Molecular Dissipative Structuring: The Fundamental Creative Force in Biology

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

This manuscript is dedicated to the Thermodynamic Dissipation Theory for the Origin and Evolution of Life by Karo Michaelian and continues a long list of similar publications. Specific focus has been made on the interaction of UV-C with natural pigments. The manuscript is robustly written and does not need further English peer-review. However, some points and literature references need clarification. This is why I recommend a revision. Here are my suggestions:

1. This is not an article, but a review. Please, revise.
2. I like Figure 1. However, its discussion lacks mentioning specific molecules: amino acids, coenzymes, pigments, etc. In particular, tryptophan, flavin and folic acid can be named and their significance can be supported by citations.
3. Section 2 contains zero citations. At least major sentences should be supported by previously published articles.
4. The list of references includes 24 self-citations of Michaelian and co-authors. This amount should be significantly reduced.
5. “… arose as spontaneous molecular dissipative structuring of organic chromophores (pigments) to dissipate the incident UV-C solar light flux available at Earth’s surface throughout the Archean”. This passage can be supplemented by citations of the leading researchers in the field, not only by self-citations. For example, the works of Szostak, di Mauro, Mulkidjanian, Kritsly and Telegina, etc.
6. “ … ATP, which could then, in numbers and in combination with cofactors and coenzymes, provide chemical potential for molecular transformation of covalent bonds” – there have been numerous studies on abiogenic synthesis of ATP on proteinoid-silicate nanoparticles. This is an appropriate place to cite them.
7. The usage of figure citations in the main text should be standardized and unified.

Author Response

I thank the reviewer for their comments and suggestions which have certainly helped improve the manuscript.

Comment 1: This is not an article, but a review. Please, revise.

Response 1: I have adopted the reviewer's suggestion and converted the manuscript into a review article by including a new section, section 2 (line 75), entitled ``A Historical Perspective of Photochemical Dissipative Structuring'' and more than doubled the number of references. The new section is a review of published literature invoking UV light in abiogenesis, related to either synthesis or to photoprotection. I have contrasted these works which consider UV light as a free energy source for molecular transformation (or invoking dissipation for photoprotection) with the present manuscript which invokes photon absorption and dissipation, not only for the free energy for synthesis, but for driving molecular concentration buildup to significant values. Emphasizing that photon dissipation (entropy production) is the fundamental thermodynamic reason for increasing the dissipative nature of the molecular concentration profile. For example, I mention that strong and very wide-band UV absorption of the final product molecule is not requirement for synthesis or photoprotection, but it is for photodissipation. In refocusing the manuscript as a review article, I have increased the number of citations from the original 66 to 132.

 

Comment 2: I like Figure 1. However, its discussion lacks mentioning specific molecules: amino acids, coenzymes, pigments, etc. In particular, tryptophan, flavin and folic acid can be named, and their significance can be supported by citations.

Response 2: In the Introduction, before Figure 1, beginning at line 54, I have included a new paragraph describing the extraordinary properties of the fundamental molecules (optical and chemical) and give an argument as to why these molecules have retained these properties until today even though they now have a number of different functions not related to UV-C light. I have also divided section 6 (old section 5) on ``Fundamental Creative Force'' into three new subsections; Molecular Level, Organism Level and Biosphere Level. In the Molecular Level subsection, I have included a discussion on the relevance of the UV-C absorption of the nucleic acids and the aromatic amino acids to the origin of life by including 3 new paragraphs starting at line 470 of the revised manuscript. New citations have been included.

Comment 3: Section 2 contains zero citations. At least major sentences should be supported by previously published articles.

Response 3: The previous section 2, now section 3, has been supplemented with citations to the relevant references concerning the thermodynamic theory.

Comment 4: The list of references includes 24 self-citations of Michaelian and co-authors. This amount should be significantly reduced.

Response 4: The number of self-citations has been reduced to 20. The remaining self-citations support important results presented in the review and are required for an understanding of how photon dissipation relates to the origin of life. However, self-citations are now about 15% of the total (132) since many new citations have been added, including all those suggested by the reviewer.

