PCLM-D-24-00267

Shifts in Coral Reef Holobiont Communities in the High-CO2 Marine Environment of Iōtorishima Island

PLOS Climate

Dear Dr. Huerlimann,

Thank you for submitting your manuscript to PLOS Climate. After careful consideration, we feel that it has merit but does not fully meet PLOS Climate’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.

First of all please again accept my apology for the long time it took to obtain reviews. However, I believe you will be pleased to hear both reviewers liked your manuscript and made detailed suggestions for improvement. Please address them as thoroughly as you can. I am looking forward to seeing the revised manuscript.

Please submit your revised manuscript by 03/06/2025. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at climate@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pclm/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Katharina C Wollenberg Valero, Dr. rer. nat

Academic Editor

PLOS Climate

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Does this manuscript meet PLOS Climate’s publication criteria ? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. 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

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Climate 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

Reviewer #2: Yes

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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: Review for: Shifts in Coral Reef Holobiont Communities in the High-CO2 Marine Environment of Iōtorishima Island

This manuscript was a very interesting read, and I liked the main species of the study being a zoanthid as opposed to scleractinian coral species. I agree with the authors that holobiont studies on zoanthids and on animals in high pCO2 sites are lacking, and I hope the publication of this study prompts similar research in the future. This said, there are a few edits/changes that should be made before publication.

Small comment: The authors should double-check to make sure all instances of pCO2 have the 'p' italicized.

Introduction

Line 92: Parenthesis missing in (e.g., in scleractinians; (17), which should be (e.g., in scleractinians; (17))

Line 94: Parenthesis missing in (e.g., (19), which should be (e.g., (19))

Materials and Methods

Lines 123-124: Maybe a bit nitpicky, but could be reworded to "As detailed in (21), Iōtorishima was visited from September 14th to 16th in 2020 (Fig. 1, Table 1).

Lines 125-126: Could you include an estimated area surveyed alongside the gps coordinates (e.g. circa 2000 m^2)?

Line 127: is the '=' in (=high CO2) a typo, or is it there to illustrate that the samples originated from the high CO2 sites? Also, should this be labelled as 'high pCO2' for consistency?

Table 1: Same small issue like 'Lines 123-124' with the presence of unnecessary periods in the 'Date Collected' column.

Lines 136-137: Were there any differences in microbial composition between the two sampling dates at Mizugama? In addition, were there any differences across sampling depth? Because all Mizugama ASVs were pooled for downstream analysis, it would be nice to have at least a supplementary table/figure that shows the microbial composition between seasons/depths if there are differences. If there is no difference, a sentence stating the reason for pooling ASVs would be appreciated.

Lines 146-148: Similar to my previous question about Mizugama, were the P. tuberculosa individuals collected in Hawaii sampled during similar seasons between 2018 and 2020? Just curious to know whether sampling across different seasons could have affected microbiome composition.

Lines 148-150: If possible, can the % concentration of DMSO in the buffer be stated? Also, missing °C symbol and should be 'and stored at room temperature (24 °C)'.

Results

Lines 259-264 & Fig. 2: Can a supplementary figure of all alpha indices metrics also be included? Also, can the specific indices used to produce Fig. 2 be stated in the 'Statistical analyses' section?

Could a figure/table of the Symbiodiniaceae clades per site also be included? Could also be supplementary.

Table 3: Possible small error but the row labelled 'O'ahu North Shore' includes too much spacing.

Discussion

Line 364: Symbiodiniaceae is misspelled

Line 375: Parenthesis missing in (former Symbiodinium ‘clade C’; (16), which should be (former Symbiodinium ‘clade C’; (16))

Line 415: Parenthesis missing in (e.g., reviewed in (55), which should be (e.g., reviewed in (55))

Lines 427-428: Parenthesis missing in (e.g., seastars (56), which should be (e.g., seastars (56))

Line 428: Parenthesis missing in (e.g., isopods, (57) and also unnecessary comma, which should be (e.g., isopods (57))

Line 451: Parenthesis missing in (e.g., (63), which should be (e.g., (63))

Line 454: Parenthesis missing in 'scleractinian corals (e.g., (64) and fish (e.g., (65)', which should be 'scleractinian corals (e.g., (64)) and fish (e.g., (65))'

Line 477: Parenthesis missing in (with the exception of (76), which should be (with the exception of (76))

Small question, but could symbiont and bacterial diversity and abundance been affected by the level of anthropogenic disturbance across sites in addition to presence of high pCO2? Because anthropogenic disturbance and Mizugama was mentioned briefly in the results section, it would be nice to have a small sentence or two addressing this in the discussion (especially since Endozoicomonas, Vibrio, Tenacibaculum and Mollicutes abundance at Mizugama are quite different compared to Iotorishima and Hawaii).

