et al. 1983, Schidlowski 1984, Hartman 1984, Braterman and CairnsSmith 1987, Mauzerall and Borowska 1988). The available evidence therefore places the appearance of photosynthetic life at least as far back as 3.5 Gyr ago, and possibly somewhat earlier. Oxygen evolution unquestionably began somewhat later than anoxygenic photosynthesis, and was clearly of dominant importance by about 2 Gyr ago and probably earlier. If the organisms that built the 3.5 Gyr old stromatolites were indeed oxygen-evolving forms, as is widely assumed, although not unambiguously established, then the major evolutionary developments that led from the more primitive forms of photosynthesis to the advanced forms capable of evolving oxygen had already taken place by this time. Contemporary cyanobacteria, the simplest oxygen-evolving photosynthetic organisms, have a mechanism of photosynthesis that is generally very similar to that found in higher plants (Bryant 1987). On a scale of complexity of photosynthesis, they are much closer to higher plants than they are to most of the other types of photosynthetic prokaryotes. Clearly, the majority of the critical evolutionary innovations that are characteristic of the most advanced forms of plant life had already occurred by the time the cyanobacteria appeared. Tracing the evolutionary development of photosynthesis is therefore likely to be a very difficult task, because the really important changes leading to the present groups of photosynthetic organisms occurred so long ago that all or most of the record of this development has been lost. One approach to reconstructing the past of this long ago lies in studies of comparative biochemistry and sequence analysis on existing organisms, both of which may yield some clues as to the nature of the evolutionary track that has been followed.

93

Mechanism of photosynthetic energy storage In all chlorophyss-based photosynthetic reaction centers the overall principles of the mechanism of energy storage appear to be the same, although the molecular details are quite varied. A chlorophyll in a specific protein environment in the reaction center is promoted to an excited singlet state, usually by excitation transfer from an antenna pigment. The excited singlet state is a very strong reductant, and transfers an electron to a nearby electron acceptor molecule. This is shown schematically in Fig. 1. The electron transfer reaction creates a radical ion-pair state, consisting of an oxidized chlorophyll and a reduced acceptor. This reaction is the step where light energy is transformed into chemical redox energy. The acceptor in most, if not all, cases also appears to be a chlorophyll or the related pigment pheophytin. A series of ultrafast electron transfer reactions follow the primary photochemical event and spatially separate the oxidized and reduced species. This prevents recombination, where the acceptor simply transfers the electron back to the donor, with the energy being dissipated to the environment as heat. The structure of the reaction center has apparently been fine-tuned by evolution to maximize the rates of the productive reactions and minimize the rates of the possible recombination reactions. Exactly hOW this is achieved is not yet well understood. The primary electron transfer step and the initial secondary reactions that stabilize the photochemical products all take place within the reaction center complex. However, for subsequent turnovers of the reaction center to take place, there must be some mechanism to remove electrons from the reduced acceptor and replace them to the oxidized donor. This can be accomplished by a cyclic process, in which the reduced acceptor transfers its electron through a series of carriers back to the oxidized donor. Energy conservation is achieved by coupling proton translocation across a membrane to the electron flow. Alternatively, non-cyclic electron flow can take place, in which one freely available substrate is oxidized and another is reduced. Both these modes of electron flow are found in contemporary photosynthetic organisms (Dutton 1986,

Electron Transfer in Photosynthesis Anoxygenic Cyclic

Anoxygenic Noncyclic

PA

PA

P*A

P*A

P+A-

P+A-

+hv

D+p

D~

D+P~/1A2

~'~A red

H+

Oxygen-Evolving Noncyclic

PA

PA

+hv

+hv

P*A

P*A

P+A-

P+A-

+

+

O÷PA1A; - ~ H+

D+PA1A; ~

NADP

Fig. 1. Schematic electron transfer pathways in photosynthetic organisms. The anoxygenic cyclic pathway is found in purple bacteria and in the filamentous green gliding bacteria. The anoxygenic non-cyclic pathway is found in the green sulfur bacteria. These organisms can also carry out cyclic electron flow, which is not shown. The oxygen-evolving non-cyclic pathway is found in cyanobacteria and chloroplasts. Cyclic electron flow around Photosystem I can also take place in these organisms. Abbreviations: P-reaction center photoactive pigment, e.g., P700; D - electron donor; A - e l e c t r o n acceptor; H + - hydrogen ions that are moved across a membrane, coupled to electron flow; h v - l i g h t absorption.

Brune 1989). Of particular note is the non-cyclic electron flow found in oxygen-evolving organisms, in which H20 serves as the oxidizable substrate and CO 2 is the ultimate electron acceptor, although the pyridine nucleotide NADP ÷ serves as an intermediate acceptor. All these modes of electron flow can lead to proton pumping and electrical potentials across the membrane, and the energy stored in these gradients (called the protonmotive force) can be used to make ATP.

94 In addition to the ATP formed by both cyclic and non-cyclic flow, reduced and oxidized substrates are accumulated during non-cyclic electron flow. The oxidized substrates are waste products and are excreted by the cell. The reduced compounds provide much of the energy necessary for carbon reduction. In those organisms that primarily carry out cyclic electron flow, the highly reducing compounds required for carbon reduction are not generated as direct products of light-driven electron transport. Instead, energy-dependent reverse electron flow from a weak reductant takes place. For example, in the purple photosynthetic bacteria, only cyclic electron flow is driven directly by light. The reduced sulfur compounds that primarily serve as substrates are oxidized and pyridine nucleotide (NAD ÷ in these organisms) are reduced by action of a N A D H dehydrogenase enzyme. This membrane protein uses the energy of ATP (or the protonmotive force directly) to drive the otherwise thermodynamically unfavorable reduction of NAD ÷ and concomitant oxidation of the sulfur compound (Dutton 1986, Brune 1989). Both cyclic and non-cyclic electron transport are carried out by many photosynthetic organisms, for example, the green sulfur bacteria among the anoxygenic prokaryotes. Cyclic electron flow can also occur in oxygen-evolving organisms, although the dominant mode is noncyclic.

