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Cited by 144Photosynthetic Processes and MechanismsProtist diversity and phylogenyMetalloenzymes and iron-sulfur proteins

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Early Archean origin of Photosystem II

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Cardona, Tanai, Sánchez‐Baracaldo, Patricia, Rutherford, A. William, Larkum, Anthony W.·2019·Geobiology
DOI 10.1111/gbi.12322PMC PMC6492235

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Abstract

Photosystem II is a photochemical reaction center that catalyzes the light-driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here, we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale, we hypothesize that this early Archean photosystem was capable of water oxidation to oxygen and had already evolved protection mechanisms against the formation of reactive oxygen species. This would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

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Figure 1 Evolution of Type II reaction center proteins. (a) A maximum likelihood phylogeny of Type II reaction center proteins. (b) A schematic representation of the phylogeny shown in (a). All reaction centers have common ancestry and descended from a homodimeric reaction center, marked A. From A, two new reaction centers emerged, one ancestral to all Type II reaction centers (II) and a second ancestral to all Type I reaction centers. This is the earliest diversification event of reaction center proteins that can be inferred from sequence and structural data and it is marked 1. The ancestral Type II reaction center protein (II) gave rise to two new proteins, one ancestral to D1 and D2, named here D0 and a second ancestral to L and M named K. The ancestral L and M subunits further diversify into Chloroflexi‐type and Proteobacteria‐type L and M subunits (5). Step 6 indicates that Type I reaction center proteins also diversified in parallel to Type II reaction center proteins. (c) Evolution of cyanobacterial D1 and D2, modified from Cardona et al. (2015). G0, G1, and G2 represent atypical D1 forms, and G3 and G4 standard D1 forms. ΔT marks the span of time between D0 and the appearance of the ancestral standard form of D1, which characterizes PSII and predates the most recent common ancestor of all known Cyanobacteria capable of oxygenic photosynthesis [Colour figure can be viewed at wileyonlinelibrary.com]
Figure 1 Evolution of Type II reaction center proteins. (a) A maximum likelihood phylogeny of Type II reaction center proteins. (b) A schematic representation of the phylogeny shown in (a). All reaction centers have common ancestry and descended from a homodimeric reaction center, marked A. From A, two new reaction centers emerged, one ancestral to all Type II reaction centers (II) and a second ancestral to all Type I reaction centers. This is the earliest diversification event of reaction center proteins that can be inferred from sequence and structural data and it is marked 1. The ancestral Type II reaction center protein (II) gave rise to two new proteins, one ancestral to D1 and D2, named here D0 and a second ancestral to L and M named K. The ancestral L and M subunits further diversify into Chloroflexi‐type and Proteobacteria‐type L and M subunits (5). Step 6 indicates that Type I reaction center proteins also diversified in parallel to Type II reaction center proteins. (c) Evolution of cyanobacterial D1 and D2, modified from Cardona et al. (2015). G0, G1, and G2 represent atypical D1 forms, and G3 and G4 standard D1 forms. ΔT marks the span of time between D0 and the appearance of the ancestral standard form of D1, which characterizes PSII and predates the most recent common ancestor of all known Cyanobacteria capable of oxygenic photosynthesis [Colour figure can be viewed at wileyonlinelibrary.com]CC BY · PubMed Central
