Chlorophyll Biosynthesis Gene Evolution Indicates Photosystem Gene Duplication, Not Photosystem Merger, at the Origin of Oxygenic Photosynthesis

Keywords: redox-switch, selective-loss, manganese, cyanobacteria, fusion

Data

The list of organisms was extracted from the GOLD table as accessed on the 16 June 2010 (Bernal et al. 2001). Genomes of photosynthetic prokaryotes were downloaded from RefSeq database release 41 of 9 May 2010 (Pruitt et al. 2005). In addition, the recently sequenced genome of Candidatus Chloracidobacterium thermophilum was also included (Garcia Costas et al. 2012). Homologous proteins involved in (bacterio)chlorophyll biosynthesis were identified by Basic Local Alignment Search Tool (BLAST) (Altschul et al. 1997) within the data set of downloaded genomes (17 eukaryotes and 87 prokaryotes, supplementary table S1, Supplementary Material online) using the proteins shown in supplementary table S2, Supplementary Material online, as queries. The BLAST lists were filtered for E values better than 10⁻¹⁰ and amino acid identities of ≥25%. Paralogs from the cobalamin pathway or later steps in the bacteriochlorophyll c pathway were removed. Because some enzymes of chlorophyll biosynthesis (BchE/ChlE, BciA, and light-dependent NADPH:protochlorophyllide oxidoreductase [LPOR]) belong to protein families with members catalyzing reactions in other pathways, possible paralogs were identified by reBLASTing against the entire National Center for Biotechnology Information (NCBI) refseq database.

Sequence Alignments and Phylogenetic Analysis

Proteins were aligned using MUSCLE (Edgar 2004) using its default parameters. Trees were reconstructed using PhyML 3.0 (Guindon and Gascuel 2003) with the WAG + I + G model and four rate categories. Alignments are available upon request and nonconcatenated phylogenetic trees are given as supplementary figures S1–S12, Supplementary Material online.

Topology Comparisons

Topology testing was performed using the approximately unbiased (AU) test and the Shimodaira–Hasegawa (SH) test (Shimodaira and Hasegawa 1999; Shimodaira 2002). Where justified, initial constrained trees with an imposed separation of (B)Chls genes from RCI- and RCII-containing organisms were created with an in-house perl script and optimized in PhyML 3.0 (Guindon and Gascuel 2003). The site likelihoods of the constrained and the nonconstrained trees were calculated using PhyML 3.0 and the AU and the SH tests performed using CONSEL v0.1k (Shimodaira and Hasegawa 2001).

Taxonomic Distribution of Photosynthesis and Bacteriochlorophyll Biosynthesis Genes

The taxonomic distribution of the photosynthetic apparatus in a sample of sequenced prokaryotic genomes is presented in figure 1 A. Photosynthesis is absent among archaebacteria and present in only 6 of the 24 bacterial phyla currently recognized by NCBI taxonomy. Within those six phyla, photosynthesis is, in general, sparsely distributed. All cyanobacterial genomes and, with one exception—the recently sequenced Ignavibacterium album bacterium (an early diverging member of the chlorobia phylum) (Iino et al. 2010; Liu et al. 2012), all chlorobial genomes sequenced so far have genes coding for the photosynthetic apparatus. Ignavibacterium is a facultative aerobe, lacks photosynthesis genes, and is currently the only nonphototrophic chlorobium to have been cultured (Liu et al. 2012). Nevertheless, the dense distribution of photosynthetic genes in cyanobacteria and chlorobia suggests their presence in the ancestors of these phyla. The same can also be assumed for chloroflexi, at least at the class level. The presence of 1 to 3 chlorophyll biosynthesis genes in Dehalococcoides sp. BAV1, Dehalococcoides sp. CBDB1, and Herpetosiphon aurantiacus probably indicates either LGT or past presence of the pathway and its subsequent loss. In contrast, within proteobacteria and the firmicutes, even at the class level, a sparse distribution of photosynthetic representatives is found, indicating either late acquisition(s) of photosynthesis or many independent losses of it. Because photosynthetic genes are often encoded in superoperons (Alberti et al. 1995; Xiong et al. 1998) or lineage-specific small photosynthetic gene clusters (Xiong et al. 2000), LGT scenarios can, in principle, account for the patchy distribution of photosynthesis among eubacteria. This would also be consistent with the presence of photosynthesis genes, including both photosystems I and II, in the marine phage metagenome (Lindell et al. 2004; Sharon et al. 2009). However, scenarios of vertical inherence have also been discussed, at least for the evolution of RCI-containing organisms (Mix et al. 2005).

Genes involved in chlorophyll biosynthesis were identified in our data set of 104 complete sequenced genomes from photosynthetic organisms (see Materials and Methods). Their taxonomic distribution is presented in figure 1 B. The enzymes of the core chlorophyll biosynthesis pathway are present in all photosynthetic organisms, regardless of which RC type the organism uses. The few differences that are observed with respect to gene presence or absence concern O₂-dependent and O₂-independent alternative enzymes for some steps (see later). Clearly, a single pathway of chlorophyll biosynthesis was present in the ancestral photosynthetic bacterium.