Types of photosynthetic organisms A remarkable variety of both prokaryotic and eukaryotic photosynthetic organisms has been characterized. The photosynthetic process in all these organisms has many similarities, and it seems probable that all chlorophyll-based photosynthetic organisms are ultimately derived from a single photosynthetic ancestor. The anoxygenic photosynthetic organisms, all of which are prokaryotes, have traditionally been divided into families based on pigment content and metabolic capabilities (Pfennig and Trfiper 1983, Staley et al. 1989). Recently, another classification scheme has been introduced, based on sequence similarities in 16S ribosomal RNA, and has gained wide acceptance (Woese 1987). The

16S rRNA method has revolutionized bacterial taxonomy, and has led to the proposal that all forms of life can be divided into three kingdoms, the eukaryotes, the eubacteria and the archaebacteria. Of these, only the eubacteria contain chlorophyll-based photosynthesis. The 16S rRNA method actually measures the relationship of only a very limited part of the organism's genetic information, and whether or not the same evolutionary path has been followed for the development of photosynthesis as for the ribosome is not yet clear (see below). The 16S rRNA method yields groupings, or, phyla, that are generally similar to the traditional groupings of photosynthetic bacteria, with some important differences. Of the ten known phyla that comprise the eubacteria, five contain photosynthetic representatives, and in most of those phyla both photosynthetic and non-photosynthetic forms are found (Fig. 2). Woese (1987) suggests that the photosynthetic capability was present in the ancestor of all or most of the lineages, and some groups subsequently lost the ability to do photosynthesis. The five phyla of eubacteria that contain photosynthetic representatives are the purple bacteria, including both the sulfur and non-sulfur families of the traditional grouping, the green sulfur bacteria, the filamentous green gliding bacteria (sometimes called the green non-sulfur bacteria), the gram positive bacteria, and the cyanobacteria. The cyanobacterial phylum includes chloroplasts from eukaryotic organisms, which were almost certainly derived from prokaryotes by endosymbiosis (Margulis 1981, Gray 1989).

Functional and structural relationships among photosynthetic reaction centers The classification methods described above are only relevant to an understanding of photosynthesis if they serve to distinguish structural or functional aspects of the process in the various groups. In some respects, there is a good correlation between the known structural and functional aspects of photosynthesis and the 16S rRNA classification system. The present discussion is largely limited to the reaction center, although

95

16 S rRNA Evolutionary Tree of Photosynthetic Organisms Green Sulfur Bacteria ~ Green Gliding Bacteria

Pheophytin-Quinone RC

~ ~~

/

Fe-S RC ~ ; ~ _ H elio bacte ria

yanobacter,a

qlll~

Purple

Bacteria

Fig. 2. Evolutionary tree of eubacteria, based on 16S rRNA analysis. The crosshatching indicates the class of reaction center found in the photosynthetic representatives. The branch lengths are not to scale. This diagram is an adaptation of one presented by Woese (1987).

antenna complexes and other proteins involved in photosynthesis should be included for a more complete picture. Organisms in the same phylum invariably have reaction centers that are more similar to each other than they are to those of organisms from another phylum. In the case of the purple bacteria, there are now a number of sequences of reaction center and antenna proteins, nicely confirming the evolutionary relatedness within the group that is predicted from both the traditional and the newer classification systems. There are, however, functional and structural similarities and differences among the various types of reaction centers that are not revealed by 16S rRNA analysis, possibly because the relatedness is quite ancestral and beyond the resolution of the method. In particular, the purple bacteria have a reaction center that is similar in many ways to that found in Chloroflexus aurantiacus (Bruce et al. 1982, Pierson and Thornber 1983, Blankenship 1985, Shiozawa et al. 1987, Kirmaier and Holten 1987, Ovchinnikov et al. 1988a,b, Shiozawa et al. 1989). Both of these reaction centers are similar, in turn, to the Photosystem II reaction center of oxygenic organisms (Barber 1987, Nanba and Satoh 1987, Michel and Deisenhofer 1988, Komiya et al.

1988, Rutherford 1988). These reaction centers all contain (bacterio)pheophytin as an intermediate electron acceptor and two quinones in association with a metal ion (in most cases iron) (Staehelin and Arntzen 1986, Amesz 1987). The spectroscopic, kinetic and magnetic resonance properties and the protein composition of all these 'pheophytin-quinone type' reaction centers bear striking similarities to each other, and there is little doubt that they share a common ancestor. This point is discussed in more detail below. There is also some evidence suggesting that a similar evolutionary relationship exists among the reaction centers of the green sulfur bacteria, Photosystem I and the heliobacterium group (Olson et al. 1976, Prince et al. 1985, Nitschke et al. 1987, Trost and Blankenship 1989, Mathis 1990, Van de Meent et al. 1990, Nitschke et al. 1990a, Nitschke et al. 1990b, Golbeck and Bryant 1991). All these reaction centers contain membrane-bound iron-sulfur centers as early electron acceptors, and are therefore called 'FeS type' reaction centers. Figure 3 shows electron transport diagrams of the 'pheophytin-quinone type' reaction centers of the purple bacteria, Chloroflexus aurantiacus, and Photosystem II on the left, and the 'Fe-S type' reaction centers of

96

Fe-S Type Reaction Center

Pheophytin-Quinone Type Reaction Center P

Purple Bacteria and C h l o r o f l e x u s aurantiacus -1.5

PS II

-

PS I

(Oxygen

Evolving

Green Sulfur Bacteria and Heliobacteria

Organisms) P700 \ A o [Chll

-1.0

FSSO

BChl \ BPh

\

A 0 ~[Chl ?1

~A1 [Ol \ F.~ X

P87o

-

P84o Psoo )

\

A1 [Q] F~e~X Fe'SA/B Fd Fd \

-0.5 hv

QA h'J

J cyt bcl Fe'SRJ /

cyt

NAD

FNR NADP

QA

QB /

0.0

X{

h~

\

E

UJ

\?

