Metagenome mining and functional analysis reveal oxidized guanine DNA repair at the Lost City Hydrothermal Field

Payton H. Utzman; Vincent P. Mays; Briggs C. Miller; Mary C. Fairbanks; William J. Brazelton; Martin P. Horvath

doi:10.1371/journal.pone.0284642

Peer Review History

Original SubmissionApril 3, 2023
6 Jul 2023 Decision Letter - Pramodkumar Pyarelal Gupta, Editor PONE-D-23-10070Metagenome mining and functional analysis reveal oxidized guanine DNA repair at the Lost City Hydrothermal FieldPLOS ONE Dear Dr. Horvath, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Aug 20 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. Thank you for stating in your Funding Statement: "This work was supported by National Science Foundation (https://www.nsf.gov/) awards to Martin. P Horvath (CHE:CLP- 1905249, 2204229) and to William J. Brazelton. (OCE-1536405). This work was also supported by the NASA Astrobiology Institute Rock-Powered Life team." Please provide an amended statement that declares all the funding or sources of support (whether external or internal to your organization) received during this study, as detailed online in our guide for authors at http://journals.plos.org/plosone/s/submit-now. Please also include the statement “There was no additional external funding received for this study.” in your updated Funding Statement. Please include your amended Funding Statement within your cover letter. We will change the online submission form on your behalf. 3. Please amend your manuscript to include your abstract after the title page. Additional Editor Comments: The author should confirm the similarity and identty between the query sequence and database sequences in BLAST research In case of protein structure prediction, how the authors have assessed the modeled strucrture quality, it should be framed appropriatey and added in the text. As the Authors have performed molecular docking experiment, what was the rational to select the binding site region, kindly add it. The molecular docking is not the wholesome validation, the authors should carry out MD Simulation study, which will give us more detail outcome in terms of dynamicity and stability. Spell check and grammar needs to corrected The PDB-id should be well define. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes ****** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: This well-written and enjoyable manuscript by Utzman et al provides compelling evidence that organisms evolved ways to deal with oxidative DNA damage prior to the Great Oxidation Event. The presence of homologues of the GO DNA repair system in microbes recovered from the Lost City Hydrothermal Field (LCHF) is interesting, and the ability of distant mutY homologues from this environment to complement E. coli mutY mutants is remarkable. This work raises a number of interesting possibilities concerning the importance of ROS and oxidative damage during the evolution of life, even in the absence of high oxygen levels. I have only a couple of minor notes: 1. In the Discussion, when covering potential sources of ROS/RNS/RSS, beyond being by-products of some metabolic pathways, might these also be generated as a form of inter-bacterial competition or warfare? The idea that many antibiotics act by generating ROS directly or indirectly is gaining traction and might be relevant selective pressures in mixed microbial communities. Also of potential relevance is the idea that some quorum sensing molecules might be progenitors of certain antibiotics, having antibiotic activities against competitors. Is there any evidence of inter-microbial competition/warfare within the LCHF or similar environments? 2. Line 174: '…and the catalytic Tyr residue is often replaced...' (missing ‘d’) ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No ******** [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0284642.r001
Revision 1
1 Dec 2023 Author Response Responses from the authors are provided for each point raised in the initial review. The authors have carefully reviewed the PLOS ONE style requirements, including those for file naming, and the revised version matches these style requirements as far as we know. The funding statement as been amended as requested, added to the cover letter, and this statement is also provided here. Thank you for updating the online submission form. That is a big help. Updated Funding Statement: This work was supported by NSF awards to MPH (CHE:CLP- 1905249, 2204229) and to WJB (OCE-1536405), by the NASA Astrobiology Institute Rock-Powered Life team, and by UROP funding from the Office of Undergraduate Research at the University of Utah awarded to PHU. The support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged. There was no additional external funding received for this study. End of Updated Funding Statement The Abstract is now included after the title page. Supplementary Information Table S2 reports the pairwise identity among query and database sequences. The text clarifies the % identity cutoff for finding MutY candidate genes in the metagenome and the E-value threshold (see Lines 162-163). Additionally, observations regarding % identity between candidate genes and query sequences are included in the text (see Lines 234-239) Table 3 now reports the pLDDT scores for each predicted structure. Notes for assessing modeled structure quality have also been added to the text (see Lines 333-348) The text now describes the rationale for selection of the binding site region in the Results section (see Lines 356-361) Thank you for this suggestion to validate the molecular docking outcomes. The report now includes MD simulation to analyze the docking outcomes. Interaction energies averaged over a 10-ns simulation are reported in Table 3 for each ligand-receptor complex. The text also describes these outcomes in a new subsection Molecular dynamics simulations (see Lines 366-437). Supporting Information Fig S7 shows time-evolution structures along with time-dependent distance and energy plots. Spelling and grammar have been corrected. PDB-ids have been defined. Thank you for reviewing our manuscript favorably! Thank you for this interesting observation and suggestion. We have added note in the Discussion to highlight the possibility of bacterial warfare (see Lines 561-563); however, so far no evidence for inter-bacterial competition has emerged from analysis of these communities. Thank you for pointing out this typographical error which has been corrected (see Line 191). Other mistakes in spelling and grammar have also been corrected. Attachments Attachment Submitted filename: Response to Reviewers.pdf https://doi.org/10.1371/journal.pone.0284642.r002
27 Dec 2023 Decision Letter - Pramodkumar Pyarelal Gupta, Editor PONE-D-23-10070R1Metagenome mining and functional analysis reveal oxidized guanine DNA repair at the Lost City Hydrothermal FieldPLOS ONE Dear Dr. Horvath, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Feb 10 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. Please include the following items when submitting your revised manuscript: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols. We look forward to receiving your revised manuscript. Kind regards, Pramodkumar Pyarelal Gupta, PhD Academic Editor PLOS ONE Additional Editor Comments: MD simulation which is an important part to the research work, but here the time consideration only for 10-nano second i.e. a very small time limit. Again the authors have mentioned in result and supportive data that the study outcome is unstable in majority of cases. As a suggestion the time limit should be minimum 100 ns or more, which will give us more data to analyze it in depth. [Note: HTML markup is below. Please do not edit.] [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0284642.r003
Revision 2
1 Apr 2024 Author Response The MD simulations have been extended to 100 ns. The trajectories are summarized as Energy and Distance plots in Supplementary Information Fig S7 and also as molecular movies Supplementary Information Movies. The main text and text for the supplementary information have been updated to include descriptions for the more extensive MD analysis. Attachments Attachment Submitted filename: Response to Reviewers for second revision.docx https://doi.org/10.1371/journal.pone.0284642.r004
17 Apr 2024 Decision Letter - Pramodkumar Pyarelal Gupta, Editor Metagenome mining and functional analysis reveal oxidized guanine DNA repair at the Lost City Hydrothermal Field PONE-D-23-10070R2 Dear Dr. Martin P. Horvath We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Pramodkumar Pyarelal Gupta, PhD Academic Editor PLOS ONE Additional Editor Comments (optional): The MD simulation study is good enough. Reviewers' comments: https://doi.org/10.1371/journal.pone.0284642.r005
Formally Accepted
26 Apr 2024 Acceptance Letter - Pramodkumar Pyarelal Gupta, Editor PONE-D-23-10070R2 PLOS ONE Dear Dr. Horvath, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps. Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. If we can help with anything else, please email us at customercare@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Pramodkumar Pyarelal Gupta Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0284642.r006

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