Mg Chelatase

The first unique intermediate of chlorophyll biosynthetic pathway, Mg-protoporphyrin IX (fig. 2 A, step 1), is generated by the insertion of Mg²⁺ into protoporphyrin IX. Biochemical and genetic analysis identified a Class I ATP-dependent magnesium chelatase, composed of three subunits BchH, BchI, and BchD, that catalyzes a reaction (Walker and Willows 1997; Willows and Beale 1998; Bollivar 2006) consisting of an activation and a chelation step. In the presence of both ATP and Mg²⁺, an AAA+ motor complex is assembled from a hexameric (Willows et al. 2004) or heptameric (Reid et al. 2003) BchI ring connected to a hexameric BchD ring (Lundqvist et al. 2010) (the activation step). Proto IX binds to the BchH catalytic subunit, and its transient interaction with the formed AAA+ motor complex leads to the insertion of Mg²⁺ in the tetrapyrrole macrocycle (the chelation step).

The Mg-chelatase complex has both sequence and structural homology with the Class I cobalt chelatase of the O₂-dependent cobalamin biosynthetic pathway (Lundqvist et al. 2009). The CobN, CobS, and CobT subunits of the trimeric cobalt chelatase are homologous with the BchH/ChlH, BchI/ChlI, and BchD/ChlD subunits of magnesium chelatase, respectively (Fodje et al. 2001; Lundqvist et al. 2009). This homology has been interpreted as reflecting ancient duplication and divergence (Lundqvist et al. 2009). Although there is a broad taxonomic distribution of the CobN gene among cobalamin-dependent organisms, a much narrower distribution is observed for the genes that compose the AAA+ motor complex (CobS and CobT) (Rodionov et al. 2003).

The Catalytic Subunit BchH/ChlH

Chlorobaculum tepidum, similar to most members of GSB, has three paralogous genes for this subunit, named BchS, BchH, and BchT. Single- and double-mutant experiments (Gomez Maqueo Chew et al. 2009) showed that strains with only the BchH or the BchS gene retained sufficient Mg-chelatase activity to be viable, but its activity was maximal if the BchS gene was present together with BchH. This was also confirmed by biochemical characterization of the recombinant enzymes (Johnson and Schmidt-Dannert 2008). However, in all mutagenesis experiments, a decrease in the production of bacteriochlorophyll c, the main photosynthetic pigment of GSB, was detected. This suggests that the different isoforms function in end-product regulation and/or substrate channeling of the Bch c intermediates (Johnson and Schmidt-Dannert 2008; Gomez Maqueo Chew et al. 2009).

The existence of BchH/ChlH paralogs is not unique to the GSB. All chloroflexi have at least one additional gene coding this subunit (Gomez Maqueo Chew et al. 2009), and the same is also true for some cyanobacterial species (Lohr et al. 2005). Isoforms of the gene also occur in some eukaryotes (Lohr et al. 2005) although, in this case, different duplication events are possibly at their origin.

The schematic diagram summarizing the BchH/ChlH phylogenetic tree is presented in figure 3 A. A clear dichotomy between the different subunit isoforms can be observed. The upper clade contain sequences similar to the BchH gene of Chlorobaculum tepidum TLS. With the exception of Chlorobium chlorochromatii, all organisms from the seven phyla considered contain at least one copy the BchH/ChlH gene. In this group, three distinct groups are retrieved: 1) chloroflexales and chlorobia, 2) acidobacteria and proteobacteria, and 3) heliobacteria and cyanobacteria with photosynthetic eukaryotes branching as basal members. Recent events of gene duplication can also be observed in the chloroflexales ancestor and at the species level of three land plants.

Notably, there is no relationship between the type of RC and the organization of the sequences within the tree, indicating a single origin of this pathway. Moreover, a close relationship between chlorobia and chloroflexi sequences is observed, a relationship found in most of our phylogenetic analysis. Based inter alia on the observation that fundamental aspects of core carbon and energy metabolism in chlorobia and chloroflexi are different, it has been suggested that lateral transfer of genes underlying chlorosome structure and chlorophyll biosynthesis might have occurred between these groups (Raymond et al. 2002). However, the close phylogenetic proximity of chlorophyll biosynthesis genes among organisms that contain different RC types is not confined to these two groups.

The lower clade of the tree contains sequences similar to the Chlorobaculum tepidum TLS BchS and BchT genes, belonging to chlorobia, chloroflexi, cyanobacteria, and green algae. In this clade, two distinct groups are retrieved, one comprising the cyanobacterial and plastid sequences and the other with chloroflexi BchH2 and chlorobial BchS and BchT sequences. A duplication event in the ancestor of the chlorobia appears to be the likely origin of the two isoforms.