F e ~ A/B

Ph

QB

\

I o,~, FesR I

,I °y' oo,

\ PC (cyt c)

/ c2 (AC)

F°S"l

cyI o

~P700

87O

0.5--

OEC

1.0--

~Z~F

Fig. 3. Electron transport diagrams for photosynthetic reaction centers. Heavy vertical arrows indicate energy input by photon absorption, thinner arrows indicate preferred electron transfer pathways. Carriers in parentheses indicate alternate species in some organisms. Question marks indicate carriers or electron transfer steps that are likely but have not been unambiguously established. The cytochrome bc~ and b6f complexes are boxed, and the details of the electron flow in these complexes are omitted. Abbreviations: AC - auracyanin; BChl - bacteriochlorophyll; BPh - bacteriopheophytin; Chl - chlorophyll; cyt - cytochrome; F d - s o l u b l e ferredoxin; Fe-SA/B -iron-sulfur centers contained on a low molecular weight peptide peripheral to the reaction center core; Fe-S R - Rieske iron-sulfur center; Fe-S x - i r o n - s u l f u r center contained in the reaction center core; FNR - ferredoxin-NADP reductase; hu - photon; NAD(P) - nicotinamide adenine dinucleotide (phosphate); O E C - oxygen evolving center; P870, P680, PToo, P840, Psoo- reaction center photoactive pigment with absorption maximum in nanometers at the indicated wavelength; PC-plastocyanin; Ph-pheophytin; Q - q u i n o n e (subscript indicates a specific quinone); Z - t y r o s i n e radical donor to Photosystem II.

green sulfur bacteria, heliobacteria and Photosystem I on the right. Perhaps the single most important development in the field of photosynthesis in the last quarter century has been the X-ray structural studies on bacterial reaction centers (Deisenhofer et al. 1985, Budil et al. 1987, Deisenhofer and Michel 1989, Rees et al. 1989). The organisms whose reaction center structures have been determined so far are the purple bacteria Rhodopseudornonas viridis and Rhodobacter sphaeroides. These organisms are quite closely related (see below), so it is difficult to ascertain at the present time if the many common structural features of these reaction centers are required by their similar functions or are simply reflecting

their common heritage. In order to determine what are the 'essential' features of photosynthetic reaction centers, much more information, ultimately including structures, is needed on reaction centers that are much more distantly related. Structural features that are conserved over a wide evolutionary distance are likely to be essential to function. One intriguing aspect of all photosynthetic reaction centers where the information is available is that two related yet distinct proteins make up the core of the complex. Additional proteins are also present in most cases. This structural motif consisting of a heterodimeric protein core is found in the L and M subunits of the purple bacteria, the D1 and D2 proteins of the Photo-

97 system II reaction center and in the Photosystem I reaction center psaA and psaB gene products (Barber 1987, Nanba and Satoh 1987, Michel and Deisenhofer 1988, Komiya et al. 1988, Rutherford 1988, Golbeck and Bryant 1991). In each case the two halves of the heterodimeric protein complex exhibit substantial overall sequence similarity, e.g., 45% identity for the Photosystem I case, with much higher identity in certain regions. The heterodimeric nature of the reaction center almost certainly arose by gene duplication and subsequent divergence of the two genes. This point is discussed in more detail below. To summarize, comparative studies of functional aspects of existing photosynthetic reaction centers lump them into two broad groups based on the nature of the early electron acceptors. Each group contains some anoxygenic bacterial reaction centers and one of the two types of reaction centers found in oxygen-evolving organisms. In all cases where definitive information is available, the core of the reaction center consists of a heterodimeric protein complex, with two distinct, yet related proteins.

Sequence analysis of pheophytin-quinone reaction centers The reaction center sequences of a number of the pheophytin-quinone reaction centers have now been determined, and the results are at the same time satisfying and provocative. The residual identity of the purple bacterial reaction center peptides L and M to the D1 and D2 peptides that make up the Photosystem II reaction center is very small, approximately 10 percent (Michel and Deisenhofer 1988, Komiya et al. 1988). However, many of the conserved residues of the purple bacteria are found in the D1 and D2 peptides, and hydropathy analysis indicates that D1 and D2 have five transmembrane helices similar to that found in the L and M peptides of purple bacteria (Rochaix et al. 1984, Trebst 1986). The striking similarities between the bacterial and Photosystem II reaction centers have led most workers to accept the proposal that there is an evolutionary relatedness between the bacteri-

