A model for microbial interactions and metabolomic alterations in Candida glabrata-Staphylococcus epidermidis dual-species biofilms

Maria Michela Salvatore; Angela Maione; Alessandra La Pietra; Federica Carraturo; Alessia Staropoli; Francesco Vinale; Anna Andolfi; Francesco Salvatore; Marco Guida; Emilia Galdiero

doi:10.1371/journal.pone.0279069

Peer Review History

Original SubmissionJuly 21, 2022
14 Oct 2022 Decision Letter - Joy Sturtevant, Editor PONE-D-22-20604Microbial Interactions and Metabolomic Alterations in Candida glabrata-Staphylococcus epidermidis Dual-Species BiofilmsPLOS ONE Dear Dr. Galdiero, 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. ============================== We are sorry it has taken so long to respond. There has been difficulty getting reviewers and several researchers as well as a proposed reviewer felt that the manuscript was asking a question about an interrelationship that does not physiologically exist. Additionally it was felt that C. glabrata is not a good biofilm maker. Indeed your studies really address dual species interaction and not necessarily in a biofilm. Consequently in the discussion you might include a few sentences on how your data would the interrelationship between the two species even if biofilms werent formed and why this would be important. Reviewer 1 asks for more samples but I realize these experiments are usually only done with one strain - so you should comment in discussion that these results are for only 1 strain and differences may exist since it is known that the ability to make biofilms can be strain dependent. Please ensure that your decision is justified on PLOS ONE’s publication criteria and not, for example, on novelty or perceived impact. ============================== Please submit your revised manuscript by Nov 28 2022 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. 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If you have no competing interests, please state "The authors have declared that no competing interests exist.", as detailed online in our guide for authors at http://journals.plos.org/plosone/s/submit-now This information should be included in your cover letter; we will change the online submission form on your behalf. 4. 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. [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 article entitled " Microbial Interactions and Metabolomic Alterations in Candida glabrata-Staphylococcus epidermidis Dual-Species Biofilms " is interesting and presents excellent results. The aim of the study is appropriate and novelty in polymicrobial infections field. The study is carried out in a very exhaustive way, both in the application of various techniques for the characterization of polymicrobial biofilms and in their discussion. This is an interesting, comprehensive and well-designed document, and I recommend it for publication. However, I have some considerations to make: Comments/Questions: - The sample number is low, would it be possible to increase the number of isolates? Why, use the authors a clinical isolate of Staphylococcus epidermidis and a reference strain of Candida glabrata? More strains of C. glabrata and S. epidermidis should be used! - Line 182: "Sample preparation", the first two paragraphs are repetitive - I think the data in table 2 would be more easily perceptible in graph. - The quality of the imagens in figures should be improved. ****** 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.0279069.r001
Revision 1
21 Oct 2022 Author Response Editor: We are sorry it has taken so long to respond. There has been difficulty getting reviewers and several researchers as well as a proposed reviewer felt that the manuscript was asking a question about an interrelationship that does not physiologically exist. Additionally it was felt that C. glabrata is not a good biofilm maker. Indeed your studies really address dual species interaction and not necessarily in a biofilm. Consequently in the discussion you might include a few sentences on how your data would the interrelationship between the two species even if biofilms werent formed and why this would be important. Author response: We wish to thank the academic editor for the comments and useful suggestions. Editor: Reviewer 1 asks for more samples but I realize these experiments are usually only done with one strain - so you should comment in discussion that these results are for only 1 strain and differences may exist since it is known that the ability to make biofilms can be strain dependent. Author response: According to the academic editor suggestion, text were added in the conclusion section to better explain the focus and relevance of our study which could be of wide general interest to the field of polymicrobial infections. Furthermore, as required by the editor, we also explicitly specified the strain dependence of our findings (see lines 835-845). We have added text in the conclusion rather than in the discussion since we consider extension of our approach to the investigation of polymicrobial biofilm formation and growth to other strains and microbial species to be the object of future research. Reviewer 1: This article entitled " Microbial Interactions and Metabolomic Alterations in Candida glabrata-Staphylococcus epidermidis Dual-Species Biofilms " is interesting and presents excellent results. The aim of the study is appropriate and novelty in polymicrobial infections field. The study is carried out in a very exhaustive way, both in the application of various techniques for the characterization of polymicrobial biofilms and in their discussion. This is an interesting, comprehensive