Genomic investigations of diverse corbiculate bee gut-associated Gilliamella reveal conserved pathways for energy metabolism, with diverse and variable energy sources

  1. Viet Hung Nguyen

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Abstract

Gilliamella is a genus of bacteria commonly found as symbionts of corbiculate bees. Research into energy metabolism by this genus has predominantly been done through in vivo and in vitro experiments focused on the type species Gilliamella apicola . This study examined 95 publicly available genomes representing at least 18 Gilliamella species isolated predominantly from the hindgut of corbiculate bees. Energy metabolism pathways were found to be highly conserved across not only the Gilliamella but also other members of the family Orbaceae . Evidence suggests Gilliamella are capable of fermentation of both fumarate and pyruvate. Fermentation of the former produces succinate. Fermentation of the latter can produce acetate, ethanol, formate, and both isoforms of lactate for all Gilliamella and acetoin for some G. apicola strains. According to genomic evidence examined, all Gilliamella are only capable of respiration under microoxic conditions, while higher oxygen conditions likely inhibits respiration. Evidence suggests that the glycolysis and pentose phosphate pathways are essential mechanisms for the metabolism of energy sources, with the TCA cycle playing little to no role in energy metabolism for all Gilliamella species. Uptake of energy sources, i.e. sugars and derivatives, likely relies predominantly on the phospho enol -pyruvate-dependent phosphotransferase system. Differences in the utilized energy sources may confer fitness advantages associated with specific host species.

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  1. Version published to 10.1099/acmi.0.000793.v3 on Access Microbiology
  2. Access Microbiology

    The work presented is clear and the arguments well formed. This study would be a valuable contribution to the existing literature. This is a study that would be of interest to the field and community.

  3. Access Microbiology

    Comments to Author

    I have carefully reviewed the responses and revisions provided by the authors in response to my comments. I appreciate the thoroughness of the changes implemented and the clarifications provided throughout the manuscript. The authors have adequately addressed all the concerns I raised, adding significant value and clarity to the manuscript. The additional experiments and data presented have strengthened the arguments and enhanced the overall scientific rigor of the study. The effort made to clarify complex points and the inclusion of more detailed explanations are particularly commendable and have successfully resolved the issues I highlighted in my initial review. Therefore, I am satisfied with the revisions made and support the publication of the manuscript in its current form. I believe the paper will make a valuable contribution to the field and stimulate further research. Thank you for the opportunity to review this work and for considering my suggestions.

    Please rate the manuscript for methodological rigour

    Good

    Please rate the quality of the presentation and structure of the manuscript

    Good

    To what extent are the conclusions supported by the data?

    Strongly support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  4. Access Microbiology

    Comments to Author

    The explanations and notifications about the observations made in the article seem appropriate and sufficient to maintain the points under discussion as the author suggests, so for my part I totally agree to the article being published in the submitted version.

    Please rate the manuscript for methodological rigour

    Very good

    Please rate the quality of the presentation and structure of the manuscript

    Very good

    To what extent are the conclusions supported by the data?

    Strongly support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  5. Version published to 10.1099/acmi.0.000793.v2 on Access Microbiology
  6. Access Microbiology

    The work presented is clear and the arguments well formed. This is a study that would be of interest to the field and community. The reviewers have highlighted minor concerns with the work presented. Please ensure that you address their comments. Please provide more detail in the Methods section and ensure that software is consistently cited and its version and parameters included.

