Host genetic selection for cold tolerance shapes microbiome composition and modulates its response to temperature

  1. Fotini Kokou
  2. Goor Sasson
  3. Tali Nitzan
  4. Adi Doron-Faigenboim
  5. Sheenan Harpaz
  6. Avner Cnaani
  7. Itzhak Mizrahi  Is a corresponding author
  1. Ben-Gurion University of the Negev, Israel
  2. Agricultural Research Organization, Israel

Abstract

The hologenome concept proposes that microbes together with their hosting organism are an independent unit of selection. Motivated by this concept, we hypothesized that thermal acclimation in poikilothermic organisms is connected to their microbiome composition due to their inability to maintain their body temperature. To test this hypothesis, we used a unique experimental setup with a transgenerational selective breeding scheme for cold tolerance in tropical tilapias. We tested the effects of the selection on the gut microbiome and host transcriptomic response. Interestingly, we found that host genetic selection for thermal tolerance shapes microbiome composition and its response to cold. The microbiomes of cold-resistant fish showed higher resilience to temperature changes, indicating that the microbiome is shaped by its host's selection. These findings are consistent with the hologenome concept and highlight the connection between the host and its microbiome's response to the environment.

Data availability

Data has been deposited in the SRA under accession code SRP131209.

The following data sets were generated

Article and author information

Author details

  1. Fotini Kokou

    Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Goor Sasson

    Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Tali Nitzan

    Department of Poultry and Aquaculture, Institute of Animal Sciences, Agricultural Research Organization, Rishon LeZion, Israel
    Competing interests
    The authors declare that no competing interests exist.
  4. Adi Doron-Faigenboim

    Department of Vegetable and Field Crops, Institute of Plant Science, Agricultural Research Organization, Rishon LeZion, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Sheenan Harpaz

    Department of Poultry and Aquaculture, Institute of Animal Sciences, Agricultural Research Organization, Rishon LeZion, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Avner Cnaani

    Department of Poultry and Aquaculture, Institute of Animal Sciences, Agricultural Research Organization, Rishon LeZion, Israel
    Competing interests
    The authors declare that no competing interests exist.
  7. Itzhak Mizrahi

    Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva, Israel
    For correspondence
    imizrahi@bgu.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6636-8818

Funding

European Research Council (Grant 640384)

  • Fotini Kokou
  • Goor Sasson
  • Tali Nitzan
  • Adi Doron-Faigenboim
  • Sheenan Harpaz
  • Avner Cnaani
  • Itzhak Mizrahi

Israel Science Foundation (Grant number 1313/13)

  • Fotini Kokou
  • Goor Sasson
  • Tali Nitzan
  • Adi Doron-Faigenboim
  • Sheenan Harpaz
  • Avner Cnaani
  • Itzhak Mizrahi

Ministry of Agriculture and Rural Development (Grant number 863-0045)

  • Fotini Kokou
  • Goor Sasson
  • Tali Nitzan
  • Adi Doron-Faigenboim
  • Sheenan Harpaz
  • Avner Cnaani
  • Itzhak Mizrahi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Rob Knight, University of California, San Diego, United States

Ethics

Animal experimentation: This study was approved by the Agricultural Research Organization Committee for Ethics in Using Experimental Animals and was carried out in compliance with the current laws governing biological research in Israel (Approval number: 146/09IL).

Version history

  1. Received: March 5, 2018
  2. Accepted: November 6, 2018
  3. Accepted Manuscript published: November 20, 2018 (version 1)
  4. Version of Record published: December 3, 2018 (version 2)

Copyright

© 2018, Kokou et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 5,228
    Page views
  • 807
    Downloads
  • 81
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Fotini Kokou
  2. Goor Sasson
  3. Tali Nitzan
  4. Adi Doron-Faigenboim
  5. Sheenan Harpaz
  6. Avner Cnaani
  7. Itzhak Mizrahi
(2018)
Host genetic selection for cold tolerance shapes microbiome composition and modulates its response to temperature
eLife 7:e36398.
https://doi.org/10.7554/eLife.36398

Share this article

https://doi.org/10.7554/eLife.36398

Further reading

    1. Immunology and Inflammation
    2. Microbiology and Infectious Disease
    Yuting Zhang, Min Zhang ... Guojiang Chen
    Research Article

    Marburg virus (MARV) is one of the filovirus species that cause deadly hemorrhagic fever in humans, with mortality rates up to 90%. Neutralizing antibodies represent ideal candidates to prevent or treat virus disease. However, no antibody has been approved for MARV treatment to date. In this study, we identified a novel human antibody named AF-03 that targeted MARV glycoprotein (GP). AF-03 possessed a high binding affinity to MARV GP and showed neutralizing and protective activities against the pseudotyped MARV in vitro and in vivo. Epitope identification, including molecular docking and experiment-based analysis of mutated species, revealed that AF-03 recognized the Niemann-Pick C1 (NPC1) binding domain within GP1. Interestingly, we found the neutralizing activity of AF-03 to pseudotyped Ebola viruses (EBOV, SUDV, and BDBV) harboring cleaved GP instead of full-length GP. Furthermore, NPC2-fused AF-03 exhibited neutralizing activity to several filovirus species and EBOV mutants via binding to CI-MPR. In conclusion, this work demonstrates that AF-03 represents a promising therapeutic cargo for filovirus-caused disease.

    1. Microbiology and Infectious Disease
    Chiara Andolina, Wouter Graumans ... Teun Bousema
    Research Article

    It is currently unknown whether all Plasmodium falciparum-infected mosquitoes are equally infectious. We assessed sporogonic development using cultured gametocytes in the Netherlands and naturally circulating strains in Burkina Faso. We quantified the number of sporozoites expelled into artificial skin in relation to intact oocysts, ruptured oocysts, and residual salivary gland sporozoites. In laboratory conditions, higher total sporozoite burden was associated with shorter duration of sporogony (p<0.001). Overall, 53% (116/216) of infected Anopheles stephensi mosquitoes expelled sporozoites into artificial skin with a median of 136 expelled sporozoites (interquartile range [IQR], 34–501). There was a strong positive correlation between ruptured oocyst number and salivary gland sporozoite load (ρ = 0.8; p<0.0001) and a weaker positive correlation between salivary gland sporozoite load and number of sporozoites expelled (ρ = 0.35; p=0.0002). In Burkina Faso, Anopheles coluzzii mosquitoes were infected by natural gametocyte carriers. Among salivary gland sporozoite positive mosquitoes, 89% (33/37) expelled sporozoites with a median of 1035 expelled sporozoites (IQR, 171–2969). Again, we observed a strong correlation between ruptured oocyst number and salivary gland sporozoite load (ρ = 0.9; p<0.0001) and a positive correlation between salivary gland sporozoite load and the number of sporozoites expelled (ρ = 0.7; p<0.0001). Several mosquitoes expelled multiple parasite clones during probing. Whilst sporozoite expelling was regularly observed from mosquitoes with low infection burdens, our findings indicate that mosquito infection burden is positively associated with the number of expelled sporozoites. Future work is required to determine the direct implications of these findings for transmission potential.