and well-designed document, and I recommend it for publication. Author response: We wish to thank the reviewer for the positive comments and useful suggestions to improve the manuscript. Reviewer 1: However, I have some considerations to make: Comments/Questions: - The sample number is low, would it be possible to increase the number of isolates? Why, use the authors a clinical isolate of Staphylococcus epidermidis and a reference strain of Candida glabrata? More strains of C. glabrata and S. epidermidis should be used! Author response: The focus of this manuscript is to understand if there was an interaction at biological and metabolomic level between C. glabrata and S. epidermidis in the polymicrobial environment. To achieve this goal we had, by necessity rather than by choice, to select a specified strain of each microorganism since, as all microbiological results, our findings may be strain dependent. This is in fact the reason why in Materials and Methods there is a precise information about the strains employed. In the revised version of the manuscript, we explicitly mentioned in the conclusion this aspect of our data and results. Comparing biological and metabolic characteristics of several strains of C. glabrata and S. epidermidis is outside of the scope of this paper although we consider it an excellent idea for future research. Reviewer 1: Line 182: "Sample preparation", the first two paragraphs are repetitive Author response: As suggested by the reviewer, in the revised version of the manuscript a few sentences were merged to avoid repetitions and, furthermore, the paragraphs “Sample preparation” and “GC-MS analysis” were combined in only one paragraph named “Sample preparation and GC-MS analysis” in which the essential information concerning sample preparation, derivatization before GC-MS analysis, the instrumental method and the number of replicates were reported (see lines 183-206) . Reviewer 1: I think the data in table 2 would be more easily perceptible in graph. Author response: As suggested by the reviewer, in the revised version of the manuscript Table 2 was replaced with a figure which was numbered as Figure 2 and, therefore, all subsequent figures and tables were renumbered. Reviewer 1: The quality of the imagens in figures should be improved. Author response: As suggested by the reviewer, the quality and general aspect of all the figures were scrutinized and their quality greatly improved. A few images were restyled to make their content clearer. All images are provided in .tif format 300×300 pixel/in Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0279069.r002
10 Nov 2022 Decision Letter - Marcos Pileggi, Editor PONE-D-22-20604R1Microbial Interactions and Metabolomic Alterations in Candida glabrata-Staphylococcus epidermidis Dual-Species BiofilmsPLOS ONE Dear Dr. Galdiero, 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. Authors should take into account the reviewers' observations, especially in relation to the conclusion drawn from experiments carried out only in microbiological media. Please submit your revised manuscript by Dec 25 2022 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, Marcos Pileggi, Ph.D Academic Editor PLOS ONE [Note: HTML markup is below. Please do not edit.] 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: (No Response) ******** 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: Partly ****** 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 ****** 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: (No Response) Reviewer #2: The main drawback of this manuscript is about the conclusion drawn from the experiments carried out on just microbiological media. The authours claim that the choice of the strains are do to its prevalence in skin infections. So I strongly suggest that the metabolome study and gene regulation studies should be carried out using a simulated environment like a wound medium or a simulated wound infection model ****** 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. https://doi.org/10.1371/journal.pone.0279069.r003
Revision 2
15 Nov 2022 Author Response Editor: Authors should take into account the reviewers' observations, especially in relation to the conclusion drawn from experiments carried out only in microbiological media. Answer: We thank the academic editor for considering our paper. We have carefully considered the Reviewer#2 observations concerning the use of a standard medium for growing single and dual species biofilms of C.glabrata/S. epidermidis biofilms. You can see our reply to this question in the Cover Letter and below in the answer to Reviewer#2. Reviewer#1: “This article entitled " Microbial Interactions and Metabolomic Alterations in Candida glabrata-Staphylococcus epidermidis Dual-Species Biofilms " is interesting and presents excellent results. The aim of the study is appropriate and novelty in polymicrobial infections field. The study is carried out in a very exhaustive way, both in the application of various techniques for the characterization of polymicrobial biofilms and in their discussion. This is an interesting, comprehensive and well-designed document, and I recommend it for publication.” Answer: We thank the Reviewer for the positive comments. Reviewer#2: “The main drawback of this manuscript is about the conclusion drawn from the experiments carried out on just microbiological media. The authours claim that the choice of the strains are do to its prevalence in skin infections. So I strongly suggest that the metabolome study and gene regulation studies should be carried out using a simulated environment like a wound medium or a simulated wound infection model” Answer: We thank the Reviewer for his/her observation which we have carefully considered. We understand that the main concern of the Reviewer is on the use of a standard microbiological medium (TSB medium supplemented with 1% glucose) to grow single and dual-species biofilms of the targeted microorganisms which, according to the Reviewer, is the “main drawback” of the manuscript. We respectfully observe that a standard microbiological medium is used in most of the literature dealing with the study of single species and polymicrobial biofilms of pathogenic microorganisms and this is a “choice” rather than a “drawback”. For instance, in the list of references in our paper there are not less than 10 papers which demonstrate this fact (see for instance Reference 31: [Huffines, J. T., & Scoffield, J. A. (2020). Disruption of Streptococcus mutans and Candida albicans synergy by a commensal streptococcus. Scientific reports, 10(1), 1-10)]. Obviously, the medium can be enriched with components (biological fluids or tissue fragments, etc.) whose function is to simulate the biochemical environment of specific infected tissues or medical devices. Both approaches are legitimate, and the choice depends on the objectives pursued. In our manuscript we consider for the first time the biological and metabolic changes in the interaction of C. glabrata-S. epidermidis during biofilm formation, and the scope of our work is to collect information on fundamental biological and metabolic effects of this interaction. Although we have selected the microorganisms considering their role in real-world infections, it is perfectly reasonable to consider first their interaction when they are cultivated in vitro in a standard medium which contains only the ingredients necessary to ensure wellness of both microorganisms in order to trace a groove for future research. Data collected under such conditions will not provide a definitive and universal model which can be applied without changes in all real-world situations but will give fundamental information which may be useful as a guide for further studies. In fact, in this field there is nothing like a universal model since any model is to some extend contingent and dependent on the data and conditions under which it was developed. The list of factors which may influence the model is very long and includes, among others, the strains of the microorganisms, the nature of the surface on which biofilms are deposited, the composition of the medium and the presence of exogenous substances which may or may not be present. This is because, in a specific work, factors which may influence the outcome of experiments must be accurately specified and controlled (as we did in our work). In other words, each model represents only one tooth of a gear and we do not pretend that our work represents the whole gear, but we do pretend that it represents a single tooth of the gear. The Reviewer suggestion of carrying out experiments using an environment simulating real-world infections is welcome since it is exactly what we are going to do in the continuing work, but it is, by definition, outside of the scope of the present work. In any case we have accurately scrutinized the manuscript and made changes and added text and references to better specify its significance and further support our conclusions based on the presented data. - We have modified the title to “A Model for Microbial Interactions and Metabolomic Alterations in Candida glabrata-Staphylococcus epidermidis Dual-Species Biofilms” which makes evident that the outcome of our paper is a basic model for the interactions between C. glabrata/S. epidermidis biofilms. -By pursuing the same objective, we have substantially modified the “Introduction” and added text to better delineate the ambit and significance of our results. - To better support our conclusions and to better connect them to previous studies, we have added further references and added text in the “Results” sections. -We have also modified the “Conclusions” to make the significance of our work clearer. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0279069.r004
1 Dec 2022 Decision Letter - Marcos Pileggi, Editor A Model for Microbial Interactions and Metabolomic Alterations in Candida glabrata-Staphylococcus epidermidis Dual-Species Biofilms PONE-D-22-20604R2 Dear Dr. Galdiero, 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 for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, 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, Marcos Pileggi, Ph.D Academic Editor PLOS ONE Additional Editor Comments (optional): 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 #2: All comments have been addressed ******** 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 #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? 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 #2: Yes ****** 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 #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 #2: (No Response) ****** 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 #2: No ******** https://doi.org/10.1371/journal.pone.0279069.r005
Formally Accepted
4 Dec 2022 Acceptance Letter - Marcos Pileggi, Editor PONE-D-22-20604R2 A Model for Microbial Interactions and Metabolomic Alterations in Candida glabrata-Staphylococcus epidermidis Dual-Species Biofilms Dear Dr. Galdiero: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. 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 plosone@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. Marcos Pileggi Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0279069.r006

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