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    Comments to Author

    Review for Viet Hung Nguyen et al This study delves into the energy metabolism of Gilliamella bacteria in corbiculate bee guts, analyzing 95 genomes from various species. It uncovers highly conserved energy metabolism pathways within the genus and the Orbaceae family, indicating Gilliamella's ability for microaerophilic respiration and fermentation of multiple substrates, but not for fully aerobic or anaerobic respiration. The research emphasizes the crucial roles of glycolysis and the pentose phosphate pathways, with minimal involvement of the TCA cycle. The findings suggest potential fitness advantages for Gilliamella in associating with specific bee species. This comprehensive genomic analysis enhances the understanding of Gilliamella's ecological roles and energy metabolism, laying groundwork for future research on its activities beyond the bee gut and in sugar metabolism, although it calls for further experimental validation. However I have several concerns which are given below Line 14 The use of "here" is colloquial and might be replaced with "in this study" for a more formal tone. Line 18 The abstract should avoid expressions that imply uncertainty like "seem to be capable". And I did not understand this statement microaerophilic, but not fully aerobic or anaerobic respiration. Line 23 Rephrase "Differences in potential energy sources utilized may represent fitness advantages associating with specific host species." To Differences in the utilized energy sources may confer fitness advantages associated with specific host species. Line 24: "Associating with specific host species" could be rephrased to "associated with specific host species." Line 131-134: The sentence is quite long and packed with information. Consider breaking it into two sentences for better readability, e.g., "Respiration involves a redox reaction where electrons are transferred from an electron donor to a terminal electron acceptor. This process is facilitated by membrane-bound enzymes and enzymatic complexes, coupled with cation translocation across the cell membrane, to generate an electrochemical gradient that drives ATP synthesis via an F-type ATP synthase." Line 138 ETC Give full form first then abbreviate. Line 139 Rephrase the sentence. All genes except one necessary for the biosynthesis of chorismate via the shikimate pathway, prenyl diphosphate and 3-methylbut-2-en-1-yl diphosphate via the methylerythritol pathway, and then subsequent anaerobic biosynthesis of ubiquinone-8 from these precursor compounds were identified in all 95 genomes examined. The above sentence is a bit lengthy and contains a lot of technical detail, which can make it challenging to follow. Here's a revised version for clarity and conciseness: "In all 95 genomes studied, we identified nearly all genes required for the biosynthesis of ubiquinone-8: those catalyzing chorismate formation via the shikimate pathway, prenyl diphosphate and 3-methylbut-2-en-1-yl diphosphate via the methylerythritol pathway, and the subsequent anaerobic synthesis from these precursors (refer to Supplementary Figure S1). Line 179 You started the sentence with frdA, frdC, and frdD Briefly describe the importance if frdA in anaerobic respiration for general reader. Lines 321-327- The explanation of the phylogenetic relationship involving the ptsH gene is dense and could be challenging for readers to follow. It might benefit from a more simplified and step-by-step explanation of these relationships and what they imply about the evolutionary history of the taxa involved. Lines 331-337: The text presents the hypothesis of an HGT event but does not detail the evidence supporting this hypothesis. As HGT can significantly impact the understanding of bacterial evolution, further explanation or evidence to support this claim would be essential for the reader. Lines 338-342 While it is stated that the presence of the ptsH homologs suggests an important role, a more in-depth discussion of their possible functions, or even hypothetical roles based on their activity in related species, would enrich the narrative. Line 425 remove "an" from the sentence therefore Gilliamella glycolysis plays an all the more important role in energy metabolism.

    Please rate the manuscript for methodological rigour

    Good

    Please rate the quality of the presentation and structure of the manuscript

    Satisfactory

    To what extent are the conclusions supported by the data?

    Strongly support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  8. Access Microbiology

    Comments to Author

    Overall, the paper is written very well, and the analysis conducted is comprehensive. The author presents a compelling argument regarding the energy metabolism of Gilliamella within the bee gut. I don't think there are any additional analysis needed to improve on what they have done. Well done! There are some minor grammatical error across the paper (missing articles [mechanisms for *the* metabolism of energy sources] and misused of past tense [The author declares no data deposition into repositories *was* required]). I would recommend the author use a programme like grammarly to detect and correct these. Some questions/comments I had while reading the manuscript are as follows: 1. Bacteria (in general) do not exist homogeneously across populations, especially if they are continuously seeded from the environment. One could imagine a dynamic nature fluctuating between different strains of Gilliamella in the gut. This could explain some of the high strain heterogeneity in the genome that was removed from the analysis. It might be interesting to examine the read coverage over the energy metabolism genes of these genomes to see if there is a reduction in read coverage. This might indicate that not all of the strains contain full copies of the genes needed for synthesis and are reliant on the population to provide the energy needed to survive. 2. What about co-occurring bacterial species found in the bee gut? By utilizing shotgun metagenomics in the bee gut, you should be able to quantify the metabolic capacity of the environment. This would provide the evidence needed to show that what you observed in the genus is also present in the bee gut, particularly if the genome is compensated by other bacteria found within the environment. As you have presented, I believe the comments I have written could help in obtaining more evidence (without conducting experimental work) to validate your findings. I do not think it is necessary for this publication, but I think they can help strengthen the evidence you are presenting.

    Please rate the manuscript for methodological rigour

    Very good

    Please rate the quality of the presentation and structure of the manuscript

    Very good

    To what extent are the conclusions supported by the data?

    Strongly support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  9. Access Microbiology

    Comments to Author

    In general, the article has the virtues of integrating bioinformatics advances with the evolutionary history of Gialliamella symbionts genus and corbiculate bees. I consider my observations to be minor revisions. It seems very appropriate to me that the figures of phylogeny metabolic routes are part of the complementary file, however I would like you to manage to integrate a figure with the general panorama, I send you a proposal. And a phylogenomic tree with only the 95 genomes used in the study and 2 of outgroup genomes of Orbaceae. On the other hand, in the complementary phylogenetic trees, it seems to me that they use too many sequences from very distant genera such as E. coli, and they collapse the Gialliamella branches, which are of more interest, take a closer look at that clade, within the same figure. Sugar/energie/fermentation Metabolic rutes/sources Egg Larva Young Adult Old adult Free lifestyle microaerophilic, not fully aerobic, anaerobic respiration Figure X. General panoramic interactome of metabolism between Gialliamella symbionts genus and corbiculate bees

    Please rate the manuscript for methodological rigour

    Very good

    Please rate the quality of the presentation and structure of the manuscript

    Very good

    To what extent are the conclusions supported by the data?

    Strongly support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  10. Version published to 10.1099/acmi.0.000793.v1 on Access Microbiology