The role of these subunits has been proposed to be either end-product regulation and/or substrate channeling of the Bch c intermediates (Johnson and Schmidt-Dannert 2008; Gomez Maqueo Chew et al. 2009). Both chlorobia and chloroflexi have Bch c pigments, but the cyanobacteria synthesize only chlorophyll a, raising the question of what the role of these cyanobacterial homologs might be. The Gloeobacter violaceus ChlH2 sequence alone falls outside these two main clades; furthermore, it is more similar to homologs in nonphotosynthetic lineages (euryarchaeotes and firmicutes) than to its photosynthetic homologous (data not shown). This suggests that Gloeobacter ChlH2 is not involved in chlorophyll biosynthesis.

The presence of BchH/ChlH isoforms in three out of the six considered bacterial phyla and their monophyly within the two clades may suggest their presence in the ancestral chlorophyll pathway, in which case the isoforms would have been lost (or not LGT acquired) in proteobacteria, acidobacteria, and heliobacteria.

The AAA⁺ Motor: BchI/ChlI and BchD/ChlD

The BchI/ChlI subunit is a member of the AAA⁺-ATPase family of proteins, which includes proteins of diverse function (Fodje et al. 2001). With the exception of some land plants (Kobayashi et al. 2008; Huang and Li 2009) and green algae (Lohr et al. 2005), there is a consensus in the literature that photosynthetic organisms only have one BchI/ChlI subunit. However, a study of two recombinant isoforms of BchI from Prosthecochloris vibrioformis showed that both had Mg chelatase activity in vitro (Petersen et al. 1998), and in the recently sequenced genome of Chloroflexus aurantiacus, three genes were annotated as BchI (Tang et al. 2011). In our search, several isoforms belonging to both chlorobia and chloroflexi were retrieved. These enzymes are distinct from the aerobic cobalamin chelatase CobS gene and were included in the analysis (fig. 3 B).

The BchI/ChlI tree is divided into two clades, one comprising BchI/ChlI genes among all photosynthesizers and one containing the different isoforms from GSB and GNSB, which we call the GSB/GNSB clade. In the former, two major groups can be observed, one with heliobacteria, chlorobia, chloroflexi, acidobacteria, and proteobacteria (branching in that order) and a second one, where the cyanobacteria and eukaryotic sequences cluster together. The isoforms present in the GSB/GNSB clade, as in the case of G. violaceus ChlH2 sequence, have high similarity with sequences similar to hypothetical magnesium chelatases from nonphotosynthetic organisms. Although the results from P. vibrioformis indicate that both isoforms have identical activities in vitro, their sequences show higher similarity with sequences from organisms that do not synthetize bacteriochlorophyll, questioning their role in chlorophyll biosynthesis. Specifically, within delta-proteobacteria, proprionobacterales, firmicutes, and euryarchaeota, some organisms possess isoforms of the BchI/ChlI gene in addition to CobS. Other cobalamin producers possess only the BchI/ChlI gene and lack CobS. In these organisms, the BchI/ChlI genes probably substitute the missing CobNST genes (Xiong et al. 1998; Lohr et al. 2005). The distributions of BchI/ChlI and CobS homologs suggest a way in which pre-existing building blocks could have been recruited into the assembly of the ancestral chlorophyll and O₂-dependent cobalamin pathway.

The N-terminus of BchD/ChlD gene, which is also a member of the AAA⁺-ATPase family of proteins (Fodje et al. 2001), has a segment of approximately 260 amino acid residues with sequence homology to BchI/ChlI (Masuda et al. 1999). BchD/ChlD has a proposed structural role in magnesium chelatase, functioning as a platform for the convergence of the other two subunits (Axelsson et al. 2006). The BchD/ChlD phylogenetic tree in figure 3 C was rooted by two sequences of von Willebrand factor Type A, which is considered to be an ancient protein domain (Ponting et al. 1999). The overall BchD/ChlD tree topology is very similar to the upper part of the BchH/ChlH tree with the exception of the position of C. Chloracidobacterium thermophilum. There are two distinct BchD/ChlD clades. One contains acidobacteria, the GSB/GNSB clade, and proteobacteria. In the second, heliobacteria, cyanobacteria, and eukaryotic sequences cluster. There are two eukaryotic clades, one composed of green algae isoforms that branch between heliobacteria and cyanobacteria, and a second in which at least one copy from every eukaryotic organism is represented in a sister group of the G. violaceus sequence. However, this branch is poorly supported. As in the case of BchI/ChlI, copies of this gene are also present in nonphotosynthetic organisms.

Mg Protoporphyrin IX Methyltransferase

The next step in the pathway of synthesis is the insertion of a methyl group by the enzyme Mg-protoporphyrin IX methyl transferase (BchM/ChlM) to form the Mg-protoporphyrin IX monomethyl ester (MPE) (fig. 2 A, step 2). This enzyme belongs to the Class I S-adenosylmethionine-(SAM-)dependent methyltransferase family (Gibson and Hunter 1994) and transiently interacts with BchH/ChlH (Johnson and Schmidt-Dannert 2008). With the exception of Arabidopsis thaliana, all photosynthetic organisms have only one BchM/ChlM gene. There is strong support for monophyly of the major photosynthetic taxa, and in this case, because cyanobacteria and eukaryotes cluster together, while heliobacteria branch closer to the chlorobia/chloroflexi sister groups and acidobacteria closer to proteobacteria (fig. 3 D).