Figure 2 Decrease of sequence identity of D1 and D2 proteins as a function of divergence time. D1 subunits are shown in gray and D2 in orange. The divergence time between pairs of species is plotted against the level of sequence identity as tabulated in Supplementary Table S1. The red circle, placed at 79.2%, corresponds to the average sequence identity of the three distinct Group 4 D1 sequences of Gloeobacter violaceous in comparison with that of Cyanidioschyzon merolae. The light orange bar marks the GOE. The dashed line is fitted from a linear function and shows that over a period of at least 2.0 Ga, no dramatic changes in the rates of evolution of D1 and D2 are observed. The red dashed lines show an extrapolation of current rates of evolution throughout Earth's history. This line highlights that the rate is too slow for the divergence of D1 and D2 to have started right before the GOE. The gray dots around 3.5–3.8 Ga mark a speculative timing for the earliest events in the history of photosynthesis: the divergence of D1 and D2 (~29% sequence identity), the divergence of anoxygenic (L/M) and oxygenic (D1/D2) reaction center proteins (~17%), and the divergence of Type I and Type II reaction center proteins (≤10%). The curved blue line highlights that any scenario for the diversification of reaction centers after the origin of life requires faster rates of evolution at the earliest stages in the evolution of photosynthesis [Colour figure can be viewed at wileyonlinelibrary.com]
Figure 2 Decrease of sequence identity of D1 and D2 proteins as a function of divergence time. D1 subunits are shown in gray and D2 in orange. The divergence time between pairs of species is plotted against the level of sequence identity as tabulated in Supplementary Table S1. The red circle, placed at 79.2%, corresponds to the average sequence identity of the three distinct Group 4 D1 sequences of Gloeobacter violaceous in comparison with that of Cyanidioschyzon merolae. The light orange bar marks the GOE. The dashed line is fitted from a linear function and shows that over a period of at least 2.0 Ga, no dramatic changes in the rates of evolution of D1 and D2 are observed. The red dashed lines show an extrapolation of current rates of evolution throughout Earth's history. This line highlights that the rate is too slow for the divergence of D1 and D2 to have started right before the GOE. The gray dots around 3.5–3.8 Ga mark a speculative timing for the earliest events in the history of photosynthesis: the divergence of D1 and D2 (~29% sequence identity), the divergence of anoxygenic (L/M) and oxygenic (D1/D2) reaction center proteins (~17%), and the divergence of Type I and Type II reaction center proteins (≤10%). The curved blue line highlights that any scenario for the diversification of reaction centers after the origin of life requires faster rates of evolution at the earliest stages in the evolution of photosynthesis [Colour figure can be viewed at wileyonlinelibrary.com]CC BY · PubMed Central
Figure 3 Relaxed molecular clock of Type II reaction center proteins. A log‐normal autocorrelated relaxed clock is shown implementing a CAT + GTR + Γ model with flexible boundaries on the calibration points. Red dots are calibration points as described in Materials and Methods. The gray dot denoted II represents the ancestral Type II reaction center protein, as schematized in Figure 1. The orange dot (D0) marks the initial divergence of D1 and D2. The violet dot marks the divergence point between G2 atypical D1 sequences and standard D1. The green dot marks the divergence point between the microaerobic D1 forms (G3) and the dominant form of D1 (G4). This point represents the last common ancestral protein to all standard D1 forms predating crown group Cyanobacteria. The blue dot represents the origin of the dominant form of D1 inherited by all extant Cyanobacteria and photosynthetic eukaryotes. The gray bars represent the standard error of the estimated divergence times at the nodes. The orange bar shows the GOE [Colour figure can be viewed at wileyonlinelibrary.com]
Figure 3 Relaxed molecular clock of Type II reaction center proteins. A log‐normal autocorrelated relaxed clock is shown implementing a CAT + GTR + Γ model with flexible boundaries on the calibration points. Red dots are calibration points as described in Materials and Methods. The gray dot denoted II represents the ancestral Type II reaction center protein, as schematized in Figure 1. The orange dot (D0) marks the initial divergence of D1 and D2. The violet dot marks the divergence point between G2 atypical D1 sequences and standard D1. The green dot marks the divergence point between the microaerobic D1 forms (G3) and the dominant form of D1 (G4). This point represents the last common ancestral protein to all standard D1 forms predating crown group Cyanobacteria. The blue dot represents the origin of the dominant form of D1 inherited by all extant Cyanobacteria and photosynthetic eukaryotes. The gray bars represent the standard error of the estimated divergence times at the nodes. The orange bar shows the GOE [Colour figure can be viewed at wileyonlinelibrary.com]CC BY · PubMed Central
