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. 2023 Feb 7;62(4):934–941. doi: 10.1021/acs.biochem.2c00689

Energetic Diversity in the Electron-Transfer Pathways of Type I Photosynthetic Reaction Centers

Tomoki Kanda †, Hiroshi Ishikita †,‡,*
PMCID: PMC9949227  PMID: 36749324

Abstract

graphic file with name bi2c00689_0007.jpg

Photosynthetic reaction centers from heliobacteria (HbRC) and green sulfur bacteria (GsbRC) are homodimeric proteins and share a common ancestor with photosystem I (PSI), classified as type I reaction centers. Using the HbRC crystal structure, we calculated the redox potential (Em) values in the electron-transfer branches, solving the linear Poisson–Boltzmann equation and considering the protonation states of all titratable sites in the entire protein–pigment complex. Em(A–1) for bacteriochlorophyll g at the secondary site in HbRC (−1157 mV) is as low as Em(A–1) for chlorophyll a in PSI (−1173 mV). Em(A0/HbRC) is at the same level as Em(A0/GsbRC) and is 200 mV higher than Em(A0/PSI) due to the replacement of PsaA-Trp697/PsaB-Trp677 in PSI with PshA-Arg554 in HbRC. In contrast, Em(FX) for the Fe4S4 cluster in HbRC (−420 mV) is significantly higher than Em(FX) in GsbRC (−719 mV) and PSI (−705 mV) due to the absence of acidic residues that correspond to PscA-Asp634 in GsbRC and PsaB-Asp575 in PSI. It seems likely that type I reaction centers have evolved, adopting (bacterio)chlorophylls suitable for their light environments while maintaining electron-transfer cascades.

Introduction

In photosynthesis, type I reaction centers use Fe4S4 clusters as terminal electron acceptors and type II reaction centers use quinones. Photosystem I (PSI) is a type I reaction center. In the heterodimeric PsaA/PsaB reaction center of PSI, a pair of chlorophyll a epimer (Chla′)/chlorophyll a (Chla), PA/PB, accessory Chla, A–1A/A–1B (nomenclature widely used in, e.g., refs (1−4) or eC-B2/eC-A2 used in ref (5)), electron acceptor Chla, A0A/A0B, and phylloquinone, A1A/A1B, form two electron-transfer branches, which merge at an Fe4S4 cluster, FX. Photosynthetic reaction centers from heliobacteria (HbRC) and green sulfur bacteria (GsbRC) are also type I reaction centers. In contrast to PSI, HbRC and GsbRC form homodimeric reaction centers, the PshA/PshA and PscA/PscA proteins, respectively6,7 (Figure 1). Furthermore, quinone molecules, which are present at A1 in the PSI structures,5,8 are not observed in the HbRC9 and GsbRC10 structures. Nevertheless, the HbRC and GsbRC structures exhibit several notable differences. HbRC has the bacteriochlorophyll g epimer (BChlg′) for P, bacteriochlorophyll g (BChlg) for A–1, and 81-hydroxychlorophyll a (81-OH-ChlaF) for A0, whereas GsbRC has the bacteriochlorophyll a epimer (BChla′) for P and Chla for A–1 and A0. To the best of our knowledge, neither the redox potential (Em) value for A–1 in HbRC (Em(A–1/HbRC)) nor Em(BChlg) in solvents has been reported. The experimentally estimated Em(A0/HbRC) value is −854 mV,11 whereas Em(81-OH-ChlaF) is not reported. Thus, it remains unclear how the protein environment interacts with these cofactors in HbRC.

Figure 1.

Figure 1

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Electron-transfer chains in the homodimeric reaction centers of HbRC (PDB code 5V8K).9 Arrows indicate electron transfer. The two identical PshA proteins are colored red and blue for clarity.

