Dynamics of immune memory and learning in bacterial communities
- University of Toronto, Canada
Abstract
From bacteria to humans, adaptive immune systems provide learned memories of past infections. Despite their vast biological differences, adaptive immunity shares features from microbes to vertebrates such as emergent immune diversity, long-term coexistence of hosts and pathogens, and fitness pressures from evolving pathogens and adapting hosts, yet there is no conceptual model that addresses all of these together. To this end, we propose and solve a simple phenomenological model of CRISPR-based adaptive immunity in microbes. We show that in coexisting phage and bacteria populations, immune diversity in both populations is coupled and emerges spontaneously, that bacteria track phage evolution with a context-dependent lag, and that high levels of diversity are paradoxically linked to low overall CRISPR immunity. We define average immunity, an important summary parameter predicted by our model, and use it to perform synthetic time-shift analyses on available experimental data to reveal different modalities of coevolution. Finally, immune cross-reactivity in our model leads to qualitatively different states of evolutionary dynamics, including an influenza-like traveling wave regime that resembles a similar state in models of vertebrate adaptive immunity. Our results show that CRISPR immunity provides a tractable model, both theoretically and experimentally, to understand general features of adaptive immunity.
Data availability
Source code and data is available for all main text figures on GitHub at https://github.com/mbonsma/CRISPR-dynamics-model.Source data for Figures 6E-G and 7C-D is available on GitHub at https://github.com/mbonsma/CRISPR-dynamics-model.Raw simulation data has been uploaded to Dryad: https://doi.org/10.5061/dryad.sn02v6x74.
-
Simulation data from: Dynamics of immune memory and learning in bacterial communitiesDryad Digital Repository, doi:10.5061/dryad.sn02v6x74.
Article and author information
Author details
Madeleine Bonsma-Fisher
Funding
Natural Sciences and Engineering Research Council of Canada (Vanier Canada Graduate Scholarship)
- Madeleine Bonsma-Fisher
Ministry of Colleges and Universities (Queen Elizabeth II Graduate Scholarship in Science & Technology)
- Madeleine Bonsma-Fisher
Walter C. Sumner Foundation (Walter C. Sumner Memorial Fellowship)
- Madeleine Bonsma-Fisher
Natural Sciences and Engineering Research Council of Canada (Discovery Grant RGPIN-2015)
- Sidhartha Goyal
Natural Sciences and Engineering Research Council of Canada (Discovery Grant and RGPIN-2021)
- Sidhartha Goyal
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2023, Bonsma-Fisher & Goyal
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
-
- 938
- views
-
- 214
- downloads
-
- 1
- citation
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Citations by DOI
-
- 1
- citation for umbrella DOI https://doi.org/10.7554/eLife.81692
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)
Dynamics of immune memory and learning in bacterial communities
eLife 12:e81692.
https://doi.org/10.7554/eLife.81692