Mg-Protoporphyrin IX Monomethyl Ester Oxidative Cyclases

The next step in the pathway is the formation of the isocyclic ring by the conversion of MPE to 3,8-divinyl protochlorophyllide a. This complex reaction entails the cyclization of the ring and the introduction of a keto group at carbon 13¹. This step is catalyzed by either of two different and unrelated enzymes: the oxygen-dependent enzyme AcsF (fig. 2 A, step 4) and the oxygen-independent enzyme (BchE), both of which catalyze the reaction (fig. 2 A, step 3). The arguably more ancient reaction of the oxygen-independent cyclase, BchE, uses water as electron donor and is widely distributed among heliobacteria, proteobacteria, GNSB, and GSB. Although all cyanobacteria have the AcsF enzyme, some, including Synechococcus sp. PCC 6803, also harbor a functional ChlE gene (Minamizaki et al. 2008) that can complement Rhodobacter capsulatus BchE-deficient strains (Bollivar 2006). BchE/ChlE is a radical-SAM enzyme with homology to adenosylcobalamin-binding domain. In R. capsulatus and Chlorobium limicola strain 1230, the enzyme appears to be vitamin B12 (cobalamin) dependent (Fuhrmann et al. 1993; Gough et al. 2000). However, these two sequences lack the canonical signature motif (DXHXXG) that typically contains the cobalt coordinating histidine residue (Drennan et al. 1994). The BchE/ChlE alignment reveals, however, a highly conserved histidine (H102 Chlorobaculum tepidum TLS numbering) that might function as the missing cobalt ligand, and, in sequences where H102 is missing, another histidine residue (H108 Synechocystis sp. PCC6803 numbering) is present close by, whereas no functional role of either in B12 binding has been shown. The two clades of the phylogenetic BchE tree (fig. 3 E) can be divided by the position of this residue

Chlorobaculum tepidum has seven BchE homologous genes, whereby only three (BchE, BchR, and BchQ) are involved in bacteriochlorophyll biosynthesis (Gomez Maqueo Chew et al. 2007). BchR and BchQ act as methyl transferases performing specific methylations in the later steps of Bacteriochlorophyll c pathway (Gomez Maqueo Chew et al. 2007) and probably arose from later lineage-specific duplication events. These paralogs and all BchE-related genes with higher sequence similar to homologs from nonphotosynthetic organisms were removed from the phylogenetic analysis.

The BchE tree reveals two well-supported major clades, one containing the Chlorobaculum tepidum and R. capsulatus sequences and another where cyanobacterial homologs and proteobacterial BchE isoforms are sister groups (fig. 3 E). Within the first clade, there is a clear separation between proteobacteria sequences from the other taxa. In this tree, the sequences belonging to heliobacteria and acidobacteria cluster between chloroflexi and chlorobia.

AcsF is the enzyme from the O₂-dependent pathway. It is present in cyanobacteria, photosynthetic eukaryotes, and chloroflexi, as well as in some photosynthetic proteobacteria. This oxygen-dependent enzyme most likely had its origin within the cyanobacteria and was vertically inherited and horizontally transferred to other photosynthetic organisms. Until the discovery of photosynthesis in Acidobacteria, this enzyme was only present in RCII-containing organisms. The presence of an O₂-dependent enzyme in an RCI phototroph is interesting due to the usual oxygen sensitivity of the iron–sulfur centers of RCI (Tsukatani et al. 2012). However, the C. Chloracidobacterium thermophilum RCI center is not oxygen sensitive, probably because of adaptation of the organism to the aerobic lifestyle (Tsukatani et al. 2012). The AcsF phylogenetic tree can be divided into two major clades, both containing cyanobacterial sequences (fig. 3 F). Nostocales and Cyanothece taxa have two AcsF isoforms named here AcsF1 and AcsF2. At first sight, the dichotomy of the tree might seem to be a reflection of this duplication event. Nevertheless, none of the clades contain sequences from all represented cyanobacteria organisms. Specifically, the major branch contains AcsF1 from all photosynthetic phyla chosen, but no Prochlorococcus sequences are present. These cluster in the lower branch of the tree, with the other cyanobacterial AcsF2 isoforms. This could suggest that the oxygenic photosynthetic ancestor (or at least the extinct ancestor of nostocales and Cyanothece and possibly Prochlorococcus) had two AcsF isoforms, which were selectively lost in some organisms, with the AcsF1 isoform having been laterally transferred to other photosynthetic lineages. The C. Chloracidobacterium thermophilum sequence is basal to the group of noncyanobacterial AcsF sequences and has higher sequence similarity with the chloroflexi clade.