The membrane-extrinsic PscB protein subunit adjacent to the PscA/PscA reaction center has two Fe4S4 clusters, FA and FB, in GsbRC,10 as does the PsaC protein subunit adjacent to the PsaA/PsaB reaction center in PSI. However, the corresponding membrane-extrinsic protein subunit is not observed in the HbRC structure.9 The absence of a tightly bound membrane-extrinsic protein subunit may be associated with the Em(FX/HbRC) value of −440 to −510 mV,11−13 which is ∼200 mV higher than those of Em(FX/GsbRC)14,15 and Em(FX/PSI).16−19 However, the loss of the PsaC protein subunit leads to an increase of only 40 mV in Em(FX/PSI),20 which does not sufficiently account for the high Em(FX/HbRC) value. HbRC forms a linage that is sister to a larger group that includes GsbRC and reaction centers from Chloracidobacterium thermophilum (CabRC) and Chloroflexi bacterium (CfxRC),21 which implies that the difference in the amino acid sequence is responsible for the Em difference between HbRC and GsbRC.

Here, we investigated the HbRC protein environment that interacts with redox-active cofactors and shifts their Em values by solving the linear Poisson–Boltzmann equation and considering the protonation states of all titratable sites in the entire protein–pigment complex.

Methods

Coordinates and Atomic Partial Charges

The atomic coordinates were taken from the X-ray structure of HbRC from Heliobacterium modesticaldum (PDB code, 5V8K).9 Hydrogen atoms were generated and energetically optimized with CHARMM.22 Atomic partial charges of the amino acids were adopted from the all-atom CHARMM2223 parameter set. The atomic charges of BChlg, 81-OH-ChlaF, 4,4′-diaponeurosporene (C4D), and 1-[glycerolylphosphonyl]-2-[8-(2-hexyl-cyclopropyl)-octanal-1-yl]-3-[hexadecanal-1-yl]-glycerol (DGG) were determined by fitting the electrostatic potential in the neighborhood of these molecules using the RESP procedure24 (Tables S1–S3). The atomic charges of BChlg were used for the atomic charges of BChlg′. The electronic densities were calculated after geometry optimization by the density functional theory (DFT) method with the B3LYP functional and LACVP* basis sets using the JAGUAR program.25 For the atomic charges of the nonpolar CHn groups in cofactors (e.g., the phytol chains of BChlg), a value of +0.09 was assigned for nonpolar H atoms.

The cavity spaces were represented implicitly with a dielectric constant of 80, whereas the following water molecules were represented explicitly: ligand water molecules of A–1 (A1276), A0 (A1193), and other BChlg (A1111, A1124, and A1125).

Em Calculation: Solving the Linear Poisson–Boltzmann Equation

To obtain the Em values in the proteins, we calculated the Em shift (ΔEm) between the protein environment and the reference system by solving the linear Poisson–Boltzmann equation with the MEAD program.26 The Em value in the protein environment was obtained by adding ΔEm to the Em value for (bacterio)chlorophyll in a model system (see below). The ensemble of protonation patterns was sampled using the Monte Carlo method with Karlsberg.27 Each Monte Carlo scan changed the protonation states of all titratable sites. The initial protonation pattern was obtained by performing 10,000 Monte Carlo scans. Fully protonated/deprotonated sites were excluded from further Monte Carlo scans. For the remaining sites, the protonation pattern was obtained by performing another 100,000 scans. The linear Poisson–Boltzmann equation was solved using a three-step grid-focusing procedure at resolutions of 2.5, 1.0, and 0.3 Å. Monte Carlo sampling yielded the probabilities [Aox] and [Ared] of the two redox states of molecule A. Em was evaluated using the Nernst equation. A bias potential was applied to obtain an equal amount of both redox states ([Aox] = [Ared]), thereby yielding the redox midpoint potential as the resulting bias potential. All computations were performed at 300 K, pH 7.0, and an ionic strength of 100 mM. The dielectric constants were set to 4 for the protein interior and 80 for water.28,29

