Ir para a Avaliação PREreview

Avalilação PREreview de The broad-spectrum RumC1 bacteriocin targets a transient peptidoglycan intermediate of the nascent cell wall

Publicado
DOI
10.5281/zenodo.19637706
Licença
CC BY 4.0

The manuscript by Boyeldieu et al. explores the cell-wall poisoning mechanism of the RumC1 bacteriocin, produced by Ruminococcus gnavus E1. The authors developed an ordered genome-wide mutagenesis strategy in Streptococcus pneumoniae to identify RumC1-resistant mutants. These studies helped confirm RumC1's inhibition of transpeptidase activity, thereby blocking peptidoglycan (PG) synthesis and cell growth. The selective binding of RumC1 to the nascent PG had not been reported before. They also identified the immunity protein RumIc1 from the RumC1 biosynthetic gene cluster as sufficient to counteract RumC1 toxicity in S. pneumoniae. The findings reported in this study have exciting implications for antimicrobial resistance, potentially shifting the paradigm for treating infections caused by multidrug-resistant pathogens. Overall, the data in this manuscript is well presented and supports the authors' claims. We enjoyed reading this manuscript and outline major and minor adjustments to improve clarity in reporting and presentation, as well as providing additional context for a broader audience.

Major comments

- Figure 1D shows the morphology and HADA incorporation in WT and Rum1C-resistant mutants. In lines 206-208, you mention that Rum1C-resistant mutants show reduced HADA labeling; it would be helpful to include fluorescence quantification, as represented in Figure 6. Similarly, for Figures 2C and D, consider incorporating the quantification for cell width. It will also help support the results mentioned in lines 251-258. For instance, quantification of cellular morphology would provide clear evidence of “effects of RumC1 on cell morphology and PG synthesis differ from those caused by vancomycin”.

- To strengthen the conclusion that variants of RumIc1 do not confer immunity, consider including evidence that the protein variants are stable by showing an immunoblot. Along this line, please provide immunoblots for the strains used in Figure 4 and onwards, in which genes are expressed from an ectopic promoter site.

Minor comments

-All figures: Consider color coding the name of the strain and applying this color-coding across figures to improve reader comprehension.

-Ensure all supplementary figures are referred to in the main text.

-Statistic data representation: Consider changing “,” to “.” for the p values.

-The introduction is well written. A description of WalR and WalK and how they play a role in PG homeostasis would benefit non-initiated readers.

-RumC1 exhibits antibacterial efficacy against monoderm and LPS-poor strains, and an unencapsulated strain of Spn was used for this study. We understand how difficult it would have been to use an encapsulated strain for this work as they are more genetically recalcitrant, but clinically all pathogenic strains have a capsule. Please consider including discussion on the potential impact of RumC1 on an encapsulated strain.

-Figure 1F: The controls were appropriate and nicely contextualizes RumC1 stress induction; Bacitracin targets undecaprenyl pyrophosphate (membrane carrier for cell wall precursors) which serves as a positive control and kanamycin, which targets protein synthesis, serves as a negative control. Please consider including this information in the legend.

-Line 272: A little more background is needed about peptidoglycan (PG) synthesis, especially before mentioning the nascent PG.

-Figure 4: At 0.4 µM RumC1, explain why rumIc2 is having a lag? Why are MIC and growth curves not corresponding?

-Figure S9: How was the highest immunity achieved when all the immunity proteins were co-expressed? How did RumIc2 become neutral?

-Figure 5C: Comment on the trend of growth of the strains at 0.4 µM RumC1 after 16 h, it appears that strains have started to grow again, likely because of suppressors. Consider including the growth curve for 24 h for clarity.

-Figure 6F: Please explain how the cleavage sites from MD simulation were predicted.

-Adding a few sentences in the discussion of how much RumC1 may be produced in the gut would be of interest, as well as speculation to what its effect on the gut microbiome may be.

- Figure 1C: Consider modifying the color of the control (WT) so it’s clearly apparent that 0.6 µM RumC1 results in no growth.

-Figure 1D: WT has debris; consider picking another field or enhancing the brightness.

-Figure 1E: spr1875 appears to be a little stretched in the X axis.

-Figure S3D: Please consider using in-text citations of Figure S3C and Figure S3D. Moreover, please provide an explanation of Figure S3D, in which the WT strain, when incubated with RumC1, shows lower expression of pcsB and spr1875 or is it a mislabeling?

-Figure 6A: Consider color coding the last 2 D-Alanine in the model where the cleavage is happening.

-Line 290: Consider defining sacculus and protoplast.

-Lines 121, 141, 252: Missing references.

-Line 200: Fluorescent microscopy should be changed to fluorescence microscopy.

-Line 410: Points mutants should be changed to point mutants.

-Figure S4: Please consider including the time of treatment on the graph for clarity.

-Line 231: Refer to Figure S5C to improve clarity.