(Di)Vinyl Reductases

With exception of some Prochlorococcus strains (Chisholm et al. 1992) and heliobacteria (bacteriochlorophyll g), (bacterio)chlorophylls have an ethyl group at position 8 of ring II. The reduction of the 8-vinyl group by a 8-vinyl reductase enzyme may occur at various steps of the chlorophyll biogenesis pathway (Tripathy and Rebeiz 1988; Kim and Rebeiz 1996; Adra and Rebeiz 1998; Kolossov and Rebeiz 2001) either in a sequential or in a parallel route (Parham and Rebeiz 1995; Nagata et al. 2005), thereby generating some of the observed heterogeneity of chlorophylls and their intermediates. For clarity, here we show a sequential representation, keeping the other possible alternatives in mind.

There are at least two unrelated enzymes that catalyze this reaction: BciA and BciB (or slr1923) (Islam et al. 2008; Ito et al. 2008; Bryant et al. 2012). BciA (fig. 2 A, step 5) belongs to the short-chain dehydrogenases/reductases family having a ligand-binding site and a NAD(P)⁺/NAD(P)H-binding site. It is present in some organisms belonging to chlorobia, cyanobacteria, eukaryotes, and proteobacteria. Mutagenesis and biochemical experiments identified the BciA gene in Chlorobaculum tepidum, A. thaliana, and Oryza sativa (Nagata et al. 2005; Nakanishi et al. 2005; Chew and Bryant 2007; Wang et al. 2010). As seen in figure 4 A, these orthologo genes form a well-supported clade that can be subdivided into two groups, one comprising GSB and proteobacteria sequences and another with cyanobacteria and eukaryotic sequences. The only exception is the Acaryochloris marina sequence that clusters within the proteobacterial clade.

Because of the broad distribution of NAD(P)H-binding sites (Rossman folds) in proteins, database searching retrieved many additional hits (lower part of the tree). BciA shares sequence similarity with a proposed chaperone for quinone binding in PSII (Ermakova-Gerdes and Vermaas 1999) and also with some sequences of unknown function among chlorobia. Interestingly, another Aca. marina isoform is positioned with the functionally undetermined chlorobial sequences. To root the tree, a group of five sequences belonging to photosynthetic and nonphotosynthetic organisms was used.

The BciB gene (fig. 2 B, step 6) is present in all phyla considered here, and, with exception of gamma-proteobacteria, the groups are all monophyletic (fig. 4 B). BciB has high homology with coenzyme F420-reducing hydrogenase only found in methanogenic archaea (Islam et al. 2008). The G. violaceus sequence, basal to the proteobacterial clade, represents a second copy (an isoform) of the BciB gene in the Gloeobacter genome and was probably a later acquisition via lateral transfer from proteobacteria. The BciB tree is one of the few cases where chloroflexi and chlorobia are not sister groups, with chloroflexi closer to Allochromatium vinosum and C. Chloracidobacterium thermophilum sequences. Also, BciB shows separation between the major proteobacterial clade and the other photosynthetic taxa.

Protochlorophyllide Reductases

The last step of the common metabolic pathway of (bacterio)chlorophyll consists of the reduction of the IV pyrrole ring of protochlorophyllide to form chlorophyllide. Two distinct enzymes have evolved to catalyze this reaction, the LPOR and the light-independent protochlorophyllide reductase (DPOR) composed of three different subunits, BchL/ChlL, BchN/ChlN, and BchB/ChlB.

LPOR (fig. 2 A, step 7) belongs to the short chain alcohol dehydrogenases family and is present in oxygenic photosynthetic organisms (Dahlin et al. 1999). This enzyme most likely originated in cyanobacteria and was acquired by eukaryotes at the origin of plastids (Yang and Cheng 2004). Because of its involvement in the development of etiolated and greening tissues (Fujita 1996), LPOR from different organisms has been studied extensively in terms of mechanism, function, localization, and expression (summarized in Reinbothe et al. [2010]). Several isoforms of this nuclear encoded enzyme are present in eukaryotic phototrophs (named PorA, PorB, and PorC in A. thaliana) with differential expression and function along A. thaliana development (Masuda et al. 2003). Besides the isoforms present in eukaryotes, additional putative LPORs belonging to cyanobacteria and Dinoroseobacter shibae DFL 12 were retrieved via database searching. The Dinoroseobacter gene clusters within the Synechococcus clade and is probably a recent gene acquisition. The tree in figure 4 C can be divided into two major clades, each one containing cyanobacterial and eukaryotic homologs. The upper part of the tree contains biochemically characterized LPORs. The several PorA, PorB, and PorC enzymes found in angiosperms cluster together, indicating duplication and functional or regulatory specialization during plant evolution.

The lower part of the LPOR tree contains cyanobacterial isoforms and eukaryotic isoforms, the latter, so far, uncharacterized. Curiously, in this subtree, angiosperm (Vitis vinifera and Oryza sativa) and algal sequences (Micromonas sp. and Ostreococcus lucimarinus) form two statistical significant groups, the former clustering with Aca. marina and Cyanothece sequences and the later with marine cyanobacteria (Synechococcus and Prochlorococcus). It is possible that these two major LPOR isoforms existed before the origin of plastids and were acquired then, with subsequent differential loss. This suggestion is in agreement with the presence of multiple LPOR isoforms in modern cyanobacteria.