Em values for (bacterio)chlorophyll and metal-complex cofactors can also be calculated using a quantum mechanical/molecular mechanical (QM/MM) approach.30,31 In the present study, the Em values were reported, solving the linear Poisson–Boltzmann equation to facilitate direct comparisons with previous reports for PSI1,20,32,33 and GsbRC.15

Reference Em Values of (Bacterio)chlorophylls

In HbRC, P is BChlg′, A–1 is BChlg, and A0 is 81-OH-ChlaF. To the best of our knowledge, the reference Em values for BChlg and BChlg′ are not reported (refs (34, 35)). As the experimentally measured Em(P/P•+) value is 225 mV12 and the absorption energy at 800 nm is 1550 meV, Em(P/P•–) is estimated to be −1325 mV. To reproduce Em(P/P•–) = −1325 mV in the HbRC protein environment, Em(BChlg′) was estimated to be −1028 mV in water by solving the Poisson–Boltzmann equation in the present study. Assuming that Em(BChlg′) ≈ Em(BChlg), Em(BChlg) = −1028 mV was used to calculate Em(A–1/HbRC). As Em(A0/HbRC) was experimentally estimated to be −854 mV,11Em(81-OH-ChlaF) was estimated to be −1024 mV in water by solving the Poisson–Boltzmann equation in the present study. FX binds to four cysteine residues from two identical sequences of PshA/PshA in HbRC, PscA/PscA in GsbRC, and PsaA/PsaB in PSI. Thus, Em(Fe4S4) = −428 mV in water was used for FX in HbRC, as used for FX in GsbRC and PSI.15

Results and Discussion

Em(A0/HbRC) was experimentally estimated to be −854 mV.11 The Em value is as high as Em(A0/GsbRC) (−800 mV15) but ∼200 mV higher than Em(A0/PSI) (−1050 mV36,38,39), which suggests that the high Em(A0) values are a feature of homodimeric reaction centers (Figure 2).

Figure 2.

Figure 2

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Em for one-electron reduction in the electron-transfer chains in type I reaction centers. (a) HbRC, (b) GsbRC,15 and (c) PSI.33,36 The experimentally estimated values are shown for Em(A0/HbRC) (−854 mV11) and Em(FX/PSI) (−705 mV16).

Nevertheless, the influence of the HbRC protein environment on Em(A0/HbRC) differs significantly from the influence of the GsbRC protein environment on Em(A0/GsbRC). The Em value of 81-OH-ChlaF, which is used for A0 in HbRC, is ∼230 mV lower than the Em value of Chla, which is used for A0 in GsbRC (Table 1). Based on the calculated Em shift of 170 mV from water to the HbRC protein environment, Em(81-OH-ChlaF) can be estimated to be −1024 mV in water (Table 1). The result suggests that the protein environment increases Em(81-OH-ChlaF) more significantly at A0 in HbRC than Em(Chla) at A0 in GsbRC (Table 1). In GsbRC, PscA-Asp634 contributes to a decrease of 217 mV in Em(A0/GsbRC)15 (Table 2). However, PscA-Asp634 in GsbRC is replaced with charge-neutral PshA-Tyr550 in HbRC (Figure 3). Thus, the HbRC protein environment increases Em(A0/HbRC) more significantly than the GsbRC protein environment does Em(A0/GsbRC), which eventually overcomes the difference between Em(81-OH-ChlaF) (−1024 mV) and Em(Chla) (−798 mV) and leads to Em(A0/HbRC) ≈ Em(A0/GsbRC) (Figure 3).

Table 1. Em Values of (Bacterio)chlorophyll Cofactors in Type I Reaction Centers and Shifts Caused by the Protein Atomic Charges and Loss of Solvation in mVa.