Figure 4 Effect of model selection on estimated divergence times. (a) Divergence times of key nodes in the evolution of Type II reaction centers as a function of the root prior. The root prior was varied from 3.2 to 4.1 ± 0.05 Ga under a CAT + GTR + Γ model. The colored dots match selected nodes of interest in Figure 3. The thick gray bar marks the GOE and the narrow bar marks the minimum accepted age for the origin of photosynthesis. (b) Identical to (a) but using a LG + Γ model of amino acid substitutions. (c) Divergence times of key nodes assuming a root prior of 3.5 Ga as a function of the standard deviation on the root. The standard deviation was varied from 0.025 to 0.4 Ga under a CAT + GTR + Γ model. (d) Identical to (c) but using a LG + Γ model. In every case, D0 is the oldest node after the root and the magnitude of ΔT is always in the range of a billion years [Colour figure can be viewed at wileyonlinelibrary.com]
Figure 4 Effect of model selection on estimated divergence times. (a) Divergence times of key nodes in the evolution of Type II reaction centers as a function of the root prior. The root prior was varied from 3.2 to 4.1 ± 0.05 Ga under a CAT + GTR + Γ model. The colored dots match selected nodes of interest in Figure 3. The thick gray bar marks the GOE and the narrow bar marks the minimum accepted age for the origin of photosynthesis. (b) Identical to (a) but using a LG + Γ model of amino acid substitutions. (c) Divergence times of key nodes assuming a root prior of 3.5 Ga as a function of the standard deviation on the root. The standard deviation was varied from 0.025 to 0.4 Ga under a CAT + GTR + Γ model. (d) Identical to (c) but using a LG + Γ model. In every case, D0 is the oldest node after the root and the magnitude of ΔT is always in the range of a billion years [Colour figure can be viewed at wileyonlinelibrary.com]CC BY · PubMed Central
Figure 5 Rates of evolution as a function of time. (a) Change in the rate of evolution of oxygenic (gray) and anoxygenic (orange) Type II reaction center proteins. The rates correspond to the tree in Figure 3, assuming an origin of photosynthesis at about 3.5 Ga. The dashed lines represent a fit of a single‐component exponential decay and the rates are given as amino acid substitutions per site per million years. (b) Changes in the rate of evolution constraining the root to younger and younger ages. The red curve farthest to the right was calculated using a root prior of 4.2 ± 0.05 Ga, while the green curve farthest to the left was calculated using a root prior of 0.8 ± 0.05 Ga. Younger divergence times imply initial faster rates of evolution. (c) Change in the rate of evolution as a function of ΔT, the dashed lines represent a fit to a power law function. The curve in orange was calculated using ΔT values subtracting the mean average of the divergence times of D0 and the ancestral standard D1. The curve in gray was calculated using ΔT values subtracting the minimum age of D0 and the maximum age for ancestral standard D1 [Colour figure can be viewed at wileyonlinelibrary.com]
Figure 5 Rates of evolution as a function of time. (a) Change in the rate of evolution of oxygenic (gray) and anoxygenic (orange) Type II reaction center proteins. The rates correspond to the tree in Figure 3, assuming an origin of photosynthesis at about 3.5 Ga. The dashed lines represent a fit of a single‐component exponential decay and the rates are given as amino acid substitutions per site per million years. (b) Changes in the rate of evolution constraining the root to younger and younger ages. The red curve farthest to the right was calculated using a root prior of 4.2 ± 0.05 Ga, while the green curve farthest to the left was calculated using a root prior of 0.8 ± 0.05 Ga. Younger divergence times imply initial faster rates of evolution. (c) Change in the rate of evolution as a function of ΔT, the dashed lines represent a fit to a power law function. The curve in orange was calculated using ΔT values subtracting the mean average of the divergence times of D0 and the ancestral standard D1. The curve in gray was calculated using ΔT values subtracting the minimum age of D0 and the maximum age for ancestral standard D1 [Colour figure can be viewed at wileyonlinelibrary.com]CC BY · PubMed Central