al L and M peptides and the D1 and D2 peptides of Photosystem II. The assumption has often been that the D1 protein is descended from the L peptide and the D2 protein is descended from the M peptide. This identification cannot be based on the small residual sequence similarity between the Photosystem II proteins and the bacterial proteins, but is instead derived largely from the fact that the second quinone acceptor QB is associated with D1 and L, and the primary quinone acceptor QA is associated with D2 and M. In fact, careful analysis of the reaction center sequences does not support the widely accepted L into D1 and M into D2 scenario. This discrepancy was first pointed out by Williams et al. (1986), and we have confirmed and extended their analysis. Figure 4 shows a phylogenetic tree based on reaction center sequence analysis using protein parsimony methods (Felsenstein 1988a). Recently, Beanland (1990) has used similar methods and arrived at essentially the same conclusions. Very similar trees are produced using distance methods or if only the central portions of the reaction center sequences are considered (M. Whitehead and R.E. Blankenship, unpublished). Included in the analysis are four purple bacteria (Williams et al. 1983, 1986, Youvan et al. 1984, Michel et al. 1986, Bdlanger et al. 1988), Chloroflexus aurantiacus (Ovchinnikov et al. 1988a,b, Shiozawa et al. 1989), a cyanobacterium (Williams and Chisholm 1987, Ravnikar et al. 1989) and a higher plant (Zurawski et al. 1982, Holschuh et al. 1984). Several striking features emerge from this analysis. First, the purple bacteria are tightly grouped, as predicted by any classification scheme. Similarly, the cyanobacteria and higher plant reaction centers are very similar to each other, also as expected. However, the sequence comparisons clearly indicate that D1 is much more similar to D2 than it is to L. This would seem to require that two gene duplications occurred, one leading to the L / M line and the other leading to the D1/D2 line. Whether or not this is actually the evolutionary path that has been followed is not absolutely certain, but does appear to be likely. Different rates of evolutionary change in different branches of a tree can sometimes lead to incorrect topologies (Felsenstein 1978, Lake 1991). How-

98

Photosynthetic Reaction Center Evolutionary Tree RCAPM RSPHM

SYNCYSD1

SPIND2

SPIND1

SYNCYSD2

R~RM

RRUBM

CAURM

RCAPL

RRUBL

RSPHL

RVIRL

Gene Duplication

---~

-.,,-- Gene Duplication

line

D1/D2 Line

ANCEST

Fig. 4. Evolutionary tree of pheophytin quinone reaction centers, based on parsimony analysis of reaction center protein sequences. The tree was generated using the Protparse program of the Phylip package (Felsenstein 1988a). Branch lengths are approximately proportional to number of changes in the sequences. The alignment is approximately that of Michel and Deisenhofer (1988). Presumed gene duplication events that gave rise to distinct L and M and D1 and D2 proteins are indicated. Abbreviations: Names ending in L, M, are the bacterial L and M reaction center proteins; names ending in D1 or D2 are the Photosystem II reaction center core proteins (psbA and psbD gene products, respectively); syncys-Synechocystis 6803 (Ravnikar et al. 1989, Williams and Chisholm 1987); spin-Spinacia oleracea (Zurawski et al. 1982, Holschuh et al. 1984); caur - Chloroflexus aurantiacus (Ovchinnikov et al. 1988a,b, Shiozawa et al. 1989); rvir - Rhodopseudomonas viridis (Michel et al. 1986); rrub-Rhodospirillum rubrum (B61anger et al. 1988); r c a p - Rhodobacter capsulatus (Youvan et al. 1984); r s p h Rhodobacter sphaeroides (Williams et al. 1983, 1986).

ever, different methods of tree generation, with different sensitivities to varying rates of evolutionary change all produce essentially identical trees, so it seems reasonable to interpret the tree at face value. Another striking feature of the tree shown in Fig. 4 is that Chloroflexus aurantiacus is clearly out of place, compared to where the 16S rRNA analysis would have placed it (compare Figs. 2 and 4). The 16S rRNA data very clearly indicate

that Chloroftexus branched away from the rest of the eubacteria prior to the divergence of the purple bacteria from the cyanobacteria and chloroplasts (Woese 1987). The reaction center sequence data just as clearly place it much closer to the purple bacteria than to Photosystem II. This discrepancy is well outside the statistical errors associated with either method (Felsenstein 1988b, Sneath 1989, Beanland 1990). The protein sequence data confirm what

99 kinetic and spectral measurements suggested several years ago, namely that the Chloroflexus reaction center is in essence closest to the purple bacterial reaction centers, but is less similar to any purple bacterial reaction center than all the purples are to each other (Bruce et al. 1982, Pierson and Thornber 1983, Blankenship 1985, Shiozawa et al. 1987, Kirmaier and Holten 1987, Ovchinnikov 1988a,b, Shiozawa et al. 1989). Although the data sets are much less complete, there is also clear evidence for a reasonably close evolutionary relatedness between the purple bacteria and Chloroflexus when the membranebound bacteriochlorophyll a-containing antenna complexes (Wechsler et al. 1985, 1987) and the membrane-bound cytochrome that donates electrons to the oxidized reaction center (Dracheva et al. 1991) are examined. The significance of this disagreement between the evolutionary trees generated from 16S rRNA and the reaction center sequences is yet unclear. The simplest explanation is that a lateral gene transfer event may have moved the genes necessary for photosynthesis into (or out of) an ancestor of Chloroflexus. The necessary genes include the reaction center structural genes, the genes that code for the other electron transfer proteins and the genes needed for biosynthesis of pigments and other cofactors. These genes are clustered together in purple photosynthetic bacteria into a single 46 kilobase gene cluster (Young et al. 1989, Wellington et al. 1991).

The special position of Chloroflexus aurantiacus The filamentous green gliding bacterium Chloroflexus aurantiacus (Pierson and Castenholz 1974a,b) exhibits a unique set of properties suggesting that it may indeed be some sort of chimeric organism. According to 16S rRNA analysis, it is the earliest branching organism within the eubacteria that exhibits the photosynthetic phenotype (Woese 1987). In addition to the reaction center traits discussed earlier, this organism has many decidedly unusual features, including a novel pathway of carbon fixation (neither the Calvin cycle nor the reverse TCA cycle) (Holo and Sirevhg 1986), an unusual lipid