  HbRC
 GsbRCb
 PSIc
  P A–1 A0 P A–1 A0 PA A–1A A0A
  BChlg′ BChlg 81-OH-ChlaF BChla′ Chla Chla Chla′ Chla Chla
Em in protein –1325 –1157 –854d –1167b –1077b –798b –1264c –1173c –1049c
                   
Em in water –1028 –1028 –1024 –641c –798c –798c –798c –798c –798c
                   
Em shift –297 –129 170 –526 –279 0 –466 –375 –251
protein charge –47 123 386 –290 –42 129 –209 –102 18
solvation loss –250 –252 –216 –236 –237 –129 –256 –273 –268
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a

In PSI, the values in the A branch are shown for clarity.

b

See ref (15).

c

See ref (36).

d

See ref (11).

Table 2. Residues That Increase Em(A0/HbRC) with Respect to Em(A0/GsbRC) by More Than 50 mVa.

HbRC
 GsbRC
 difference
PshA   PshA(2)   PscA   PscA(2)    
Tyr550 –17 Tyr550 5 Asp634 –217 Asp634 –27 232
Arg554 197 Arg554 38 Arg638 120 Arg638 16 99
Lys425 12 Lys425 69 Asn521 0 Asn521 1 80
Arg406 19 Arg406 221 Arg502 8 Arg502 173 59
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a

PshA(2) and PscA(2) are the PshA and PscA subunits to which the focusing A0 molecules do not belong.

Figure 3.

Figure 3

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A0 binding site. (a) HbRC and (b) GsbRC. Dotted lines indicate H-bonds. Numerical values indicate H-bond distances in Å. Residues that significantly increase and decrease Em(A0) are labeled in blue and red, respectively.

Two arginine residues, PshA-Arg406 and PshA-Arg554, near A0 in HbRC contribute to increases in Em(A0/HbRC) (Table 2). They are conserved as PscA-Arg502 and PscA-Arg638 in GsbRC (Figure 3). In GsbRC, PscA-Arg502 also increases Em(A0/GsbRC) most significantly.15 PscA-Arg638 not only serves as a binding site of a phosphatidylglycerol molecule21 but also increases Em(A0/GsbRC) with respect to Em(A0/PSI).15 The phosphatidylglycerol molecule might be menaquinone before the purification process.40 From the analogy, it seems possible that PshA-Arg554 serves as a binding site of a phospholipid molecule in HbRC (see below).

However, PshA-Arg554 in HbRC is replaced with PsaA-Trp697 in PSI (Table 3). Thus, Em(A0/PSI) (−1050 mV36,38,39) is 200–250 mV lower than Em(A0/HbRC) and Em(A0/GsbRC)15 (Figure 2). In PSI, PsaA-Trp697 and PsaB-Trp677 form quinone binding sites A1A and A1B, respectively.5 It seems likely that the absence of quinone binding sites (i.e., tryptophan) in HbRC and GsbRC ultimately contributes to the upshift of Em(A0/HbRC) and Em(A0/GsbRC) with respect to Em(A0/PSI).

Table 3. Residues That Increase Em(A0/HbRC) with Respect to Em(A0A/PSI) by More Than 50 mVa.

HbRC
 PSI
 difference
PshA   PshA(2)   PsaA   PsaB    
Arg554 197 Arg554 38 Trp697 8 Trp677 3 224
Ser442 1 Ser442 –5 Gln588 4 Asp575 –172 163
Met559 4 Met559 0 Glu702 –60 Glu682 –16 80
Phe410 0 Phe410 1 Phe559 0 Asp546 –79 80
Lys425 12 Lys425 69 Asn571 1 Asp558 1 79
Asp447 –36 Asp447 –91 Asp593 –61 Asp580 –121 54
Cys316 0 Cys316 –1 Asp438 –12 Glu419 –43 54
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a

PshA(2) is the PshA subunit to which the focusing A0 molecule does not belong.

