The cost of endosymbionts on the reproductive fitness of the soft tick Ornithodoros moubata
Influence of endosymbionts on the reproductive fitness of the tick Ornithodoros moubata
Recommendation: posted 28 September 2023, validated 28 September 2023
Gobet, A. (2023) The cost of endosymbionts on the reproductive fitness of the soft tick Ornithodoros moubata. Peer Community In Infections, 100087. 10.24072/pci.infections.100087
Ticks are amongst the most important pathogen vectors in medical and veterinary clinical settings worldwide (Dantas-Torres et al., 2012). Like other holobionts, ticks live in association with a diverse microbiota. It includes tick-borne pathogens (TBP) and other microorganisms that have a beneficial or detrimental effect on the physiology of the host and can also affect the transmission of TBP to animals or humans. In this microbiota, primary endosymbionts, which are obligatory and inheritable, play a role in tick reproduction, the host defense and adaptation to varying environmental conditions (Duron et al., 2018). However, the effect of the microbiota structure and of the endosymbionts on tick fitness and reproduction is not well known. The soft tick Ornithodoros moubata, a parasite known to transmit African swine fever virus (Vial, 2009), is known to host Francisella-like and Rickettsia endosymbionts (Duron et al., 2018). These endosymbionts carry genes involved in B vitamin synthesis which may be supplemented to the host (Bonnet & Pollet, 2021).
Here, the authors investigated the role of endosymbionts on the reproductive fitness of Ornithodoros moubata by conducting two experiments (Taraveau et al., 2023). First, they tested the effect of antibiotic treatment of 366 first-stage nymphs on the main endosymbionts Francisella-like and Rickettsia, and measured the endosymbionts presence overtime by qPCR. Second, they surveyed the effect of antibiotic treatment with or without the addition of B vitamins on the survival and reproductive fitness of 132 females over 50 days. This second experiment intended to identify whether the endosymbionts have an effect on the host reproduction or on its nutrition. The supplementation of B vitamin did not have a drastic effect on tick fitness or reproductive traits. However, antibiotic treatments reduced the presence of endosymbionts while increasing tick survival, suggesting a potential cost of hosting endosymbionts on the tick fitness.
The authors did a lot of work to thoroughly follow the propositions from Dr Raggi, Dr Aivelo and myself to reconstruct and to revise the manuscript. I believe that the manuscript now reads very well and the answers to the reviews also add some value to the manuscript. As Dr Aivelo pointed out, “this study follows the traditional path of so-called population perturbation studies, where ecologists have administered antibiotics or antihelminths to different animals and seen how the community changes and what effects this has on the host fitness and survival”. As both reviewers stated, results from this study are valuable and provide important basic knowledge that will likely help conduct future experiments on tick microbiota. This recommendation is the result of the thorough reviewing work of Dr Aivelo and Dr Raggi which I warmly thank.
Bonnet, S. I., & Pollet, T. (2021). Update on the intricate tango between tick microbiomes and tick‐borne pathogens. Parasite Immunology, 43(5), e12813. https://doi.org/10.1111/pim.12813
Dantas-Torres, F., Chomel, B. B., & Otranto, D. (2012). Ticks and tick-borne diseases: A One Health perspective. Trends in Parasitology, 28(10), 437–446. https://doi.org/10.1016/j.pt.2012.07.003
Duron, O., Morel, O., Noël, V., Buysse, M., Binetruy, F., Lancelot, R., Loire, E., Ménard, C., Bouchez, O., Vavre, F., & Vial, L. (2018). Tick-Bacteria Mutualism Depends on B Vitamin Synthesis Pathways. Current Biology, 28(12), 1896-1902.e5. https://doi.org/10.1016/j.cub.2018.04.038
Taraveau, F., Pollet, T., Duhayon, M., Gardès, L., & Jourdan-Pineau, H. (2023). Influence of endosymbionts on the reproductive fitness of the tick Ornithodoros moubata. bioRxiv, ver.3, peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.05.09.539061
Vial, L. (2009). Biological and ecological characteristics of soft ticks (Ixodida: Argasidae) and their impact for predicting tick and associated disease distribution. Parasite, 16(3), 191–202. https://doi.org/10.1051/parasite/2009163191
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
Ecology and Evolution of Infectious Diseases Program, grant no. 2019-67015-28981 from the USDA National Institute of Food and Agriculture, project “unraveling the effect of contact networks & socio-economic factors in the emergence of infectious diseases at the wild-domestic interface” (https://www.asf-nifnaf.org/)
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2023.05.09.539061
Version of the preprint: 2
Author's Reply, 06 Sep 2023
Decision by Angélique Gobet, posted 26 Jul 2023, validated 26 Jul 2023
Thank you for submitting your manuscript for a recommendation from PCI. I would like to apologize for the time taken to hand in the reviews and my recommendation. The two reviewers and I made some comments that I feel should be addressed to improve the manuscript. I hope the comments and suggestions will be of interest to the authors and help improve the manuscript. I look forward to receiving a revised version of the manuscript.
Overall, the manuscript is well written but some parts may need some rearrangements to help the reading of the manuscript.
A general comment that has also been noted by Dr Raggi is that, when the authors used the term “microbiota”, it is not clear whether they refer only to the targeted endosymbionts or to the whole microbial community associated with the ticks. In the text, it becomes clear only in the discussion L345-347, so the authors may be more specific earlier in the text.
The experimental set-up is very thorough but as suggested by Dr Aivelo, some rearrangements of the text may help the reading. For instance, in figure 1, the authors may assign a number to the different steps of the experiment and then refer to each step in the text.
As Dr Aivelo suggested, some parts of the discussion may be trimmed and rearranged in other parts of the manuscript to make the reading easier.
Please find below some specific comments complementary to those from the 2 reviewers:
L19-21: This sentence may be rephrased. With the later sentence introducing the prevalence of the endosymbionts, it is not clear whether the authors followed the whole microbiota or only the two endosymbionts.
L87: Are the “main bacterial species” Francisella-like and Rickettsia endosymbionts? Please specify.
L92: Materials and methods should be written in the past tense.
L102: I was wondering if it would be of interest to specify if these stages were only female or of both sexes.
L103-104: Can the process of blood feeding be a source of potential DNA or microbial contamination that would impact the study? Were there adequate precautions taken?
L110-112: Are the antibiotics known to have an effect on the 2 targeted endosymbionts? Please specify somewhere in the text.
L113, L147: Was the Milli-Q water UV treated or treated in order to avoid DNA contamination? Would not molecular grade water be more adequate to further use a DNA-based molecular approach?
L156: It would be more informative to give a range of DNA concentration than the volume.
L358: There is a typing mistake: “target*ed”.
L358-361: This information should be put earlier in the text to understand the antibiotic choice.
Figures 2, 3, 4: This is a minor comment but instead of writing “boxplot of”, “histogram of”, the authors may directly write the title, for instance: “Ratios of DNA concentration…”.