Figure 6 Scenarios for the evolution of Type II reaction centers. The rows of colored dots represent estimated divergence times of key nodes as highlighted in Figure 3 and calculated using the CAT + GTR + Γ and LG + Γ models and root priors of 3.8 or 3.5 ± 0.05 Ga. A highly oxidizing photosystem with enough power to split water is likely to have originated before the gene duplication event that led to D1 and D2 (orange dot). Making the MRCA of Cyanobacteria older (green arrow) pushes the earliest stages in the evolution of PSII and water oxidation closer to the origin of photosynthesis (orange arrow). The yellow vertical bar marks the GOE [Colour figure can be viewed at wileyonlinelibrary.com]
Figure 6 Scenarios for the evolution of Type II reaction centers. The rows of colored dots represent estimated divergence times of key nodes as highlighted in Figure 3 and calculated using the CAT + GTR + Γ and LG + Γ models and root priors of 3.8 or 3.5 ± 0.05 Ga. A highly oxidizing photosystem with enough power to split water is likely to have originated before the gene duplication event that led to D1 and D2 (orange dot). Making the MRCA of Cyanobacteria older (green arrow) pushes the earliest stages in the evolution of PSII and water oxidation closer to the origin of photosynthesis (orange arrow). The yellow vertical bar marks the GOE [Colour figure can be viewed at wileyonlinelibrary.com]CC BY · PubMed Central
Figure 7 Structural comparisons of Type II reaction center proteins. (a) Several structural domains are conserved in D1 and D2 but are absent in L and M: These are highlighted in orange. D1 and D2 are plotted from the crystal structure of PSII from Thermosynechococcus vulcanus, PDB: 3WU2 (Umena et al., 2011) and L and M from Thermochromatium tepidum, PDB: 3WMM (Niwa et al., 2014). (b) Overlap of D2 (gray) with M (transparent blue) and D1 (gray) with L (transparent blue). (c) Overlap of D1 (gray) and D2 (orange) highlighting the conserved N‐terminus. (d) Overlap of D1 and D2 highlighting the conserved protein fold between the 1st and 2nd transmembrane helices. (e) D1 is shown in gray and D2 in orange. ChlZD 1, CarD1, W105, and QB are shown in gray sticks. ChlZD 2, CarD2, W104, and QA are shown in orange sticks. (f) Overlap of D1 and D2 highlighting the conserved protein fold where the bicarbonate binding site is placed. (g) Overlap of D1 and D2 highlighting the conserved protein fold at the C‐terminus. (h) The Mn4CaO5 cluster coordination sphere and the equivalent location in D2. (i) Perspective view showing the interaction of CP47 and CP43 with the electron donor side of D2 and D1, respectively. The structural homology of CP43 and CP47 indicates that these originated from a gene duplication event making the homodimeric antenna to a homodimeric core (Cardona, 2016). The reason why CP47, and in particular CP43, interact with the donor side of PSII is an unsolved mystery given the fact that their main role is that of light harvesting. It can be rationalized however if water oxidation started in a homodimeric reaction center early during the evolution of photosynthesis (Cardona, 2017) [Colour figure can be viewed at wileyonlinelibrary.com]
Figure 7 Structural comparisons of Type II reaction center proteins. (a) Several structural domains are conserved in D1 and D2 but are absent in L and M: These are highlighted in orange. D1 and D2 are plotted from the crystal structure of PSII from Thermosynechococcus vulcanus, PDB: 3WU2 (Umena et al., 2011) and L and M from Thermochromatium tepidum, PDB: 3WMM (Niwa et al., 2014). (b) Overlap of D2 (gray) with M (transparent blue) and D1 (gray) with L (transparent blue). (c) Overlap of D1 (gray) and D2 (orange) highlighting the conserved N‐terminus. (d) Overlap of D1 and D2 highlighting the conserved protein fold between the 1st and 2nd transmembrane helices. (e) D1 is shown in gray and D2 in orange. ChlZD 1, CarD1, W105, and QB are shown in gray sticks. ChlZD 2, CarD2, W104, and QA are shown in orange sticks. (f) Overlap of D1 and D2 highlighting the conserved protein fold where the bicarbonate binding site is placed. (g) Overlap of D1 and D2 highlighting the conserved protein fold at the C‐terminus. (h) The Mn4CaO5 cluster coordination sphere and the equivalent location in D2. (i) Perspective view showing the interaction of CP47 and CP43 with the electron donor side of D2 and D1, respectively. The structural homology of CP43 and CP47 indicates that these originated from a gene duplication event making the homodimeric antenna to a homodimeric core (Cardona, 2016). The reason why CP47, and in particular CP43, interact with the donor side of PSII is an unsolved mystery given the fact that their main role is that of light harvesting. It can be rationalized however if water oxidation started in a homodimeric reaction center early during the evolution of photosynthesis (Cardona, 2017) [Colour figure can be viewed at wileyonlinelibrary.com]CC BY · PubMed Central