Reviewer #2: ## General comments

This manuscript invesigated the Symbiodiniaceae and bacterial communities of the zoanthids P. tuberculosa sampled in a natural analogues for ocean acidification and multiple control sites. The comparision to multiple site makes the study strong as it is highlight the uniqueness of the samples under high CO2, it is the recommended approach for natural analogues (James P. Barry et al., 2010) but often not possible due to logistic.

The authors show that individuals at the high CO2 reefs reduced Symbiodiniaceae diversity and bacterial communities with lower richness and distinct taxonomic profiles, including increased levels of Mollicutes and Vibrio spp. They concluded that the distinct Symbiodiniaceae and bacterial communities at the Iōtorishima Seep correspond to plasticity in response to environmental stress.

The methods and results are sounds. However, the introduction and discussion need to be revised. Often statements remain very vague. I have highlighted the parts that can be added, rephrased, etc in detailled comments. Although there is not much previous literature, I feel it is important to introduce and discuss more how the change in Symbiodiniaceae and bacterial diversity could contribute to the increase resistance to high pCO2.

Overall I would recommend that the introduction and discussion be improved before accepting this manuscript.

James P. Barry, Jason M. Hall-Spencer, & Toby Tyrrell. (2010). In situ perturbation experiments: Natural venting sites, spatial/temporal gradients in ocean pH, manipulative in situ p(CO ) perturbations. In U. Riebesell, V. J. Fabry, L. Hansson, & J.-P. Gattuso (Eds.), Designing ocean acidification experiments to maximise inference (pp. 121–136). Publications Office of the European Union. http://epic.awi.de/Publications/Eng2009b.pdf http://scholar.google.com/scholar?hl=en&btnG=Search&q=intitle:Guide+to+best+practices+for+ocean+acidification+research+and+data+reporting#0

## Detailed comments

### Introduction

* line 62: the high CO2 and low pH is not due to climate but to increased atmospheric CO2 concentration caused by increasing anthropogenic emmission. Please rephrase. Moreover the term ocean acidification does not appear even once in the manuscript. Maybe good to define it here.

* line 69: The iotorishima CO2 seeps is generally consider a natural analogues for ocean. acidification. To be a natural analogues of future oceans it should also include higher temperature than control sites (which is the case of Nikko Bay) but not the case of CO2 seeps such as Iotorishima or Vulcano.

* line 71: Please rephrase, it sounds like the water turn over and decay of "organic matter" (rather than biomass) is what cause elevation in both semi-enclosed bay and CO2 seeps. But for CO2 seeps elevation in CO2 is due to the release of CO2 of volcanic origin. Consider adding a sentence describing CO2 seeps.

* line 72: reorder the example to have CO2 seeps and semi-enclosed bay separately, maybe two of each.

* line 81: "is" is missing.

* line 92, need to close the parenthesis

* line 93: A little harsh on previous research, there has been genomics, diversity studies using illumina sequencing, not many but not "basic ... Moreover the reference is wrong: 19 points to a study on Isopora, not in natural analogues. Please see for example for a study that include genomic of zooxanthellae at natural analogue. Kenkel, C. D., Moya, A., Strahl, J., Humphrey, C., & Bay, L. K. (2018). Functional genomic analysis of corals from natural CO2-seeps reveals core molecular responses involved in acclimatization to ocean acidification. Global Change Biology, 24(1), 158–171. https://doi.org/10.1111/gcb.13833

* After reading the introduction, I am not sure if the study will only present symbiodinaceae or bacterial diversity too. Need to add some background on microbial diversity studies at natural analogues. Moreover there is nothing on how shift in Symbiodinaceae or microbial diversity can provide resilience. Although it is understandable to keep it for the discussion, maybe something on the selection of species and individuals based on their resistance and the role of microbes in resistance to environmental stress would be appreciated.

### Material and methods

* line 237: "standard pH" is strange, maybe use "non-acidified reefs of [...]"

### Results

* General comments: As the main topic of the manuscript is the comparision with the CO2 seep, it would be nice to state the difference between communities found at the seep and other reefs, the same way it is highlighted for the nMDS of bacterial beta-div. Similarly, consider in tables to move Iotorishima seep as the first column so it is easy to see with which a difference was found.

* Consider reorganizing to group bacteria results (alpha, beta and composition) and then Symbiodinicaea.

* line 279: between all locations?