and carotenoid composition (Knudsen et al. 1982), an apparent lack of soluble c-type cytochromes (Bartsch 1978, Freeman and Blankenship 1990) (the blue copper protein known as auracyanin (Trost et al. 1988, McManus et al. 1992) probably fulfills their functional role), novel amino acid biosynthetic pathways (Klemme 1989) and finally a cell wall structure that is very atypical for a Gram negative organism (Jurgens et al. 1987). In overall cell morphology, carotenoid composition and mat-forming behavior, it is similar to certain types of cyanobacteria (Pierson and Castenholz 1974a,b). chlorosome light harvesting antenna system in Chloroflexus (Olson 1980, Zuber 1987, Blankenship et al. 1988). A similar antenna complex is found in the green sulfur bacteria, which are not closely related organisms according to 16S rRNA analysis (Gibson et al. 1985) (see Fig. 2). However, sequence comparisons of some of the proteins found in the chlorosomes from the two types of bacteria clearly indicate an evolutionary relatedness (Wagner-Huber et al. 1988). In addition, biochemical, biophysical and ultrastructural studies all support the idea that the chlorosomes from the two types of green bacteria are very similar structures (Olson 1980, Zuber 1987, Blankenship et al. 1988). However, the reaction centers, and membrane-bound antenna complexes found in these organisms are entirely different. Chloroflexus contains a pheophytin-quinone type of reaction center, and the green sulfur bacteria contain a Fe-S type of reaction center. Thus, the more peripheral antenna complexes of these organisms are clearly quite closely related, while all the components that are integral to the membrane are very different. In the case of Chloroflexus, the membrane-bound components are most closely related to those of the purple bacteria. Woese (1987) makes a strong case for the likelihood that the progenitor of all eubacteria was photosynthetic, based largely on the observed fact that five of the ten eubacterial phyla contain photosynthetic representatives, in particular the very deeply branching phylum that contains Chloroflexus. However, because of the discrepancy between the 16S rRNA evolutionary tree and the tree predicted by the sequences of the pheophytin-quinone type of reaction center,

100 this assertion is weakened. As discussed above, there is reason to suspect that Chloroflexus may have been the recipient of photosynthetic capabilities via lateral gene transfer. Alternatively, it could have been the donor, which would preserve the photosynthetic phenotype as a likely primitive characteristic. Considerably more information about all the complexes that make up the photosynthetic apparatus and their genomic organization is needed before any firm conclusions can be drawn on this point. There is no simple evolutionary scheme that can account for these patterns of reaction center and antenna complex distribution. Complex schemes can be invented to explain the results, including lateral gene transfer of either the reaction center or antenna genes, or selective loss of one or another complex from a putative ancient organism that contained precursors of all the structures now found only in distinct groups. Some of these ideas are discussed below.

Evolution of Photosynthetic Reaction Centers

Monomeric Reaction Center

Evolutionary Change

::~~:i:i::-i~ " -:::::! Homodimeric

(

~f

ene Duplication

Divergence

~~

A scenario for the early evolution of photosynthetic reaction centers

H:taert°;~ m e ri c

[ ~ ~ . )

One of the most striking aspects of the structure of photosynthetic reaction centers is the protein composition. In all cases where definitive information is available, the core of the reaction center is found to be composed of two related, yet distinct proteins. By far the simplest explanation for this situation is that a gene duplication took place at some point in the early evolution of the reaction center, and subsequent divergence of the genes led to the heterodimeric complex found in modern reaction centers. This requires that a single gene reaction center existed at some time, which has since been replaced by the two gene reaction center. A possible scenario for the gradual conversion of a monomeric reaction center complex into a heterodimeric complex is shown in Fig. 5. The original reaction center was a protein monomer, which, over time, developed the ability to dimerize, thereby producing a homodimeric complex. The gene duplication and subsequent divergence permitted the development of a heterodimeric complex. What is the selection pressure that forced the change from a monomeric to a hetero-

!

Center

Fig. 5. Scheme for evolutionary development of photosynthetic reaction centers. Outline figures represent protein subunits in the reaction center core. Arrows within the figures are the electron transfer pathways. Arrows with x's through them are potential pathways that are not kinetically important. Different crosshatching patterns are indicative of distinguishable proteins. Details are given in text.

dimeric reaction center? A critical aspect of the structure of the reaction center from the purple bacteria is the closely coupled dimer of bacteriochlorophylls that make up the primary electron donor of the complex. This pigment dimer presumably was lacking in a reaction center consisting of only one protein subunit. While the nature of the primary electron transfer processes in reaction centers is still not understood at a deep level, one likely result is that a pigment dimer is required for the system to operate at high efficiency. So the monomeric (both pigment and protein) reaction center may have worked, but not very well. This could be remedied by forming a homodimeric complex (which still requires

101 only one gene). This may have improved the efficiency by producing the pigment dimer. The subsequent gene duplication and divergence was a fine tuning mechanism that further improved the efficiency. Interestingly, the second electron transfer pathway in the heterodimeric reaction center found in purple bacteria is clearly inactive in carrying out electron transfer. This second pathway may possibly be a 'molecular appendix', serving no functional role, but preserved possibly for structural reasons. There must be a considerable functional advantage to the heterodimeric motif of reaction center structure, as it is quite clear that at least three (and likely more) independent gene duplications took place in various classes of reaction centers. The evidence suggesting that the gene duplication event that gave rise to the L and M subunits in purple bacteria was distinct from the one that gave rise to the D1 and D2 subunits of Photosystem II was discussed above. Similarly, the two halves of the heterodimeric reaction center of Photosystem I are much more closely related to each other than either is to any other known reaction center complex. There is not yet available any definitive information concerning the protein structure of the reaction centers from two important classes of organisms, the green sulfur bacteria and the heliobacteria. It is clear from functional studies that both these reaction centers are generally similar to each other and to Photosystem I (Olson et al. 1976, Prince et al. 1985, Nitschke et al. 1987, Trost and Blankenship 1989, Mathis 1990, Nitschke et al. 1990a,b, Van de Meent et al. 1990, Golbeck and Bryant 1991). Recently, a region of the heliobacterial reaction center was sequenced chemically and found to be quite similar to a very highly conserved region found in both the Photosystem I reaction center proteins (Blankenship et al. 1991, Trost et al. 1992). The similarity of the Photosystem I proteins to each other in this region is higher than either is to the heliobacterial sequence, supporting the idea advanced above that the gene duplication that led to the heterodimeric reaction center motif in Photosystem I occurred after the divergence of the heliobacteria from organisms containing Photosystem I. It is not yet possible to determine whether the heliobacterial reaction

center also contains a heterodimeric protein complex.

