PONE-D-23-24973

Increasing temperature alleviates inhibitory effects of Irgarol 1051 and UVR on diatom photochemical performance across latitudes

PLOS ONE

Dear Dr. Wu,

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 all the points raised during the review process.

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We look forward to receiving your revised manuscript.

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Jean-François Humbert

Academic Editor

PLOS ONE

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   "This research was funded by the Natural Science Foundation of China (41876113) to Y Wu, the Key Project of Natural Science of Jiangsu High School (21KJA170001) to Y Wu, Qinglan Project of Jiangsu Province to Y Wu, and Priority Academic Program Development of Jiangsu Higher Education Institutions to Y Wu."

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Additional Editor Comments:

In particular, I ask you, in agreement with the two reviewers, to be much more careful in the abstract, discussion and conclusion of the paper about the interpretation of yours results. I also ask you to change the title of the paper. Not in any way, you can conclude from your data on what will happen in natural ecosystems at different latitudes in the context of global warming. Indeed, the three strains used in your experiments are from being representative of the three species nor of temperate and cold waters (at least you should have several recently isolated starins for each species before starting this discussion). Furthermore, your data only concern the study of very short-term responses to the two stressses applied knowing that many processes acting on different temporal scales are involved in the dynamics of phytoplakton communities.

Additional point: You have used 3-way RM ANOVA, but you have worked with triplicates. Permutation 3-way ANOVA would be more appropriate, please change.

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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: Partly

Reviewer #2: Partly

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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?

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: No

Reviewer #2: Yes

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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

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: The authors have indicated that they can provide data on request, but it is not deposited on an accessible site.

This manuscript deals with a subject involving major issues and where work is still too scarce: the interactions between the effects of contaminants and climatic parameters on primary producers. However, this manuscript needs to be reworked in certain parts by supporting them with the bibliography (example see the review by Gomes and Juneau (2017 - doi: 10.3389/fenvs.2017.00050). Thus, the discussion section deserves to be completed on the different behaviors towards applied stresses and their interactions between the 3 species studied. In the Materials and methods section, some descriptive elements are missing. Examples: information on the ecological traits of the species studied, light conditions during acclimatization, duration of UV and IRG exposure during experimentation after acclimatation, etc.

Below are my detailed comments:

Introduction

L35-38 For information, see the recent paper by Courcoul et al (2022 - DOI: 10.1111/1365-2745.14058), which proposes an approach to the effects of temperature on the photosynthetic activity of freshwater periphyton, taking into account not only the intensity of temperature, but also the duration of exposure (an important dimension in qualifying heatwaves): "A thermal dose approach". In addition, an early study investigated the effects of temperature on the sensitivity of a cyanobacteria to a PSII inhibitor (atrazine) and showed that, at higher temperatures, cyanobacteria (in monoculture) are less sensitive to atrazine, so that they expand within phtoplanktonic communities under conditions of higher temperature and herbicide contamination (Bérard et al., 1999 - doi: 10.1007/s002449900541).

L54-55 For information, IRG induces (at real concentrations in the environment) effects on planktonic and periphytic algal communities through the selection of tolerant taxa and thus the change in community composition, implying an acquisition of tolerance to IRG. IRG is more toxic than another PSII inhibitor such as atrazine on different taxonomic groups, particularly diatoms. (Nyström et al. 2002 - Water Research 36 (2002) 2020-2028; Bérard et al., 2003 - doi:10.1016/S0045-6535(03)00674-X ).

Materials and methods

L85 Apart from the fact that these 3 diatoms come from different climatic environments, they are 3 different species. Do you have any information on their life traits and possible sensitivities to different factors such as climate and pollutants?

L89-90 As the historical development conditions of the organisms can influence their response to stress, you have insisted on temperature conditions, but can you also specify the light conditions (obviously the same for the 3 species) during this pre-acclimation phase? Have you taken any measurements? Are these light conditions comparable to those observed in the environments where these strains were isolated? This seems to me an important point to discuss, given that you are testing the effects of light and UV on algae afterwards.

Fig.1 The text in the figure is written in small type. Specify in the legend the color codes (control/IRG) and the concentration of IRG applied, as well as the duration of exposure to the different stresses in the quartz tubes.

L11-112 Specify the exposure time (120 min?) of the cultures in the quartz tubes and justify this choice of exposure time (very short compared with chronic in situ conditions).

L120-124 Why is this table not in the list of tables?

