Photosynthetic Production of Molecular Oxygen by Water Oxidation

Round 1

Reviewer 1 Report

 

The review manuscript by Lars Olof Björn provides a summary of our present understanding of light-driven O2-generation through what is called oxygenic photosynthesis. The ms is concise and well-written and contains very good illustrations. The mechanistic and structural infos are up-to-date. I therefore consider this ms as perfectly suited for MDPI Oxygen after a few relatively minor revisions.

 

- I have some difficulties with the term OEC as used in this ms. Historically, the OEC is the “oxygen-evolving-complex”, considered to be made up by a set of proteins associated to the photochemical reaction centre. Although suspected since quite some time, at least since the first moderate-solution crystal structures we know that the manganese cluster is situated within the D1-protein, that is, is an integral part of the photochemical reaction centre (as in your Fig. 4) rather than harboured by some of the extrinsic proteins. Those colleagues continuing to use the OEC terminology therefore now use the term as the abbreviation of the “oxygen-evolving-cluster”. While this is also the implicit usage in this ms, there are cases where the OEC-protein resurfaces (e.g. line 209). This distinction might be dismissed as pedantic, if it were not messing up the evolutionary infos given in the last paragraph (lines 230-249). This paragraph is out-of-date and refers to scenarios which are now obsolete. For example, the proposal that the OEC shares similarity to manganese catalase doesn’t make sense anymore in the light of the 3D-information. However, more recent evolutionary scenarios building on the present structural data are not cited (e.g. Chernev et al, Nature Communications 2020, doi.org/10.1038/s41467-020-19852-0).

- line 97: shouldn’t that refer to Fig. 3 rather Fig. 1?

- line 176: with ?? of p-benzoquinone

Author Response

The review manuscript by Lars Olof Björn provides a summary of our present understanding of light-driven O2-generation through what is called oxygenic photosynthesis. The ms is concise and well-written and contains very good illustrations. The mechanistic and structural infos are up-to-date. I therefore consider this ms as perfectly suited for MDPI Oxygen after a few relatively minor revisions.

 

- I have some difficulties with the term OEC as used in this ms. Historically, the OEC is the “oxygen-evolving-complex”, considered to be made up by a set of proteins associated to the photochemical reaction centre. Although suspected since quite some time, at least since the first moderate-solution crystal structures we know that the manganese cluster is situated within the D1-protein, that is, is an integral part of the photochemical reaction centre (as in your Fig. 4) rather than harboured by some of the extrinsic proteins. Those colleagues continuing to use the OEC terminology therefore now use the term as the abbreviation of the “oxygen-evolving-cluster”. While this is also the implicit usage in this ms, there are cases where the OEC-protein resurfaces (e.g. line 209). This distinction might be dismissed as pedantic, if it were not messing up the evolutionary infos given in the last paragraph (lines 230-249). This paragraph is out-of-date and refers to scenarios which are now obsolete. For example, the proposal that the OEC shares similarity to manganese catalase doesn’t make sense anymore in the light of the 3D-information. However, more recent evolutionary scenarios building on the present structural data are not cited (e.g. Chernev et al, Nature Communications 2020, doi.org/10.1038/s41467-020-19852-0).

Response: The «oxygen-evolving center (OEC)» line 72  (line 94 in the current version) should be «oxygen-evolving complex OEC» or «oxygen-evolving cluster OEC», Since I have used «oxygen-evolving complex» on lines 11, 107, and 191 I should use that here, too. On line 20 (keyword list» the term should also have a hyphen, for consistency. Note that Ref. 36 in the current version of my ms (Yao et al. 2021) recently used «oxygen-evolving center» in this sense. I discovered that on line  83 in the current version I used «Mn₄CaO₅ cluster»; it would be OK with me to change this to  «Mn₄CaO₅ complex» if anybody would prefer this; for me it does not matter which.

            I have deleted the passage dealing with catalase, and inserted a passage referring to Chernev et al. (2020).

 

- line 97: shouldn’t that refer to Fig. 3 rather Fig. 1?  It should, in fact, be «Fig. 2».