The DPOR (fig. 2 A, step 8) is present in all photosynthetic phyla, having been lost in most of the angiosperm species (Fong and Archibald 2008). Its three subunits, (B)ChlLNB, have homology with a second chlorin reductase complex BchXYZ present only in bacteriochlorophyll-containing organisms. This complex is responsible for the reduction of the C7–C8 bond, converting chlorophyllide into bacterochlorophyllide. (B)ChlLNB also has homology with the nitrogenase complex (nifHDK) responsible for nitrogen fixation in some bacterial and archaeal taxa (Leigh 2000; Dedysh et al. 2004; Raymond et al. 2004). The nifHDK complex is proposed to have an ancient origin and to be at the base of the (B)ChlLNB complex (Dorr et al. 2003; Martin 2012).

Two groups of cyanobacteria are observed in (B)ChlLNB trees (fig. 4 D). Sequences from marine cyanobacteria (Synechococcus and Prochlorococcus) cluster with proteobacterial homologs, whereas the remaining cyanobacterial sequences and the two eukaryotes known to have (B)ChlLNB (Physcomitrella patens and Chlamydomonas reinhardtii) cluster next to the chlorobia/chloroflexi clades. Events of LGT between cyanobacteria and proteobacteria are well documented (Badger and Price 2003; Beiko et al. 2005; Zhaxybayeva et al. 2006), especially for the closely related Synechococcus and Prochlorococcus genera. However, the polarity of this LGT (who was donor, who was recipient) is still not established (Bryant et al. 2012; Gupta 2012). In the different DPOR trees, the heliobacterial sequences align either with nonmarine cyanobacteria or with the chlorobia/cloroflexi group, whereas the acidobacterial sequence is basal either to the proteobacterial clade (BchB/ChlB and BchL/ChlL) or to the Heliobacterium-containing clade (BchN/ChlN).

Two Cyanobacterial RCs: Gene Duplication, Not Lineage Merger

The most important observation from this study is that there is no coevolutionary pattern linking chlorophyll biosynthesis gene phylogeny with either RCIs or RCIIs; in other words, we observe neither Type I- or Type II-specific chlorophyll biosynthesis genes nor Type I- or Type II-specific chlorophyll biosynthesis gene phylogenies. Because RCs cannot undergo evolution in the absence of chlorophyll, this lack of coevolutionary pattern linking chlorophyll biosynthesis to the divergence of RCI and RCII allows us to exclude the widely discussed possibility that RCI and RCII diverged via lineage splitting and became reunited in cyanobacteria via a large-scale gene transfer event (Mathis 1990; Blankenship 1992; Meyer 1994; Blankenship and Hartman 1998; Xiong et al. 1998, 2000; Blankenship 2001; Xiong and Bauer 2002a, 2002b; Blankenship 2010), of the kind that Hohmann-Marriott and Blankenship (2011) call "fusion theories." Indeed, the consistently close proximity of the GSB (chlorobia, with RCI) and green nonsulfur bacteria (chloroflexi, with RCII) in chlorophyll biosynthesis trees argues strongly against the view that there was a deep evolutionary split in chlorophyll biosynthesis corresponding to a lineage split between RCI and RCII, one that would be expected to have pulled (B)Chl genes in tow. This is all the more true given the tendency for the chlorophyll biosynthesis genes from proteobacteria (with RCII) to branch in close proximity to their cyanobacterial homologs, rather than with homologs from green nonsulfur bacteria. In addition, the chlorophyll biosynthesis genes of C. Chloracidobacterium thermophylum (with RCI) usually branch in close proximity to RCII-containing taxa (proteobacteria or chloroflexi).

If we thus exclude ancient lineage splitting and later (re)union in cyanobacteria at the evolutionary origin of two RC types coexisting in the same cell, the simplest competing alternative, and one widely discussed in the literature (Olson and Pierson 1987a; Vermaas 1994; Olson 2001; Allen 2005; Mulkidjanian et al. 2006), is that gene duplication giving rise to RCI and RCII within the same genome gave rise to the photosystem configuration in oxygenic photosynthesis. This possibility is easily reconciled with chlorophyll biosynthesis phylogenies. An immediately ensuing question is: in which lineage did the gene duplication take place? Occam’s razor clearly favors the premise that the photosystem genes underwent duplication in an ancestral cyanobacterium—a protocyanobacterium—because cyanobacteria are the only group where genes for both RC types have remained present and expressed. It is possible to assume that the duplication took place elsewhere, but there is no obvious alternative location.

What Use Might Two Photosystems Be?