Although PshA-Arg554 in HbRC is conserved as PscA-Arg638 in GsbRC, the contribution of PshA-Arg554 to Em(A0/HbRC) is ∼100 mV larger than that of PscA-Arg638 in GsbRC (Table 2). This is due to the significant difference in the hydrophobicity of the protein environment near A0 between HbRC and GsbRC. The loss of solvation of A0 in HbRC decreases Em(A0/HbRC) by 216 mV, whereas that in GsbRC decreases Em(A0/GsbRC) by only 129 mV (Table 1). Thus, the electrostatic interaction between A0 and arginine is more shielded and weaker in GsbRC than in HbRC. That is, the decrease in Em(A0/HbRC) upon the binding of a phospholipid molecule at PshA-Arg554 will be larger than the decrease in Em(A0/GsbRC) upon the binding of a phospholipid molecule at PscA-Arg638. The difference in the hydrophobicity of the protein environment near A0 between HbRC and GsbRC is also responsible for the difference of ∼60 mV in the contributions of PshA-Arg406 and PscA-Arg502 to Em(A0/HbRC) and Em(A0/GsbRC) (Table 2).

The replacement of PscA-Asp634 in GsbRC with PshA-Tyr550 in HbRC also contributes to an increase in Em(A–1/HbRC) with respect to Em(A–1/GsbRC). However, Em(BChlg) (−1028 mV, Table 1) is 230 mV lower than Em(Chla) (−798 mV36). Thus, Em(A–1/HbRC) (−1157 mV) is ∼80 mV lower than Em(A–1/GsbRC) (−1077 mV) (Figure 2, Table 1). To the best of our knowledge, Em(BChlg) and Em(81-OH-ChlaF) have not been reported. The present study suggests that Em(BChlg) is almost the same as Em(81-OH-ChlaF) (Table 1). Although A–1 and A0 in the HbRC are distinct (bacterio)chlorophyll types, their Em values are similar, and their roles in electron transfer are therefore conserved among type I reaction centers.

The Em(FX/HbRC) value calculated using the HbRC crystal structure9 is remarkably high (−420 mV) with respect to Em(FX/GsbRC) and Em(FX/PSI) (Figure 2, Table 4). The result is in line with significantly high experimentally estimated Em(FX/HbRC) values of −440,13 −504,11 and −510 mV.12 The Em(FX/HbRC) value of −504 mV11 is a consensus value determined from four independent techniques. The value of −510 mV12 was determined by loss of P•+ formation, which is close to the Em(FX/HbRC) value of −504 mV.11 In contrast, the Em(FX/HbRC) value of −440 mV13 may be an outlier, as it was indirectly derived from the triplet state of the reaction center. The discrepancy of ∼60 mV between the experimentally measured11,12 and calculated Em values is likely to originate from the difference in the protein structure near FX between the HbRC crystal structure and the actual HbRC structure used for the measurements (e.g., the PshB protein, see below).

Table 4. Em Values of FX in Type I Reaction Centers and Shifts Caused by the Protein Atomic Charges and Loss of Solvation in mVa.

  HbRC GsbRCb PSIb
  FX FX FX
  Fe4S4 Fe4S4 Fe4S4
Em in protein –420 –719b –705c
       
Em in water –428 –428b –428b
       
Em shift 8 –291 –277
protein charge 1156 1057 1092
solvation loss –1149 –1348 –1369
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a

The experimentally measured Em(FX/HbRC) values were −50411 and −510 mV.12 A more positive value of −440 mV was obtained from the triplet state of the reaction center.13

b

See ref (15).

c

See ref (16).

The electrostatic difference between PshA-Tyr550 in HbRC and PscA-Asp634 in GsbRC is more pronounced at FX (288 mV, Table 5) than at A0 (232 mV, Table 2). The replacement of PscA-Asp634 in GsbRC with PshA-Tyr550 in HbRC is the most crucial factor for the high Em(FX/HbRC) value (Table 5). PscA-Asp634 is genetically not conserved since it is replaced with PsaA-Gly693 and PsaB-Trp673 in PSI. As PsaB-Trp673 is required for efficient electron transfer from A1 to FX in PSI,41 the loss of the corresponding tryptophan residue may suggest that electron transfer to FX is unlikely to be mediated by quinone in GsbRC.