Origin of the linked reaction centers in oxygenevolving organisms

As discussed above, all photosynthetic reaction centers can be placed in two groups, those with pheophytin and quinone as electron acceptors and those with Fe-S centers as electron acceptors. It seems likely that a primordial reaction center existed, which subsequently diverged into the ancestors (probably still monomeric) of the two classes of contemporary reaction centers. This is diagrammed in Fig. 6. These primitive, but distinguishable reaction centers then developed into the bacterial and plant-type reaction centers through the mechanism described above, passing through a homodimeric intermediate to the heterodimeric complexes found today. No anoxygenic organisms have been found that contain both classes of reaction centers. Some types of cyanobacteria can utilize sulfide as an electron donor in place of water (Cohen et al. 1975, Padan 1979, Cohen 1989). However, it seems likely that this metabolic capability is a later adaptation to a particular environment, rather than reflecting a transitional organism, as these organisms are fully capable of oxygen evolution under the proper conditions. More information about the nature of the sulfide oxidation system in these organisms would be very interesting (Arieli et al. 1991). The simplest scenario giving rise to the linked photosystems found in oxygen-evolving organisms is that some sort of genetic fusion event took place between two bacteria, one with a pheophytin-quinone reaction center and the other with an Fe-S reaction center. This produced a chimeric organism with two unlinked photosystems. Subsequently, the two photosystems were linked, and the oxygen evolving system added. There are no clear indications of any intermediate stages in the development of the oxygen evolving system, nor is there any hint of the evolutionary source of this complex or what

102

Evolution of Photosynthetic Reaction Centers

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Fig. 6. Scenario for evolution of photosynthetic reaction centers. Outline figures indicate protein subunits. Single figures indicate monomeric reaction centers, while double figures indicate heterodimeric reaction centers. The homodimeric stage is omitted for simplicity. The arrows indicate the putative genetic fusion that gave rise to organisms with two distinct reaction centers. The lowest level indicates the organisms that are found today, while the upper levels indicate precursor organisms that existed in the past.

might have been the function of such a precursor. The bacterial sulfur oxidizing pathways, which formally are analogous to the water oxidizing capability of oxygen-evolving organisms, are carried out by soluble enzymes with cofactors entirely different from those known to be involved in the water oxidizing process (Brune 1989). It therefore seems likely that the sulfur oxidation system is not directly related to the water oxidizing system. The oxygen evolving complex contains four Mn atoms intimately associated with the Photosystem II reaction center (Babcock 1987). Olson (1970) has suggested that

the oxygen evolving capability arose by an enzyme system gradually evolving the ability to oxidize increasingly weak reductants, possibly a series of nitrogen compounds. No contemporary photosynthetic organisms have been found with the capability to oxidize these compounds, however. Another possibility that has been suggested as a reductant that is weaker than sulfur compounds but stronger than water is F e z+ ion (Olson and Pierson 1987a). Some types of cyanobacteria can oxidize Fe 2+ to Fe 3+ using Photosystem I or possibly Photosystem II, so this seems possible (Cohen 1984).

103

Evolutionary clues from pigment types and biosynthetic pathways Many other possible scenarios for the evolutionary origin and development of photosynthesis have been proposed by other workers in the field. One of the most interesting of these is the view, emphasized by Mauzerall (Mercer-Smith and Mauzerall 1984, Mercer-Smith et al. 1985, Mauzerall 1990) and Pierson and Olson (Olson and Pierson 1987a,b, Pierson and Olson 1989), that the pigment types found in contemporary photosynthetic organisms are a direct indication of what has been the evolutionary sequence that gave rise to them. This argument is based largely on the 'Granick Hypothesis', which states in essence that 'biosynthesis recapitulates phylogeny' (Granick 1965). The intermediates in the biosynthetic pathway of a complex molecule like chlorophyll are thought to be the final products of biosynthetic pathways of earlier evolutionary forms. The later developments improved efficiency of the system, and were gradually finetuned to give rise to the molecules found in present-day photosynthetic organisms. This view is compelling in many ways and may likely be at least partially true. It is contrasted with the opposite view that biosynthetic pathways are built backwards (Gest and Schopf 1983). As existing stocks of essential molecules are depleted, the organism discovers ways to build the critical components from ever simpler building blocks. Although it seems self contradictory at first, both these concepts may be at least partially valid. It is inconceivable that an extremely complex molecule like chlorophyll with multiple chiral centers could be formed by strictly non-biological means. On the other hand, the simplest-precursors of the chlorophylls are amino acids and other colorless compounds, which could not themselves possibly serve as photopigments. Mauzerall (Mercer-Smith and Mauzerall 1984, Mercer-Smith et al. 1985, Mauzerall 1990) has described plausible abiotic mechanisms for synthesis of simple porphyrins, which could then be elaborated by subsequent biochemical steps in accordance with the Granick hypothesis. The pathway is therefore best described as evolving from the middle out to both simpler and more complex molecules.