Olson and Pierson (1987a, 1987b) have suggested an ancient gene duplication event in a cyanobacterium for the origin of the two photosystems. However, that formulation accounted for the distribution of chlorophyll-based photosynthesis and RC types among prokaryotic groups exclusively by vertical inheritance and differential loss. Today, with the number of bacterial lineages having grown, the distribution of photosynthesis and RCs (fig. 1) has become much more sparse than in 1987, such that differential loss alone is unlikely to account in full for these distributions, especially because photosynthesis genes are observed to be mobile in the marine phage metagenome, and because substantial amounts of LGT have indeed been shown for photosynthetic lineages (Raymond et al. 2002; Huang and Gogarten 2007; Shi and Falkowski 2008). Hence, a mechanistic mixture of some vertical inheritance, some differential loss, and some lateral transfer, relative amounts of which might differ from gene to gene across (B)Chl synthesis, needs to be invoked, because the trees for (B)Chl biosynthesis genes are insufficiently similar for artifacts of phylogenetic reconstruction to account for their differences.

However, how much and what kind of LGT might be required to explain the distribution of photosynthesis among prokaryotes? Various possibilities have recently been discussed, for example, by Bryant et al. (2012) and Gupta (2012). However, that question is not the focus of this article. Rather, the question at our focus is how two photosystems came to reside within a single genome so as to give rise to oxygenic photosynthesis. Gene duplication in a protocyanobacterium is the alternative most compatible with present data. If there were two photosystems, what were they doing?

This question has to do with the transition from anoxygenic photosynthesis to water splitting. Blankenship and Hartman (1998) suggested that hydrogen peroxide (H₂O₂) might have been an initial electron donor far more chemically accessible than water, for a linear two-photosystem ETC. Mulkidjanian et al. (2006) suggested that H₂ might have been the initial electron donor for a two-photosystem ETC. Nisbet and coworkers (Nisbet et al. 1995; Nisbet and Sleep 2001) suggest that the manganese complex evolved either to handle excess of peroxide or as a toxic weapon against competitors.

An alternative suggestion (Mathis 1990; Allen and Puthiyaveetil 2005) differs from the foregoing models with respect to the presumed function of the two photosystems. It posits that the two photosystems in the protocyanobacterium operated in a temporally regulated manner (Allen 2005), for example, as an H₂S-oxidizing and NAD⁺-reducing RCI when H₂S was available as it occurs in modern Chlorobium or as a light-driven proton pump (cyclic electron flow thorough RCII as in Rhodobacter) when H₂S was not available. Before the water-splitting complex had evolved, what would a bacterium with two different and specialized, nonoxygenic photosystems have done with them? Probably just what modern bacteria do: express them when needed, with the help of a regulatory switch. This model implies relatively strict regulation of the RC genes, because in the event that regulation failed, for example, through mutation of the regulatory protein constituting the redox switch, both RCIs and RCIIs became expressed in the absence of H₂S, the protocyanobacterium would be exposed to a lethal level of oxidative stress (there is no way to turn off assembled photosystems), unless it could extract electrons from an environmentally available donor.

In principle, such a donor could have been H₂O₂, or H₂, or an organic compound such as succinate. However, it also could have been aqueous Mn^II/III cations, which have the interesting property of giving off low potential electrons under ultraviolet (UV) radiation (photooxidation) (Anbar and Holland 1992; Hakala et al. 2006; Allen and Martin 2007; Russell et al. 2008). Before the accumulation of atmospheric oxygen (and hence ozone), UV was a larger component of the solar radiation that reaches the Earth’s surface than it is today. Thus, the presence of light for photosynthesis would have also meant the presence of UV radiation for Mn^II/III photooxidation. Photooxidation of aqueous, environmental Mn^II/III could have thus literally "pushed" electrons into photooxidized chlorophyll of RCII. That would have led to a lethal log-jam of electrons, or over-reduction, in the electron-transport cycle—unless the protocyanobacterium was simultaneously expressing RCI. This complex would redirect the surplus membrane-bound electrons stemming from photosystem II into CO₂-reduction and thereby create precisely the flow of electrons seen in cyanobacteria today: a linear flow through two photosystems.

Obviously, such an ETC would hardly have been perfect from the beginning. And clearly there is a difference between tapping environmental Mn atoms photooxidatively, one at a time, and the establishment of the resident, catalytic Mn₄Ca center in cyanobacterial RCII water-splitting complex. However, the overall contours of the circuit would have been right, from manganese at RCII and going on through RCI to NADH and ultimately to CO₂. The key to water splitting would then have entailed the transition from exploiting an environmental supply of soluble manganese, where each electron-donating Mn ion would reach photosystem II by simple diffusion, to holding four manganese atoms (and a calcium of as-yet-unknown function) in place. Dissolved Mn²⁺ has long been known to donate electrons to photosystem II, and thus to reconstitute noncyclic electron transport, in isolated chloroplasts biochemically depleted of the capacity to oxidize water to oxygen (Cheniae 1970). Following adsorption of Mn to its donor side, a fine tuning of photosystem II by natural selection to optimize its reduction/oxidation potential could have allowed it to oxidize a now biologically portable manganese reservoir four times in a row.