Comment 5: “… arose as spontaneous molecular dissipative structuring of organic chromophores (pigments) to dissipate the incident UV-C solar light flux available at Earth’s surface throughout the Archean”. This passage can be supplemented by citations of the leading researchers in the field, not only by self-citations. For example, the works of Szostak, di Mauro, Mulkidjanian, Kritsly and Telegina, etc.

Response 5: I have included citations to all these authors, as well as others, with reference to the utility of UV light in fundamental molecule synthesis and aspects of photoprotection in the new section 2 on the "Historical Perspective" (beginning on line 78).

Comment 6: “ … ATP, which could then, in numbers and in combination with cofactors and coenzymes, provide chemical potential for molecular transformation of covalent bonds” – there have been numerous studies on abiogenic synthesis of ATP on proteinoid-silicate nanoparticles. This is an appropriate place to cite them.

Response 6: I have included new references to Ponnamperuma et al. 1963, Kritsky et al. 2007, Kolesnikov et al. 2008, and Telegina et al. 2013 regarding the photo-production of ATP in different environments (line 390).

Comment 7:  The usage of figure citations in the main text should be standardized and unified.

Response 7: I have unified all references to figures in the text as "Fig. ...".

Finally, I have replaced the old figure 4 of the entropy production over time for the dissipative structuring of adenine with a figure that I believe is more relevant, relating to the evolution of the concentration profile of molecules on route to adenine. I still make reference to the entropy production as a function of time and point to the correct figure (Fig. 18) of the original reference Michaelian 2021 [14]. I have made many minor changes throughout the text to improve the redaction.

 

Reviewer 2 Report

Comments and Suggestions for Authors

Since this paper is based largely on the viewpoint that these phenomena cannot be explained by evolution, I think the author should quote an alternate view. See, for example, Pascal and Pross, Life 2022, 12, 2016, who advance the view that nonequilibrium phenomena can be explained by evolution and dynamic kinetic stability.

Author Response

Response to Reviewer 2

I thank the reviewer for their reading of the manuscript and for pointing out the interesting paper.

Comment 1: Since this paper is based largely on the viewpoint that these phenomena cannot be explained by evolution, I think the author should quote an alternate view. See, for example, Pascal and Pross, Life 2022, 12, 2016, who advance the view that nonequilibrium phenomena can be explained by evolution and dynamic kinetic stability.

Response 1: I have read the paper entitled ``On the Chemical Origin of Biological Cognition'' by Pascal and Pross and find it interesting. My reading of this paper is that the authors suggest that non-equilibrium thermodynamics, including what they label as ``dynamic kinetic stability'' states, may be related to cognition. Their ``dynamic kinetic stability states'' in the more formal classical irreversible thermodynamic language of Prigogine and collaborators are known as ``non-equilibrium stationary states''. These are mentioned and considered in my manuscript to play a fundamental role in evolution at different hierarchal levels of biology, so the authors of the paper and I are in complete agreement regarding the importance of these to life. I include a citation to this paper (line 139) in Section 3 on Irreversible Thermodynamics, when referring to applications of the Prigogine formalism to different aspects of living systems.

Finally, I have replaced the old figure 4 of the entropy production over time for the dissipative structuring of adenine with one that I believe is more relevant, relating to the evolution of the concentration profile of molecules on route to adenine. I still make reference to the entropy production as a function of time and point to the correct figure (Fig. 18) of the original reference Michaelian 2021 [14]. I have made many minor changes throughout the text to improve the redaction.

Reviewer 3 Report

Comments and Suggestions for Authors

Please see the attachment.

Comments for author File: Comments.pdf

Author Response

 

I thank the reviewer for their detailed reading of my manuscript and for their extensive list of corrections.

Comment 1: The manuscript is interesting and may be published after some corrections as listed below.