The generally accepted biosynthetic pathway of the porphyrins and chlorophylls (Granick 1965, Beale and Weinstein 1990) (Fig. 7) begins with either glutamate or succinate and glycine, proceeds through 5-aminolevulinic acid to simple porphyrins such as protoporphyrin IX, and is completed by closure of ring V and the reductions of ring IV and ring II. The last of these steps is found only in bacteriochlorophyll a. The fact that chlorophyll precedes bacteriochlorophylls in the biosynthetic pathway suggests via the Granick hypothesis that chlorophyll existed in nature before the additional steps needed to make bacteriochlorophyll were evolved. One problem with this view is that in all known cases chlorophyll is found only in the advanced oxygen-evolving organisms with two photosystems and never in the simpler organisms with only one photosystem. All bacteriochlorophyll a-containing organisms are anoxygenic, containing either a pheophytin-quinone type of reaction center (purple bacteria and filamentous green gliding bacteria) or an Fe-S type of reaction center (green sulfur bacteria). A few purple bacteria contain bacteriochlorophyll b instead of bacteriochlorophyll a. Thus, bacteriochlorophyll a (or b) is found in both the major classes of reaction centers. The finding of bacteriochlorophyll in distantly related organisms with very different types of reaction centers suggests that it may be a primitive characteristic. In addition, there are cases where biosynthetic intermediates of chlorophylls or bilin pigments have apparently later been utilized for a different function, in apparent violation of the Granick hypothesis (Brown 1985, Beale and Cornejo 1991). The newly discovered heliobacteria (Gest and Favinger 1983, Madigan 1992) may be important to an understanding of this question. They contain the previously unknown pigment bacteriochlorophyll g, which has chemical properties of both chlorophyll a and bacteriochlorophyll b and thus represents a possible intermediate form (Brockmann and Lipinski 1983, Michalski et al. 1987). Unfortunately, almost nothing is yet known about its biosynthetic pathway. One possible scenario is that bacteriochlorophyll g, or a related molecule, may have been the pigment in the early reaction centers. The present-day biosynthetic pathways of chlorophylls and other

104 Protoheme

Other Hemes

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Bacteriochlorophylls c, d, e

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Fig. 7. Biosyntheticpathwaysof chlorophylls and related pigments. This diagram is taken from Beale and Weinstein (1990), and

is reproduced with permission. Abbreviation: ALA- 5-aminolevulinic acid. bacteriochlorophylls may have been optimized during their early evolution to improve synthetic efficiency, and thus may not strictly reflect the evolutionary history of the organisms. Thus, while the Granick hypothesis may be correct in broad outline, it may not be correct in every detail. Finally, the details of later steps in the biosynthetic pathways for the bacterial pigments are not unambiguously established (Beale and Weinstein 1990). In many cases, there is no clear experimental evidence on important steps in the pathway, and the pathways are inferred. One interesting approach to this question that has not yet been possible to carry out is the use of sequence comparisons of the pigment biosynthetic enzymes. As more of the details of the pathways and enzymes become available, a much clearer picture of the relationship of pigment biosynthetic pathways to evolutionary development of photosynthesis will undoubtedly emerge. Recent gene sequences of proteins involved in bacteriochlorophyll synthesis in purple bacteria are an important first step in this analysis (Burke et al. 1991).

Olson and Pierson (1987a,b) and Pierson and Olson (1989) have suggested that a chlorophyllcontaining organism with both types of photosystems, but without oxygen evolution capacity is the ancestor of all contemporary photosynthetic organisms, with the possible exception of the heliobacteria (Fig. 8). This organism then developed the capability to synthesize bacteriochlorophyll, possibly as an adaptation to environments with severe light screening by other chlorophyll-containing organisms. Selective loss of one or the other photosystems led to the existing anoxygenic bacteria. The putative chlorophyll-containing organism with both types of reaction centers then developed the water oxidation system and became the cyanobacteria and eventually, via e_ndosymbiosis, the chloroplast. The Olson-Pierson scenario postulates at least three classes of organisms for which no existing examples are found. These are the anoxygenic chlorophyll-containing form with only an Fe-S type reaction center, the anoxygenic chlorophyllcontaining form with both types of reaction centers, and the bacteriochlorophyll-containing form

105

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Fig. 8. Evolutionary scenario for photosynthetic reaction centers, as proposed by Pierson and Olson (1989). Reproduced with permission.

with both types of reaction centers. It retains the attractive aspects of the Granick hypothesis, but at the expense of simplicity. The scenario described in Fig. 6 avoids most of these putative organisms, but introduces the additional complication of a postulated genetic fusion, for which no direct evidence exists. It does not incorporate any information relating to pigment compositions or biosynthetic pathways. Clearly, there is insufficient evidence currently available to choose between these alternatives. The two scenarios make quite different predictions concerning many aspects of the contemporary organisms that makes them distinguishable. The fusion hypothesis predicts that remnants of other parts of the two different organisms that fused may be found. For example, the cytochrome bc 1 complex (Gabellini 1988, Trumpower 1990) (known as b 6 f in oxygenic organisms) in the organism resulting from the fusion may have come from just one of the precursor organisms, and may therefore be much closer to the cytochrome bc 1 complex of one of the major lines than the other. The Olson-Pierson scheme predicts that the analogous cytochrome bc 1 complexes in the major lines of anoxygenic phototrophs will be approximately equally distant from

the cytochrome b 6 f complex in the oxygenic forms. Unfortunately, very little of the needed information to make these critical comparisons is yet available. Photosynthesis is a complex process that in many organisms shares electron transport complexes with other metabolic pathways such as respiration. It is plausible that there may have been considerable exchange of the genetic 'modules' that code for these systems. In present day organisms these are often organized into operons such as the p u f operon that codes for the core antenna proteins and the L and M reaction center peptides in the purple bacteria (Young et al. 1989, Wellington et al. 1991). Another example is the pet operon that codes for the cytochrome bc 1 complex (Gabellini 1988, Trumpower 1990). Our understanding of the larger scale organization of the genomes in photosynthetic bacteria is still very limited, and genetic information about critical organisms such as Chloroflexus or the heliobacteria is still almost nonexistent. The nature of the primordial reaction center