 

- line 176: with ?? of p-benzoquinone

«Hill reaction with ns of p-benzoquinone »should be «Hill reaction with p-benzoquinone».

Reviewer 2 Report

This review discussed the evolution, assembly, and possible mechanism of the O=O bond formation, as well as the functional role of each component (including manganese, calcium, chloride, bicarbonate) in the OEC. This topic is interesting for researchers in the field of photosynthesis. However, since the knowledge of the OEC in the field has been grown very rapidly during the last decade, some ‘old’ opinions related to the functional roles of bicarbonate, chloride, and calcium probably need to be corrected or reconsidered based on new findings. Meanwhile, the mechanism for the oxygen-evolution and the assembly of OEC remain largely unsolved, which are still under hot debate. Herein, I would like to suggest the author consider following points.

i)                 The chloride ion has been long considered to be a key component of the OEC, however, recently crystal studies of PSII have demonstrated that it is located outside of the OEC and not directly bound to the Mn4CaO5-cluster. Thus, it is more reasonable to state that the chloride ion could not be an essential component of the oxygen-evolving complex although it may play roles for the delivery of proton and/or substrate water during the catalytic reaction. Thus, I suggest removing the “one chloride ion” from the abstract (line 13 in page 1).

ii)               The opinion of the contribution of bicarbonate to OEC is fully questionable since most recent crystal studies (e.g. Nature, 2011, 473, 55-60; Nature, 2015, 517, 99-103) have clearly shown that there is no bicarbonate ion around the OEC. thus, in generally, the bicarbonate ion should not be considered as a component of the OEC. Meanwhile, the binding of the bicarbonate on the non-heme iron at the acceptor side is relative stable, and it is unlikely to be exchangeable under physiological condition. Thus, I donot think the two dashed lines Figure 1 related to CO2/HCO3- could be misleading. Thus, I would like to suggest the author to delete two dashed lines in the Figure 1.

iii)             The detailed structure of the OEC has been firstly reported by Shen’s group (Nature, 2011, 473, 55-60; Nature, 2015, 517, 99-103), thus, it would be more reasonable to cite these two important works in the page 2 line 62 and page 3 line 71.

iv)              The mechanism in Figure 6 is only one of possible mechanism, and detailed mechanism remains an open question. There are many other proposals as well (e. g. J. Barber*, Nat. Plan 2017, 3, 17041; H. Ishikita*, Nat. Commun. 2018, 9, 1247; P. Siegbahn*, BBA, 2013, 1827, 1003-11019). Thus, I suggest modifying the title of Figure 6. In addition, it would be more reasonable to cite some other models from other groups.

v)               For the functional role of the calcium, the author needs to consider the recent finding that the calcium can be replaced by other metal ions without significant modification of the structure and redox potential obtained by the closer mimicking of the OEC  (Science, 2015, 348, 690-693; JACS, 2021, 143, 17360-17365).

Author Response

 

1. The chloride ion has been long considered to be a key component of the OEC, however, recently crystal studies of PSII have demonstrated that it is located outside of the OEC and not directly bound to theMn4CaO5-cluster. Thus, it is more reasonable to state that the chloride ion could not be an essential component of the oxygen-evolving complex although it may play roles for the delivery of proton and/or substrate water during the catalytic reaction. Thus, I suggest removing the “one chloride ion” from the abstract (line13 in page 1).

“one chloride ion” has been removed, and I have added “although located outside the Mn₄CaO₅ cluster,” on line 129.

 

1. The opinion of the contribution of bicarbonate to OEC isfully questionable since most recent crystal studies (e.g.Nature, 2011, 473, 55-60; Nature, 2015, 517, 99-103)have clearly shown that there is no bicarbonate ion around the OEC. thus, in generally, the bicarbonate ion should not be considered as a component of the OEC. Meanwhile, the binding of the bicarbonate on the non-heme iron at the acceptor side is relative stable, and it is unlikely to be exchangeable under physiological condition. Thus, I do not think the two dashed lines Figure 1 related to CO₂/HCO₃- could be misleading.Thus, I would like to suggest the author to delete two dashed lines in the Figure 1.

The dashed lines mentioned by the reviewer, and their explanation, have been removed from the figure, and the legend has been adjusted to show that the figure is slightly different from the one in the source.