Response 1: All of the listed corrections have been incorporated into the new version of the manuscript, as specified by the reviewer, except for the following, so as not to alter the intended meaning, as described below;

Line 93- 97 : “3. The existence of various sets of these internal forces and flows for different linear/nonlinear subsystems at the same initial boundary conditions producing monostable / multistable dissipative structures at different stationary states (unstable and stable) – each set ----“

Rewritten as (line 167);

``The potentiality of various distinct sets of these internal forces and flows for non-linear systems for the same initial and boundary conditions, (i.e., multiple, locally stable, dissipative structures or processes, at stationary states) -- each set --''

Line 101-105 : “ 5. The positive feedback from autocatalytic and cross-catalytic steps generates greater dissipation (entropy production) energy with stable/larger attractor basin in the parameter space, which may have a tendency to stochastic evolution through perturbation of the stationary states

Rewritten as (line174);

The non-deterministic (stochastic) tendency for evolution on perturbation to stationary states (dissipative structures) affording greater dissipation (entropy production), particularly through routes with autocatalytic and cross-catalytic steps, since these have a larger and thus more stable attractor basin in this generalized parameter space.

Fig.4. : The unit of entropy production should be J K-1 cm-3 s-1

The entropy production as presented is integrated over depth, so the correct units are J K-1 cm-2 s-1. This figure 4 was, however, replaced by a new figure of the simulated concentration profile of the intermediate molecules compared with an experiment. I believe that this is a more relevant and interesting figure. Reference in the text is still made to the increase in entropy production as a function of time to the correct figure (Fig. 18) of the original reference [14].

Fig.7 is a schematic representation (not computed) – Can you calculate it numerically from a physical model?

We have published a physical model of selection through entropy production for non-linear ecosystems. I have included the phrase ``For a numerical analysis of a physical model depicting this, see reference Michaelian, 2005 [79]'' at the end of the caption of Figure 7.

I have included a new section, Section 2 ``A Historical Perspective...'' in response to the suggestion of Reviewer 1. I have also made many small corrections to the text to improve the redaction.

Reviewer 4 Report

Comments and Suggestions for Authors

The explanation of life's origin in this paper is quite consistent and differs in emphasis from the conventional “chemical evolution theory.” Life did not begin because self-replicators or mutations arose by chance, but rather because molecular dissipation structures, formed to dissipate solar radiation, inevitably acquired self-sustaining and proliferative behavior. Nature selected entropy production as a selection criterion, explaining changes in Archean atmospheric composition and surface light spectra from the perspectives of absorption wavelength, molar absorptivity, and quantum efficiency. The process by which pigment molecules were mass-produced to efficiently dissipate solar energy is highly intriguing. The author's argument is compelling. If the author can address a couple of questions, I recommend acceptance for publication.

 

1. If dissipative structuring occurs at the molecular level, resulting in observable natural selection-like behavior, would molecules that are disadvantageous for entropy production be eliminated?
2. Why are radiative transitions sometimes selected despite conical intersection being dominant for entropy production after electronic excitation?

3. I think it's acceptable to cite Hill's paper (Nature 348(1990)426-428), which studies crystal structure transitions using entropy production as a selection criterion.

Author Response

I thank the reviewer for their interesting questions, the answers to which have certainly improved the redaction of the manuscript.

Comment 1: If dissipative structuring occurs at the molecular level, resulting in observable natural selection-like behavior, would molecules that are disadvantageous for entropy production be eliminated?

Response 1: Under the non-equilibrium thermodynamic formalism, in first approximation, molecules disadvantageous for entropy production would be those that don't absorb photons. However, there are other ways in which a molecule may foment entropy production. For example, a hydrophilic-hydrophobic molecule having chemical affinity to a pigment molecule will help anchor it to the ocean surface where photon intensity would be greater, thereby improving overall photon dissipation. In reference Mejia and Michaelian [62] we have suggested that the amphipathic amino acids (tyrosine, tryptophan methionine, lysine) played this anchoring role for DNA or RNA which gave rise to their amino acid - codon assignment and the first information storage in nucleic acid given the suggested stereochemical era, Yarus et al. 2009 [121]. I have now mentioned this in section 6.1 (line 494). A molecule which in no way foments entropy production, could appear for time to time, but since it does not increase photon dissipation, would indeed be selected against, as described in figure 2, but analogously for the complex.

Comment 2: Why are radiative transitions sometimes selected despite conical intersection being dominant for entropy production after electronic excitation?