L125 Final IRG concentration of 400ng/L: specify whether this is the nominal or measured concentration in the tubes. Give references on the effects of this level of contamination. Examples: This concentration already inhibits freshwater phytoplankton and periphyton by almost 50% (Nyström et al., 2002, Bérard et al., 2003). Similarly, in the marine environment, concentrations of 60 to 250 ng/L significantly inhibit phytoplankton (Dahl and Blanck, 1996 - https://doi.org/10.1016/0025-326X(96)84828-4). See also the work of Buma et al (2009 - doi:10.1016/j.seares.2008.11.007 ), who tested IRG on T. weissflogii. These elements could also be used in the discussion section of your manuscript (examples L249-250).

L150 Do you consider 60 min to be the time when the effect of applied stresses no longer varies? Specify this before L192.

Discussion

L230-232 Give references to support your assertion

L233-235 Specify (in the Materials and methods section) how long these diatom strains have been isolated and grown in the laboratory (under what conditions?). See also my comment about light conditions during the acclimation phase.

L237-239 See Courcoul et al (2022 - DOI: 10.1111/1365-2745.14058)

L242-245 For information, IRG is much more toxic than atrazine (another PSII inhibitor). See results and discussion in Dahl and Blanck (1996) and Bérard et al. (2003).

L242-253 Discuss the differences in sensitivity to PSII between the 3 species studied.

L251 Cite references showing ecosystem effects through algae. Starting with work on the selection and destructuring effects of algal communities in relation to exposure to IRG.

L251-253 Here you suggest interactions between herbicide and nutrient effects: that's another subject, you need to clarify or find other references that show significant effects of PSII.

L256-258 Can you cite work on the attenuation by temperature rise of the sensitivity of microalgae and cyanobacteria to PSII inhibitors? (see details in Gomes and Juneau 2017 - doi: 10.3389/fenvs.2017.00050)

Reviewer #2: The manuscript by Bi and colleagues submitted for consideration to Plos One report an experimental study regarding short-term effects of UV radiation and an antifouling compound against marine diatoms with varying temperatures. Several issues can be raised, both substantive and formal, that need to be discussed and addressed before acceptance for publication.

The most critical issue is the absence of analytical control of the experimental irgarol exposure, that is assumed to be equal to 0.4 µg/L. The lack of actual exposure data is emphasized as a recurrent issue in experimental evaluation of herbicide toxicity to phytoplankton (see for example the review by Hanson et al. 2019 https://doi.org/10.1016/j.scitotenv.2019.04.336 for atrazine). Without analytical control of irgarol concentration (at least in solvent solution) repeatability and overall strength of the study is flawed. The authors need to address this problem, either by providing actual concentration data or by discussing this point by any means.

I would also raise a general concern about the main direction and conclusions of the submitted manuscript. Authors emphasize the fact that raising temperature decrease the effect of irgarol exposure on photosynthetic potential as measured using variable fluorescence transients. Their conclusions (and the manuscript title) guide readership towards an erroneous view of reduced hazard from marine water herbicide contamination in the frame of global warming. A cautionary discussion is needed, since the experimental procedure here is based on (very) short-term exposure that does not consider adaptation at an individual time scale (i.e. more or less a day, that is a mean doubling time for actively growing diatoms), neither selection of tolerant variants inside a population (at week to month timescale) or competition among phytoplankton populations inside a community in the realm. One should assume that the results presented here are linked to biochemical and toxic-target interactions at very short timescale and that consequences for diatom populations and communities in the field are far from predictable based on these data.

Specific comments:

Title: mentioning here “across latitudes” is confusing, since this was a lab experiment, and maybe a more explicit statement of the provenance of diatom strains would be better suited.

Abstract: I consider that the sentence “These results suggest that elevated temperatures can mitigate…” needs balance or caution, stating that this is correct only at very short term.

References: The introduction section needs more specific references, that can have a global significance and support the current study. I suggest for example considering review papers such as Boyce et al. 2010 (doi:10.1038/nature09268) and / or Tréguer et al. 2018 (10.1038/s41561-017-0028-x) more suited as a context for the present study.

Minor comments:

Lines 91-92: did the authors controlled the cell densities in each culture? Does the current experimental procedure drive each strain to the same overall growth rate?

Lines 98-99: provide more evidence for the absence of effect of DMSO at 0.1% including interactions with temperature – or provide literature references.

Lines 107-108: did the different temperatures resulted in significant differences in observed growth rates?

Line 110: be more specific on acclimation. I assume that 1) temperatures did not change between pre-culture and short term irgarol exposure conditions; 2) the PAR was equal during the two phases; and 3) that changing from polycarbonate bottles to quartz tubes resulted in an UV exposure during short-term experiment. If so, acclimation is encompassing any “bottle effect” and sudden exposure to UVR?

Lines 115-116: technical characteristics of the light filters (material, cutoff lambda…)

Lines 120-124: the Table could be simplified – PAR control / PAB control / PAR + Irgarol / PAB + Irgarol; in current state redundant and confusing.