What was the nature of the primordial reaction

106 center? Was it more similar to the pheophytinquinone reaction centers or the Fe-S reaction centers? What pigments did it contain? Did it carry out cyclic or non-cyclic electron transport? Definitive answers to these questions are certainly not yet available, although some plausible speculations are possible. Many other authors have considered this question; the interested reader is referred to the recent discussions by van Gorkom (1987), Olson and Pierson (1987a,b), Pierson and Olson (1989), Mathis (1990), Nitschke and Rutherford (1991). One deep similarity between the pheophytinquinone reaction centers and the Fe-S reaction centers is the presence of a quinone as an early electron acceptor, preceded by a chlorophylltype pigment. While the details of the thermodynamic properties of the quinones and the identity of the chlorophyll-type pigments and the later electron carriers are very different, the very earliest steps appear to be at least broadly similar. Perhaps this represents a vestige of the mechanism of photochemistry in the primordial reaction center. Alternatively, it could represent the fact that these systems carry out difficult chemistry, and there may not be many distinct feasible solutions to the task of efficient photochemistry. This similarity would then represent convergent evolution rather than common ancestry. There is no firm evidence that relates the two classes of reaction centers, except that they use similar pigments and contain some other similar cofactors such as quinones and carotenoids. No readily identifiable residual sequence similarity is apparent between the two classes of reaction centers, although Robert and Moenne-Loccoz (1990), Margulies (1991), Nitschke and Rutherford (1991) and Otsuka et al. (1992) have proposed some structural similarities. When more sequences of the Fe-S type of reaction center become available, and especially when the structure of one of these reaction centers is determined, residual similarities may appear that are not now apparent. A recent suggestion that most species of all the major families of anoxygenic photosynthetic prokaryotes contain a similar tightly bound c-type cytochrome which serves as electron donor to the reaction center is quite intriguing. This might suggest a common origin for all photosynthetic

electron transport chains, although insufficient sequence data is currently available for this relationship to be established with any certainty. The current data on the relationship is limited to the EPR properties of the tetraheme cytochromes that donate to the reaction center (Feiler et al. 1989, Nitschke and Rutherford 1991, van Vliet et al. 1991). Sequences of these cytochromes would be a very important addition to the database. Despite this lack of any clear structural evidence that unites the two classes of reaction centers, it seems likely that they are indeed descended from a common photosynthetic ancestor. The mechanism of photochemistry is generally the same, with the excited singlet state of the pigment serving as a reductant, and the pigments and other cofactors are similar. The primordial reaction center therefore probably contained a quinone as an early acceptor, and may have also contained an earlier chlorophyll-type acceptor. There is no very clear evidence, however, that it was closer in its properties to either one or the other of the existing classes of reaction centers. One can make a weak case that it may have been closer to the Fe-S type of reaction center, because this type is often found in organisms (e.g., heliobacteria and green sulfur bacteria) that prefer anaerobic environments, and the early atmosphere is almost certain to have been anaerobic. Several authors have suggested that the primordial reaction center was essentially similar to the pheophytinquinone reaction center found in Chloroftexus aurantiacus because of its deep branching position in the eubacteria (Prince et al. 1985, Woese 1987). However, if lateral gene transfer has taken place either to or from this organism as suggested above, then this argument is invalid. There are instances where there is reasonably clear evidence for lateral transfer in bacterial systems (Krawiec and Riley 1990, Smith et al. 1991). As discussed above, the earliest reaction center was almost certainly a protein monomer or at most a homodimer, as the evidence for multiple gene duplications leading to heterodimeric reaction centers is compelling. The pigment was probably a simple porphyrin, with the biosynthetic embellishments that led to stronger red absorption and more favorable redox properties as later developments.

107

Conclusions Clearly, much more is now known about the possible evolutionary origin and development of photosynthesis than was understood just a few years ago. However, it is now becoming increasingly clear that the problem is a multilayered one which may have no one simple answer. The strong possibility that lateral gene transfer events may have taken place during the 3.5 billion years or more that photosynthesis has existed on Earth means that reliable conclusions as to evolutionary pathways may be problematic, and that different parts of the photosynthetic apparatus may have had different original sources. This discussion has centered almost exclusively on the structure, sequence analysis and comparative biochemical analysis of the reaction center complexes. While the reaction center is clearly at the heart of photosynthesis, and must be considered in any treatment of the subject, it is not the only essential player. Complexes that carry out energy collection, secondary electron transfer, carbon fixation, ion transport and ATP synthesis should all be included for a more complete picture.

Acknowledgements I thank Hyman Hartmann for editing this special issue of Photosynthesis Research, Sam Beale, Dan Brune and Donald Burke for helpful discussions, and Jim McManus for assistance with the data analysis for Fig. 4. This is publication #86 from the Arizona State University Center for the Study of Early Events in Photosynthesis. The Center is funded by US Department of Energy grant #DEFG-88-ER13969 as a part of the U S D A / D O E / N S F Plant Science Centers Program. This work was supported by a grant from the Exobiology Program of NASA.

Note added in proof The gene for the reaction center in Chlorobium limicola has been sequenced and shown to have a clear similarity to the core proteins of Photo-

system I (Btittner M, Xie D-L, Nelson H, Pinther W, Hauska G and Nelson N, Proc Acad Sci USA, in press). These authors also provide evidence in favor of a homodimeric reaction center complex in this organism.

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Origin and early evolution of photosynthesis.

Photosynthesis was well-established on the earth at least 3.5 thousand million years ago, and it is widely believed that these ancient organisms had s...
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