Figure 8 Carotenoids in the reaction center core. (a) Overlap of the M subunit of the anoxygenic Type II reaction center from Thermochromatium tepidum (light blue) with the D2 subunit of PSII from Thermosynechococcus vulcanus (gray) and the PshA subunit of the homodimeric Type I reaction center of Heliobacterium modesticaldum (orange), PDB ID: 5v8k (Gisriel et al., 2017). The protein backbone is showed in transparent ribbons, some of the photochemical pigments are displayed as thin sticks, and the closest carotenoids to the core are shown as thick sticks. SX stands for spirilloxanthin and DN for 4,4′‐diaponeurosporene. CarD2 is the core beta‐carotene bound by D2. Both SX and CarD2 have been demonstrated to have photoprotective roles, while the role of DN in the homodimeric Type I reaction center has not been demonstrated yet. However, based on its structural position overlapping with half of CarD2 and in Van der Waals contact with several bacteriochlorophyll g molecules, it can be predicted that it also has a photoprotective role. P denotes the photochemical “special pair” pigments. (b) A rotated view of the position of the carotenoids in the overlapped structures. The protein backbone has been hidden for clarity. ChlZD 2 and the bacteriochlorophyll g molecule, GBF 1024, occupy homologous positions [Colour figure can be viewed at wileyonlinelibrary.com]
Figure 8 Carotenoids in the reaction center core. (a) Overlap of the M subunit of the anoxygenic Type II reaction center from Thermochromatium tepidum (light blue) with the D2 subunit of PSII from Thermosynechococcus vulcanus (gray) and the PshA subunit of the homodimeric Type I reaction center of Heliobacterium modesticaldum (orange), PDB ID: 5v8k (Gisriel et al., 2017). The protein backbone is showed in transparent ribbons, some of the photochemical pigments are displayed as thin sticks, and the closest carotenoids to the core are shown as thick sticks. SX stands for spirilloxanthin and DN for 4,4′‐diaponeurosporene. CarD2 is the core beta‐carotene bound by D2. Both SX and CarD2 have been demonstrated to have photoprotective roles, while the role of DN in the homodimeric Type I reaction center has not been demonstrated yet. However, based on its structural position overlapping with half of CarD2 and in Van der Waals contact with several bacteriochlorophyll g molecules, it can be predicted that it also has a photoprotective role. P denotes the photochemical “special pair” pigments. (b) A rotated view of the position of the carotenoids in the overlapped structures. The protein backbone has been hidden for clarity. ChlZD 2 and the bacteriochlorophyll g molecule, GBF 1024, occupy homologous positions [Colour figure can be viewed at wileyonlinelibrary.com]CC BY · PubMed Central

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Metadata

Authors
Cardona, T., Sánchez‐Baracaldo, P., Rutherford, A. W., & Larkum, A. W.
Affiliations
  • Imperial College London (GB)
  • University of Bristol (GB)
  • University of Technology Sydney (AU)
Corresponding author
Cardona, Tanai
ORCID
Venue
Geobiology
Publisher
Wiley
Published
2018-11-09
Volume
17
Issue
2
Pages
127-150
ISSN
  • 1472-4669 (ISSN-L)
  • 1472-4677
DOI
10.1111/gbi.12322
PMC
PMC6492235
OpenAlex
W2900344826
Cited by
144
References
168
Citations by year
2026: 12 · 2025: 21 · 2024: 23 · 2023: 13 · 2022: 22 · 2021: 17 · 2020: 14 · 2019: 18 · 2018: 4
FWCI
4.69
Type
journal article
Language
en
Open access
Licence
Locations
  • Geobiology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Bristol Research (University of Bristol) (publishedVersion, cc-by)
  • UTS ePRESS (University of Technology Sydney) (submittedVersion)
  • Spiral (Imperial College London) (submittedVersion, other-oa)
Funders
  • Imperial College London
  • Leverhulme Trust (RPG‐2017‐223)
  • Royal Society
  • Biotechnology and Biological Sciences Research Council (BB/K002627/1, BB/L011206/1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Metalloenzymes and iron-sulfur proteins
Keywords
photosystem II, water oxidation, oxygenic photosynthesis, Archean, evolution of photosynthesis, cyanobacteria, anoxygenic photosynthetic bacteria, reaction center proteins, reactive oxygen species, eukaryotic origin
MeSH terms
Cyanobacteria, Bacterial Proteins, Bayes Theorem, Photosynthesis, Phylogeny, Evolution, Molecular, Photosystem II Protein Complex

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