-Figure 6C: This panel is not mentioned in the main text.

Josy Joseph and Tahreem Zaheer (Indiana University Bloomington) - not prompted by a journal; this review was written within a Peer Review in Life Sciences graduate course led by Alizée Malnoë with input from group discussion including Carter Collins, Camy Guenther and Lily Pumphrey. We are part of the Dept. of Biology where Malcolm E. Winkler’s group is located. Malcolm is a co-author on a publication in which one of the authors (Cécile Morlot) provided antibodies; this prior interaction did not influence the choice of this preprint for our class.

Competing interests

The authors declare that they have no competing interests.

Use of Artificial Intelligence (AI)

The authors declare that they did not use generative AI to come up with new ideas for their review.

Comentários

Escrever um comentário
  1. Comment by Patrice Polard

    Publicado
    Licença
    CC BY 4.0

    Dear Alizée Malnoë, Tahreem Zaheer, Josy Joseph, Carter Collins, Camryn Guenther, and one anonymous author of IU Bloomington Biology

    Thank you for reviewing our manuscript and providing your comments in a peer-review format, following the editorial procedure commonly used by scientific journals. Your analysis is a very helpful complement to improve the presentation and clarity of our work, and it also provides an initial assessment of our study with the same public visibility as that offered by bioRxiv.

    We are particularly grateful for your very positive feedback on our fundamental and integrative study that we conducted in S. pneumoniae to unveil the unprecedented modes of action of the bacteriocin RumC1 and of its cognate immunity protein RumIc1. In addition, we were delighted to read your assessment of the importance of our study in the frame of the global antibiotic resistance crisis, and the emergency to develop innovative tools to fight against multi-drug pathogenic bacteria.

    Below, we respond to your comments in detail for the two major points and more generally for the minor points you raised.

    Major comments

    Point #1: … it would be helpful to include fluorescence quantification, as represented in Figure 6. Similarly, for Figures 2C and D, consider incorporating the quantification for cell width….

    You are absolutely right to raise these points, which are fully feasible. We will perform these fluorescent and cell-shape quantifications and include them in the final revised version of the manuscript.

    Point #2: To strengthen the conclusion that variants of RumIc1 do not confer immunity, consider including evidence that the protein variants are stable by showing an immunoblot…

    Addressing this point rigorously would require either (i) generating antibodies against RumIc1, or (ii) engineering functional immuno-tagged fusions of the WT and point-mutant RumIc1 proteins, followed by Western blot analysis of total cell extracts to demonstrate that the mutations do not destabilize the protein, but specifically impair its proteolytic activity. Importantly, both approaches are not fully guaranteed to succeed (e.g., the antibodies might lack sensitivity, and the tagged WT fusion might not be functional). For these reasons, we instead chose to provide direct biochemical evidence that RumIc1 has proteolytic activity, which is the primary objective of its functional characterization. As shown in Fig. 6C, RumIc1 clearly displays proteolytic activity. In addition, the RumIc1 point mutant that we purified to demonstrate processing of the pentapeptide in this experiment was produced at levels comparable to the WT protein and showed similar solubility when expressed in E. coli, which generally indicates that the mutation does not affect the overall fold of the protein and is unlikely to compromise its stability.

    Minor comments

    Thank you very much for this well-organized list of minor points, which will help us improve the final version of the manuscript. As mentioned above, we will not provide here a point-by-point reply (as typically done in response to referees’ comments during journal peer review process); instead, when appropriate, most of your suggestions will be incorporated into the revised and finalized version after acceptance.

    In particular, we appreciate your identification of errors in the text and figures, which will be corrected. We also noted your suggestion to explain more clearly what is known about WalRK, which we will address in the revised manuscript. Finally, we understand the proposal to include a capsulated strain of S. pneumoniae in the analysis; however, it is known and published that capsulated strains of S. pneumoniae are sensitive to RumC1. Thus, including a capsulated strain (more difficult to manipulate as you acknowledge) would have substantially expanded the manuscript focused on the functional analysis of RumC1 and RumIc1 to characterize their mode(s) of action. To this end we selected our laboratory strain of S. pneumoniae as powerful ‘genetical chassis’ and an advanced model for single-cell microscopy analysis for such analysis. Nonetheless, now that we know that RumC1 interacts and interferes with PG homeostasis, an important perspective is to pursue its analysis in other sensitive pneumococcal strains with different cell envelopes.

    In conclusion, we warmly thank you for taking the time to select and peer-review our manuscript and, again, for your very positive feedback on our work. Your comments support our study describing the novel antibacterial mode of action displayed by the RumC1 bacteriocin, together with the unique self-protection provided by the immunity protein RumIc1, both targeting the synthesis and maturation of the peptidoglycan – two discoveries that define the take-home message of our manuscript.

    Patrice Polard

    Competing interests

    The author of this comment declares that they have no competing interests.