It is notable that the Mn atoms of the water-splitting complex are bound directly by the proteins of the photosystem II RC, without an intervening protein or electron carrier. This suggests that no major evolutionary invention was required for photosystem II to tap environmental Mn as an electron source. In line with that, it has recently been shown (Allen et al. 2012) that an engineered, Mn-binding RCII of R. sphaeroides will produce O₂ from Inline graphic {\rm O}_{\rm 2}^- in the presence of Mn in a light-dependent reaction in which photodamage is impeded in comparison with that in a wild-type, Mn-free RC. Allen et al. (2012) interpret this observation as an important clue to the origin of oxygenic photosynthesis.

In what sort of setting could suitably high concentrations of Mn^II/III have accumulated for such series of events to transpire? Mn is not a good candidate for high enough concentrations to make the model viable in an open ocean setting. However, in a locally circumscribed freshwater setting, sufficiently high Mn^II/III concentrations could, in principle, have accumulated.

In this context, it is of particular interest that Blank and Sáchez-Baracaldo (2010) recently provided evidence that oxygenic photosynthesis arose in a freshwater environment, based on the basal phylogenetic position of freshwater cyanobacteria and the derived phylogenetic position of marine cyanobacteria.

Related Pathways and the Cell That Invented Chlorophyll

Chlorophylls coordinate Mg²⁺ and belong to the tetrapyrrole family, which includes cobalamin (Co²⁺), heme (Fe²⁺), sirohem (Fe²⁺), heme d1 (Fe²⁺), and F₄₃₀ (Ni²⁺) (Heinemann et al. 2008; Warren and Smith 2009; Zappa et al. 2010). All tetrapyrrole biosynthetic pathways are related in the sense that they start from the universal precursor, δ-aminolevulinic acid, and share three enzymatic steps that generate the tetrapyrrole macrocycle uroporphyrinogen III (UroIII) (fig. 5). Proto IX is the common precursor for chlorophyll synthesis and heme synthesis via the classical pathway that occurs in eubacteria and eukaryotes (Heinemann et al. 2008). Precorrin-2 is the common precursor for cobalamin, heme synthesis via the alternative pathway recently discovered in archaebacteria (Storbeck et al. 2010; Bali et al. 2011), siroheme (a cofactor in some nitrite and all sulfite reductases (Tripathy et al. 2010), heme d1 (a cofactor only present in the bacterial cd₁ nitrite reductases (Allen et al. 2005), and F₄₃₀ pathways. F₄₃₀ is a cofactor that is critical to methanogenesis and has only been found in methanogens so far (Thauer 1998). In addition to two routes for heme synthesis, there are also two routes for cobalamin synthesis, one O₂ dependent (often called the late pathway due to the late insertion of Mg²⁺) and one O₂ independent (early insertion of Mg²⁺) (Martens et al. 2002; Warren et al. 2002). The O₂-dependent cobalamin pathway involves the Co²⁺ chelatase CobNST, the three subunits of which are related to (B)ChlHID. It has been suggested that (B)ChlHID arose from CobNST (Xiong et al. 2000), but the converse might be more likely given the presence of one O₂-dependent step in the late cobalamin pathway (Martens et al. 2002; McGoldrick et al. 2005). In the early (O₂ independent) cobalamin pathway, the CbiK/CbiX^L/CbiX^s chelatases are related to the SirB and HemH chelatases of the siroheme and classical heme pathways, respectively (Schubert et al. 1999; Brindley et al. 2003; Romao et al. 2011). The chelatase for the F₄₃₀ pathway is unknown, but genes related to (B)ChlHID are present in methanogens and encode candidates for the Ni²⁺-chelatase. In some organisms, the insertion of iron and cobalt into sirohydrochlorin is performed by multifunctional chelatases (CysG and Met8p) (Spencer et al. 1993; Fazzio and Roth 1996; Schubert et al. 2002) (Class III).

What did the cell that invented chlorophyll biosynthesis have in terms of tetrapyrrole pathways? It definitely contained cobalamin and might have had a cobalamin biosynthesis pathway (the O₂-independent type, obviously), because the O₂-independent route to 3,8-divinyl protochlorophyllide a via (B)ChlE, a cobalamin-dependent reaction (Fuhrmann et al. 1993; Gough et al. 2000). Of course, it could also have just been cobalamin dependent; some cyanobacteria synthesize cobalamin, and many, however, acquire it from the environment via high affinity importers (Tang et al. 2012). The cell that invented chlorophyll also had a classical heme pathway, because barring chlorophyll, the three steps from UroIII to Proto IX are specific to classical heme synthesis (Heinemann et al. 2008) and hence preceded the (B)Chl pathway. The first cell with chlorophyll probably also fixed nitrogen, because the subunit of DPOR, (B)ChlNBL, is related to nitrogenase subunits (Xiong et al. 1998). We propose that the cell that invented chlorophyll was a cobalamin-dependent, heme-synthesizing, diazotrophic anaerobe.

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