 

• The detailed structure of the OEC has been firstly reported by Shen’s group (Nature, 2011, 473, 55-60;Nature, 2015, 517, 99-103), thus, it would be more reasonable to cite these two important works in the page2 line 62 and page 3 line 71.

I have included citations to the mentioned works in the text (lines 6 and 83–84), and in the reference list.

 

6. The mechanism in Figure 6 is only one of possible mechanism, and detailed mechanism remains an open question. There are many other proposals as well (e.g. J. Barber*, Nat. Plan 2017, 3, 17041; H. Ishikita*, Nat.Commun. 2018, 9, 1247; P. Siegbahn*, BBA, 2013,1827, 1003-11019). Thus, I suggest modifying the title of Figure 6. In addition, it would be more reasonable to cite some other models from other groups.

The following has been added, and additional references entered in the list: “It should be realized that Figure 6 is tentative, one of several possible mechanisms; many other figures with different versions of the cycle have been published (Klauss et al. (2012), Barber (2017), Pushkar et al. (2018), Guo et al. (2022), Allgöwer et al. (2022), and Han et al. (2022)). It is too early to draw a final version of this cycle.”

 

 

1. v) For the functional role of the calcium, the author needs to consider the recent finding that the calcium can be replaced by other metal ions without significant modification of the structure and redox potential obtained by the closer mimicking of the OEC (Science

2015, 348, 690-693; JACS, 2021, 143, 17360-17365).

The JACS article (Yao et al. 2021) has been included. The Science article mentioned by the reviewer does not deal directly with any other element replacing calcium. But it refers to Tsui & Agapie (2013), and I have referred to them, and I also added Lockett et al. (1990) who had indications that vanadyl ions have a calcium-like effect.

 

Reviewer 3 Report

The present review article by Björn et al revisits the oxygen evolution assembly in photocatalytic systems. A detailed discussion about the water oxidation in the photosystem II and Mn₄CaO₄ cubance structure has been presented. The manuscript introduction is very well structured and follow some minor detail about the role of various units leading to oxygen evolution. The manuscript topic is appealing; however, more in-depth discussion is needed to improve the quality of the manuscript. Some Comments are:

1. The abstract should clearly state what is the motivation of the review and what is broadly covered in the manuscript.

2. In the introduction, the author has raised the question that four photons don’t strike simultaneously, and natural photosynthesis found a way to solve this issue. However, no explanation has been given in the following sections of how multiple electrons and holes are transferred.

 

3. The examples discussed in the review are very limited and must be expanded. (Catalysts 2020, 10(2), 185) Additionally, some chemical studies have used similar cubance structures and investigated the role of ligands in water oxidation. Some similar studies can be included. For example, J. Am. Chem. Soc. 2010, 132, 33, 11467–11469.

Author Response

 

1. The abstract should clearly state what is the motivation of the review and what is broadly covered in the manuscript.

I have added three sentences at the start of the abstract to clarify this.

 

2. In the introduction, the author has raised the question that four photons don’t strike simultaneously, and natural photosynthesis found a way to solve this issue. However, no explanation has been given in the following sections of how multiple electrons and holes are transferred.

I have now tried to clarify this on lines 69–74.

 

3. The examples discussed in the review are very limited and must be expanded. (Catalysts 2020, 10(2), 185) Additionally, some chemical studies have used similar cubance structures and investigated the role of ligands in water oxidation. Some similar studies can be included. For example, Am. Chem. Soc. 2010, 132, 33, 11467–11469.

 

I think that one should be restrictive with inclusion of non-biological literature (only include this if there is special reason to do so) in order not to let the article grow too much. Thus I find the second article mentioned by the reviewer, Robinson et al. (2010) J. Am. Chem. Soc. 2010, 132, 33, 11467–11469, although quite interesting, to be beyond the topic I had intended. Li et al. (2020) Catalysts 2020, 10(2), 185, on the other hand, although also dealing with an artificial system, is more aimed at understanding the natural system. It is a good review, mainly discussing various versions of the S-cycle. I have now mentioned it on lines 6y–68.