* line 305: Typo: Tsukishima instead of Iotorishima

* It is not clear what was the community of Symbiodinaceae at each locations. What species are dominant. In the discussion, it is stated that for Hawaii, all were Cladopium, what about at other sites? Maybe showing the community composition from symportal could help.

* Figure 5: how were the sample pooled together? Also it is not the abundance but the relative abundance. Were the percentage calculated from the overall read count for each OTU/ASV?

### Discussion

* The first paragraph should resume the results. At the moment it is not very useful: "both expected and surprising findings"?? Need to write what was expected and what was surprising (without going into details).

* line 379: "Iōtorishima P. tuberculosa exhibited lower Symbiodiniaceae diversity than the control sites." : I think this result is not presented?

* line 374-383: Consider moving most of it to results.

* line 397: Do you mean that Symbio. that show higher photosynthesis rates under high CO2 have been selected?

* line 390: Why does the authors thinks it is premature to state that pCO2 is the main cause? There are several control sites that are all different. Of course the measurement of more environmental parameters would be required, but still I feel that as all sites are quite similar among them but different from the CO2 seep, there is a good chance that CO2 is the main driver.

* Paragraph 372: It would be nice to develop more on how different (and lower diversity) of Symbio community contributes to resistance to environmental stressors.

* Paragraph line 417. This paragraph mostly restate the results. The only "discussion" is some on Mollicutes but this can be moved to the next paragraph. Some comparision with corals/cnidarians microbial diversity in other CO2 seep would be nice. Is it common to see increase Firmicutes or Entoplasmatales? Do corals/cnidarian under elevated CO2 typically show lower microbial diversity?

* 437: Consider rephrasing and fix the grammar: "While Mollicutes were found in relatively low numbers in both Hawaiʻi and Okinawan P. tuberculosa specimens, it was almost absent (< 0.01% relative abundance) at the control site at Iōtorishima, but highly abundant (25.6 % relative abundance) at the high pCO2 site." I think it should be "Mollicutes were found in relatively low numbers in both Hawaiʻi and Okinawan P. tuberculosa specimens and were almost absent (< 0.01% relative abundance) at the control site at Iōtorishima, but they were highly abundant (25.6 % relative abundance) at the high pCO2 site."

* line 441 : despite

* line 440: What was the dominant group/species in the high CO2 sites? Was it consistent across samples? Are there any information on the potential role they play in octocorals for example? line 336 "significant role" is very vague.

* paragraph line 444: Maybe a link with the level of urbanisation and some literrature?

* paragraph line 452: Consider moving some to the intro and fusing it with the next paragraph. These two paragraphs are good to justify the study (so introduction) and the only "discussion" is that note that the mechanisms of resistance of P. tuberculosa may not be applicable to other groups.

* concluding paragraph. Consider rephrasing as for now except for the first sentence, it is very vague: what do you mean by narrow and wide scale? the method used are not so "powerful", they are quite typical for such studies... Highlight that it is a unique study as the holobiont of zoanthids is understudied and it is the only study in natural analogues. Also highlight that the communities were distinct under high CO2 from all other (multiple) sites.

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Reviewer #1: Yes:  Joshua M. Heitzman

Reviewer #2: Yes:  Sylvain Agostini

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Attachments

Attachment

Submitted filename: Iotorishima_manuscript_author_responses_submission.docx

PCLM-D-24-00267R1

Shifts in Coral Reef Holobiont Communities in the High-CO2 Marine Environment of Iōtorishima Island

PLOS Climate

Dear Dr. Huerlimann,

Thank you for submitting your manuscript to PLOS Climate. After careful consideration, we feel that it has merit but does not fully meet PLOS Climate’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.

==============================

Required Changes.

1. Both reviewers identified several minor typos that need to be addressed:

(a.) On page 3, lines 40-41, the 2 in CO2 needs to be in subscript form.

(b) Include the missing parenthesis on page 4, line 65 and Page 24, line 481.

(c) add ** in the species table for Iōtorishima Seep versus Hawaiʻi Island Kona.

(d.) I agree that having "based on our results" twice in a row near line 419 makes reading this paragagraph the a bit odd. I recommend restructing one of the sentences for better readability.

(e.) Check line 430 and ensure that the quotations are placed as intended.

(f.) There a period in line 526 that should be rmoved.

2. Reviewer 1, was concerned about the use of the term "Non-parametric multidimenional scaling" in the materials and methods and the introduction of the term "Non-Pac Multidimentional Scaling" in the figure description. To avoid confusion please use the same term. 