Table 5. Residues That Increase Em(FX/HbRC) with Respect to Em(FX/GsbRC) by More Than 50 mVa.

HbRC
 GsbRC
 difference
PshA   PshA(2)   PscA   PscA(2)    
Tyr550 13 Tyr550 13 Asp634 –131 Asp634 –131 288
Lys425 58 Lys425 58 Asn521 5 Asn521 5 105
Lys584 24 Lys584 24 Ser671 –11 Ser671 –11 71
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a

PshA(2) and PscA(2) are the PshA and PscA subunits to which the focusing A0 molecules do not belong.

Nevertheless, PscA-Asp634 in GsbRC is likely to be functionally conserved as PsaB-Asp575 in PSI.1 ,32 The uptake of 1 H+ by PscA-Asp634 upon A0•– formation in GsbRC15 resembles the uptake of 0.4–0.5 H+ by PsaB-Asp575 upon A1A•– formation in PSI.1,33 The uptake of 0.4 H+ by PscA-Asp634 was also observed in response to FX– formation in GsbRC, which suggests that its protonation state is coupled with the redox state of FX in GsbRC.15 However, the present study shows that no proton uptake is observed in response to the formation of A0•– and FX– in HbRC. The absence of a PscA-Asp634-like residue in HbRC can partially explain why Em(FX/HbRC) is specifically higher than Em(FX/GsbRC) and Em(FX/PSI).

The HbRC crystal structure does not have the PshB protein.9 The PshB protein (e.g., PshB1 and PshB2), which was previously considered to be an analogue of the PsaC protein in PSI, serves as a ferredoxin-like protein.42 In PSI, the loss of the PsaC protein leads to an increase of 42 mV in Em(FX/PSI).20 From the analogy, Em(FX/HbRC) would be lower in the presence of the PshB1 protein, which is in line with the experimentally estimated Em(FX/HbRC) value of −504 mV.11

Conclusions

Em(A0/HbRC) and Em(A0/GsbRC) are 200–250 mV higher than Em(A0/PSI) (Table 1, Figure 2), which is likely a common feature of homodimeric reaction centers. PshA-Arg406 and PshA-Arg554 in HbRC are conserved as PscA-Arg502 and PscA-Arg638 in GsbRC. These two arginine residues commonly increase Em(A–1) and Em(A0) in HbRC and GsbRC (Table 2, Figure 4). PshA-Arg406 in HbRC is also conserved as PsaB-Lys542 in PSI. However, PshA-Arg554 in HbRC is replaced with PsaA-Trp697/PsaB-Trp677 in PSI, forming the A1 quinone binding sites.5,8 The presence of PshA-Arg554 in HbRC and PscA-Arg638 in GsbRC is disadvantageous for quinone binding but contributes to upshifts of Em(A0/HbRC) and Em(A0/GsbRC), thereby increasing the driving force between A–1 and A0. The large energy gap may be a prerequisite for homodimeric reaction centers to inhibit backward electron transfer and facilitate charge separation. The absence of the A1 quinone in these homodimeric reaction centers is disadvantageous in terms of the electronic coupling between A0 and the electron acceptor (FX) (although the A0···FX distance is ∼4 Å shorter in HbRC than in PSI43), but the presence of the arginine residue is advantageous for the driving force for electron transfer from the electron donor (A–1) to A0, eventually contributing to charge separation in a manner distinct from PSI.

Figure 4.

Figure 4

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Conserved residues that differentiate Em values most significantly among the three type I reaction centers. (a) Em(A–1) and Em(A0) and (b) Em(FX). PshA(2) and PscA(2) are the PshA and PscA subunits to which the focusing A0 molecules do not belong. Solid and dotted horizontal bars indicate Em values in proteins and water, respectively. Blue and red labels indicate residues that upshift and downshift the Em values, respectively. The values in brackets indicate Em shifts in mV units.

