Host genetic selection for cold tolerance shapes microbiome composition and modulates its response to temperature
- Ben-Gurion University of the Negev, Israel
- 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.
-
Blue tilapia gut microbiomeNCBI Sequence Read Archive, SRP131209.
Article and author information
Author details
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).
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
-
- 5,666
- views
-
- 850
- downloads
-
- 111
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
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)
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
Further reading
-
- Immunology and Inflammation
- Microbiology and Infectious Disease
Pseudomonas aeruginosa (PA) is an opportunistic, frequently multidrug-resistant pathogen that can cause severe infections in hospitalized patients. Antibodies against the PA virulence factor, PcrV, protect from death and disease in a variety of animal models. However, clinical trials of PcrV-binding antibody-based products have thus far failed to demonstrate benefit. Prior candidates were derivations of antibodies identified using protein-immunized animal systems and required extensive engineering to optimize binding and/or reduce immunogenicity. Of note, PA infections are common in people with cystic fibrosis (pwCF), who are generally believed to mount normal adaptive immune responses. Here, we utilized a tetramer reagent to detect and isolate PcrV-specific B cells in pwCF and, via single-cell sorting and paired-chain sequencing, identified the B cell receptor (BCR) variable region sequences that confer PcrV-specificity. We derived multiple high affinity anti-PcrV monoclonal antibodies (mAbs) from PcrV-specific B cells across three donors, including mAbs that exhibit potent anti-PA activity in a murine pneumonia model. This robust strategy for mAb discovery expands what is known about PA-specific B cells in pwCF and yields novel mAbs with potential for future clinical use.
-
- Biochemistry and Chemical Biology
- Microbiology and Infectious Disease
Teichoic acids (TA) are linear phospho-saccharidic polymers and important constituents of the cell envelope of Gram-positive bacteria, either bound to the peptidoglycan as wall teichoic acids (WTA) or to the membrane as lipoteichoic acids (LTA). The composition of TA varies greatly but the presence of both WTA and LTA is highly conserved, hinting at an underlying fundamental function that is distinct from their specific roles in diverse organisms. We report the observation of a periplasmic space in Streptococcus pneumoniae by cryo-electron microscopy of vitreous sections. The thickness and appearance of this region change upon deletion of genes involved in the attachment of TA, supporting their role in the maintenance of a periplasmic space in Gram-positive bacteria as a possible universal function. Consequences of these mutations were further examined by super-resolved microscopy, following metabolic labeling and fluorophore coupling by click chemistry. This novel labeling method also enabled in-gel analysis of cell fractions. With this approach, we were able to titrate the actual amount of TA per cell and to determine the ratio of WTA to LTA. In addition, we followed the change of TA length during growth phases, and discovered that a mutant devoid of LTA accumulates the membrane-bound polymerized TA precursor.