3. In your figure decription also include a statement explaining what the ovals in the figures represent.

4. Please address all the questions raised by reviewer 1 about any data transformation that occured. If no data tranformation was done please state this in your response to reviews.

5. Please address the question(s) about the impact of seasonality on the microbial community. 

6. Also, please inform if Palythoa mitochondrial/chloroplast ASVs were removed from bacterial reads. If they were, please add a relevant statement in the methods.

==============================

Please submit your revised manuscript by . If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at climate@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pclm/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

We look forward to receiving your revised manuscript.

Kind regards,

Karl D. Castillo, Ph.D.

Academic Editor

PLOS Climate

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments (if provided):

Overall, I agree with the reviewers that the manucript has improved significantly from the previous version and that most of the issues and concerns raised were approapriately addressed. There are only a few minor fixes that needs to be addressed to ensure that the manuscript sfully comply with PloS Climate's publication criteria.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: (No Response)

Reviewer #2: All comments have been addressed

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2. Does this manuscript meet PLOS Climate’s publication criteria ? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. 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

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Climate 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

Reviewer #2: No

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6. 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: Review for:

Shifts in Coral Reef Holobiont Communities in the High-CO2 Marine Environment of Iōtorishima Island

Most of the mistakes that I stated in the previous review have been amended, with the exception of a few small errors.

Abstract & Discussion

Page 3, Line 41; Page 21, Line 407 - "high-pCO2" the "2" in pCO2 should be superscripted like in the rest of the manuscript

Introduction & Discussion:

Page 4, Line 65 - "(e.g.; (1-5)" is missing a close parenthesis at the end. Should be "(e.g.; (1-5))"

Page 24, Line 481 - Same error as above, where "(reviewed in (64)" should be "(reviewed in (64))"

Results:

Figures 3 & 5 - You state in the materials and methods that nMDS was used for beta-diversity, but the naming in the figure captions for both figures is stated as "Non-Pac Multidimensional Scaling". I have not seen non parametric multidimensional scaling abbreviated in that way before, but correct me if I am wrong. In addition, I would also include what the oval lines for each group represent (I assume it's the 95% conf interval but still).

Lastly, I have some questions that could be addressed in the materials and methods and/or discussion portion of the manuscript:

Was the data transformed prior to plotting nMDS? If so, state the transformation in the materials and methods. Also, was the data used for nMDS transformed to relative abundance prior to getting the distance matrices, or is it absolute abundance? Could state the form of data in the materials and methods as well.

Collection dates are scattered across several seasons; do you think that the microbial community composition varies seasonally, or does the microbial community of Palythoa remain consistent year-round usually? If seasonal variability is something that could have affected the presented data, maybe a caveat could be added to the discussion?

In addition, did you remove Palythoa mitochondrial/chloroplast ASVs from your bacteria reads? If so, maybe include that in the materials and methods.

Reviewer #2: The authors responded to all comments and modified the manuscript appropriately. The revised manuscript showed improve readability with clear improvements in the intro and discussion, which was my main concern. I have only a couple of minor comments that can be fixed during the proof reading step.

line 40: the 2 in CO2 need to be in subscript

table 2: you are missing ** in the species table for Iwotorishima seep vs Hawai'i Kona

line 419, it is a little strange to have two following sentene starting with "based on our results". I think you can remove the second one and place the reference at the end.

line 430: is it a direct quote? why the "" marks? If it is a direct quote that's fine but could make clearer: "[...] our results support the hypothesis proposed by Howe‐Kerr et al. [56] that that “corals from distinct [...]

line 526: there is a typo, an extra "."

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For information about this choice, including consent withdrawal, please see our Privacy Policy .

Reviewer #1: Yes:  Joshua M. Heitzman

Reviewer #2: Yes:  Sylvain Agostini

**********

[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.]

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Attachments

Attachment

Submitted filename: Response_to_reviewers.docx

Shifts in Coral Reef Holobiont Communities in the High-CO2 Marine Environment of Iōtorishima Island

PCLM-D-24-00267R2

Dear Dr. Huerlimann,

We are pleased to inform you that your manuscript 'Shifts in Coral Reef Holobiont Communities in the High-CO2 Marine Environment of Iōtorishima Island' has been provisionally accepted for publication in PLOS Climate.

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow-up email from a member of our team. 

Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.

IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.

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Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Climate.

Best regards,

Karl D. Castillo, Ph.D.

Academic Editor

PLOS Climate

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Additional Editor Comments (if provided):

Thanks for addressing the additional concerns raised by the reviewers in revision 1.

Reviewer Comments (if any, and for reference):