1. Microbiology and Infectious Disease
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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
Research Article
  • Cited 33
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Cite this article as: eLife 2018;7:e36398 doi: 10.7554/eLife.36398

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.

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).

Reviewing Editor

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

Publication 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.

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Further reading

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    Background:

    Early identification of severe dengue patients is important regarding patient management and resource allocation. We investigated the association of 10 biomarkers (VCAM-1, SDC-1, Ang-2, IL-8, IP-10, IL-1RA, sCD163, sTREM-1, ferritin, CRP) with the development of severe/moderate dengue (S/MD).

    Methods:

    We performed a nested case-control study from a multi-country study. A total of 281 S/MD and 556 uncomplicated dengue cases were included.

    Results:

    On days 1–3 from symptom onset, higher levels of any biomarker increased the risk of developing S/MD. When assessing together, SDC-1 and IL-1RA were stable, while IP-10 changed the association from positive to negative; others showed weaker associations. The best combinations associated with S/MD comprised IL-1RA, Ang-2, IL-8, ferritin, IP-10, and SDC-1 for children, and SDC-1, IL-8, ferritin, sTREM-1, IL-1RA, IP-10, and sCD163 for adults.

    Conclusions:

    Our findings assist the development of biomarker panels for clinical use and could improve triage and risk prediction in dengue patients.

    Funding:

    This study was supported by the EU's Seventh Framework Programme (FP7-281803 IDAMS), the WHO, and the Bill and Melinda Gates Foundation.

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    The influenza A virus (IAV) genome consists of eight negative-sense viral RNA (vRNA) segments that are selectively assembled into progeny virus particles through RNA-RNA interactions. To explore putative intersegmental RNA-RNA relationships, we quantified similarity between phylogenetic trees comprising each vRNA segment from seasonal human IAV. Intersegmental tree similarity differed between subtype and lineage. While intersegmental relationships were largely conserved over time in H3N2 viruses, they diverged in H1N1 strains isolated before and after the 2009 pandemic. Surprisingly, intersegmental relationships were not driven solely by protein sequence, suggesting that IAV evolution could also be driven by RNA-RNA interactions. Finally, we used confocal microscopy to determine that colocalization of highly coevolved vRNA segments is enriched over other assembly intermediates at the nuclear periphery during productive viral infection. This study illustrates how putative RNA interactions underlying selective assembly of IAV can be interrogated with phylogenetics.