Response 2: Since conical intersections are located energetically down-hill from the Franck-Condon region, the direction and velocities of approach of the nuclear coordinates to a conical intersection are important in defining the outcome (Schuurman and Stolow, Dynamics at Conical Intersections, Annu. Rev. Phys. Chem., 2018).

If there are conical intersections to internal conversion to the ground state, then the quantum efficiencies for any other transition (e.g., fluorescence) are usually small or very small. For example, for the cases of tryptophan and tyrosine, which do have a conical intersection to internal conversion, the quantum efficiencies for fluorescence are still 0.13 and 0.14 respectively (Chen, 1967 [120], while for the nucleobases it is much smaller, for example, adenine; 2.6x10^{-4} (Nikogosyan and Letokhov, 1970 [122]. If the two are associated together, however, the quantum efficiency for the amino acid fluorescence reduces to 10% of its nominal free value (Dimicoli and Helene,1974 [123]. The decrease in quantum efficiency for fluorescence upon aromatic amino acid - nucleic acid interaction, in fact, is widely used to monitor protein binding to nucleic acid (e.g., via Stern-Volmer analysis). We have proposed (Mejia and Michaelian. 2020 [62]) the thermodynamic imperative of increasing dissipation as a reason for the amino acid - codon assignments in the suggested stereochemical era (Yarus et al., 2002 [121]). I have included this data in section 6 (line 494).

Comment 3: I think it's acceptable to cite Hill's paper (Nature348(1990)426-428), which studies crystal structure transitions using entropy production as a selection criterion.

Response 3: I thank the reviewer for pointing out this paper which definitely supports the case being made of molecular dissipative structuring based on selection through entropy production. Organic materials, are however, generally more effective at UV photon dissipation than inorganic materials since they are ``soft materials'' in the sense that their vibrational degrees of freedom in the electronic excited state can couple significantly to their vibrational degrees of freedom in the electronic ground state through conical intersections (non-adiabatic coupling), unlike in most inorganic materials, except for special cases, like near local defects in transition metal complexes (Atanasov et al., 2019 [87]). I have included a new paragraph at the end of Section 4 (line 244) where I summarize the results of Hill.

Finally, I have replaced the old figure 4 of the entropy production over time for the dissipative structuring of adenine with one that I believe is more relevant, relating to the evolution of the concentration profile of molecules on route to adenine. I still make reference to the entropy production as a function of time and point to the correct figure (Fig. 18) of the original reference, Michaelian 2021 [14]. I have made many minor changes throughout the text to improve the redaction.

Round 2

Reviewer 1 Report

Comments and Suggestions for Authors

Thank you for answering to my questions. Now the manuscript suits for publication as a review article.

Author Response

I thank the reviewer for recommending publication of the manuscript in its present form.

Reviewer 3 Report

Comments and Suggestions for Authors

Journal: Entropy

Manuscript ID: entropy-4110649

Type of manuscript: Article

Title: Molecular Dissipative Structuring; the Fundamental Creative Force in

Biology 

Authors: Karo Michaelian *

Comments about the revised version:

 

The revised version is much better and probably suitable for publication, if other reviewers do not object to it. I find the following weak points / mistakes in the revised version.

1) C18:3n-2 in Figure 5 caption, if removed completely, will probably be much clear presentation (IUPAC name states everything).

2) Number of self-citations may be restricted to within five-six.

Comments for author File: Comments.pdf

Author Response

I thank the reviewer for their second round of suggestions. 

I have removed the reference to "C18:3n-2" in Figure 5 caption. 

Regarding the number of self-citations, the manuscript is now a Review article on molecular dissipative structuring as the chemistry and physics behind the origin and evolution of life. Our group initiated this perspective and has done most of the work on associated themes. I removed all self-citations non-essential to the review in my first revisión. The percentage of self-citations to the total was reduced to 15%. Those that remain are directly related to the background, history, or different aspects of molecular dissipative structuring in relation to the origin of life and would negatively affect the value of the manuscript if removed. I believe that the reader deserves elaboration and justification of the propositions within the manuscript if they are so inclined to seek.
 
I have made numerous small corrections throughout the text to improve the redaction.

 

Reviewer 4 Report

Comments and Suggestions for Authors

This is excellent work.

Author Response

I thank the reviewer for their kind comment.