In contrast, Em(FX/HbRC) is ∼200 mV higher than Em(FX/GsbRC) and Em(FX/PSI) (Table 1, Figure 2), predominantly due to the absence of acidic residues that correspond to PscA-Asp63415 in GsbRC and PsaB-Asp5751,32,33 in PSI (Figure 4). The loss of the PshB1 protein in the HbRC crystal structure may partially be responsible for the calculated high Em(FX/HbRC) value. The PshB1 protein in HbRC is quite different from the PscB protein in GsbRC and the PsaC protein in PSI, as it may serve as a mobile ferredoxin protein,42 which is likely the origin of the significant difference in Em(FX) between the two homodimeric reaction centers.

PshA-Arg406 in HbRC is fully conserved among GsbRC (PscA-Arg502), CfxRC (PscA-Arg392), and CabRC (PscA-Arg671). PshA-Arg554 in HbRC is also fully conserved among GsbRC (PscA-Arg638), CfxRC (PscA-Arg523), and CabRC (PscA-Arg801). The difference between PshA-Tyr550 and PscA-Asp634 is the most significant difference in Em(A–1), Em(A0), and Em(FX) between HbRC and GsbRC (Figure 4). Remarkably, CfxRC has PscA-Tyr519, whereas CabRC has PscA-Asp797. Thus, the protein electrostatic environment of CfxRC resembles that of HbRC, whereas that of CabRC resembles that of GsbRC. It seems possible that the Em profile of CfxRC may be similar to that of HbRC (e.g., high Em(FX)), whereas that of CabRC may be similar to that of GsbRC (e.g., low Em(FX)).

Overall, none of the three type I reaction centers share the same Em profile. Em(A–1/HbRC) is similar to Em(A–1/PSI) (Figure 5). However, the contributions of the protein environment to Em(A–1/HbRC) and Em(A–1/PSI) differ, as Em(BChlg) (−1028 mV) and Em(Chla) (−798 mV) originally differ by ∼200 mV (Table 1). Em(A–1/GsbRC) is similar to Em(A0/PSI). Em(A0/HbRC) and Em(A0/GsbRC) are at the same level, 200–250 mV higher than Em(A0/PSI). In contrast, only Em(FX/HbRC) is significantly high, whereas Em(FX/GsbRC) and Em(FX/PSI) are at the same level. HbRC and GsbRC exhibit different Em profiles irrespective of the two reaction centers being classified into homodimeric reaction centers, as their (bacterio)chlorophyll molecules are already distinct (Figure 5). The present study suggests that the ancestral homodimeric reaction center diverged into modern homodimeric reaction centers, including HbRC and GsbRC,21,40 adopting (bacterio)chlorophylls suitable for their light environments while simultaneously maintaining essential electron-transfer cascades.

Figure 5.

Figure 5

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Energetic diversity in the electron-transfer pathways of type I reaction centers. Horizontal bands (yellow, orange, pink, cyan, and purple) indicate groups at the same Em levels. Solid and dotted horizontal bars indicate Em values (mV) in proteins and water, respectively. Red, blue, and black arrows indicate similar driving forces for electron transfer.

Acknowledgments

This research was supported by JSPS KAKENHI (JP20H03217 and JP20H05090 to H.I.) and Interdisciplinary Computational Science Program in CCS, University of Tsukuba.

Supporting Information Available

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.biochem.2c00689.

  • Atomic partial charges of BChlg, 81-OH-ChlaF, 4,4′-diaponeurosporene, and 1-[glycerolylphosphonyl]-2-[8-(2-hexyl-cyclopropyl)-octanal-1-yl]-3-[hexadecanal-1-yl]-glycerol (PDF)

The authors declare no competing financial interest.

Supplementary Material

bi2c00689_si_001.pdf (151.7KB, pdf)

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