Line 126: cited reference is for marina waters, quite different from a “typical” coastal environment. Discuss, amend, or provide more references.

Lines 131-133: Light and UVR measurements are more suited for the 2.2. experimental setup section.

Lines 133-136: what is the rationale for choosing a “no dark-adaptation” procedure? What were the biomass / cell densities of each strain for each pre-incubation condition?

Lines 139-following section: give a short explanation of Qy significance (photosynthetic potential?). Consider verifying that the current experiment is actually providing F measurements, not F’ values? I recommend to cite any paper that explain fully the significance of in vivo chlorophyll fluorescence transients – for example Maxwell & Johnson 2000, or any of the numerous ones by Govindjee.

More generally, the authors would have gained information by using the OJIP feature of the AquaPen device, that is able to highlight the different steps of PSII inhibition by herbicide exposure completing Qy evaluation.

Line 148: “U + I” is not defined – see remark above regarding “table” of conditions, and be consistent throughout the manuscript for clarity. Also, why use Y instead of Qy – or precise line 141 that Qy is further noted as Y.

Line 149-150: What is the rationale for the selection of 60-120 minutes exposure to define an average quantum yield?

Line 156-158: since Qy are ratios, it appears not evident that addition of Qy “fractions” is feasible – one should expect that Fm’, or Fo’ can change independently under exposure. Any comment?

Line 185: is there any explanation for a lower Qy in Entomoneis sp.?

Line 222-223: il appears at a shortcut. Does it suggest that UVR and temperature were prone to degrade irgarol as a compound, and / or that the “possible modulation” is to be considered at the metabolic level, where toxicity is compensated by increasing turnover of PSII proteins?

Lines 225-228: this is al least awkward. The gap between the present short-term assessment and global effects with long term pace is extremely wide.

Line 230: Cullen and Lesser 1991 is missing in the reference list.

Line 231: which previous research reports?

Line 237-241: please consider enhancing clarity of this sentence?

Line 249: photosynthetic inhibition or photosynthetic potential? The former needs quantitative assessment, for example using O2 production or CO2 fixation measurements.

Line 253: not fully convinced by the cited references, especially the one about prairie wetlands. See above the example of Boyce et al. 2010 more suited.

Line 260: precise that these studies were on cyanobacteria and chlorophytes – any differences regarding diatom PSII functioning?

Line 261: I really missed the link between the sentence, the Sal et al. reference and what is the intention of the authors here.

Line 264: avoid citing papers without precision – the first one address mixotrophy, and the second one deserves more consideration, since there is also a possible trade-off between herbicide sensitivity, thermal acclimation / adaptation, that could be discussed in the current report.

Table 1: emphasize (bold character) the significant values? And make coherent condition notations throughout. Precise in Table legend that all effects were negative?

Figure 5: harmonize the y axis for all the panels? This would allow a more direct visual comparison of interactions.

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Reviewer #1: No

Reviewer #2: No

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PONE-D-23-24973R1Short-term responses of marine diatoms to Irgarol 1051 and UV radiation: Insights into temperature interactionsPLOS ONE

Dear Dr. Wu,

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 two minor points raised during the review process (1.Addition of some references and 2. Minor change in the title of your paper).

Please submit your revised manuscript by Jan 08 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,

Jean-François Humbert

Academic Editor

PLOS ONE

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.

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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: All comments have been addressed

Reviewer #2: All comments have been addressed

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2. 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

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?

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

Reviewer #2: Yes

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5. 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

Reviewer #2: Yes

**********

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: Authors: there are indeed some publications available for Thalassiosira weissflogii and Skeletonema costatum, while there are relatively fewer studies on Entomoneis sp. It is important to note that comparing the sensitivities of these species can be challenging due to variations in the experimental conditions used in different studies.

My answer: Yes, it's difficult to compare work performed under different conditions, but if there are a lot of studies, similar behaviour can sometimes emerge between them. I think you can at least refer to the publications you're talking about for these species (if only to say that there are a few studies for the first two and fewer data for the last one).

Reviewer #2: I acknowledge the changes, comments and precisions that were included in the revised manuscript, in my opinion making it suitable for acceptance.

I have just one suggestion, to keep an important feature of the presented study - in my opinion - change the title for:

"Short-term responses of temperate and subarctic marine diatoms to Irgarol 1051 and UV radiation: Insights into

temperature interactions"

This would add visibility to this experimental work, but it's optional. Depends on other reviewers comments and Editor advice, no need for further reviewing from my point of view on this precise question.

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7. 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

Reviewer #2: 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.

Short-term responses of temperate and subarctic marine diatoms to Irgarol 1051 and UV radiation: Insights into temperature interactions

PONE-D-23-24973R2

Dear Dr. Wu,

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.

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Kind regards,

Jean-François Humbert

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments: