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Alternating lysis and lysogeny is a winning strategy in bacteriophages due to Parrondo's paradox

Cheong, Kang Hao and Wen, Tao and Benler, Sean and Koh, Jin Ming and Koonin, Eugene V. (2022) Alternating lysis and lysogeny is a winning strategy in bacteriophages due to Parrondo's paradox. Proceedings of the National Academy of Sciences of the United States of America, 119 (13). Art. No. e2115145119. ISSN 0027-8424. PMCID PMC9060511. doi:10.1073/pnas.2115145119. https://resolver.caltech.edu/CaltechAUTHORS:20220323-704173000

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Abstract

Temperate bacteriophages lyse or lysogenize host cells depending on various parameters of infection, a key one being the ratio of the number of free viruses to the number of host cells. However, the effect of different propensities of phages for lysis and lysogeny on phage fitness remains an open problem. We explore a nonlinear dynamic evolution model of competition between two phages, one of which is disadvantaged in both the lytic and lysogenic phases. We show that the disadvantaged phage can win the competition by alternating between the lytic and lysogenic phases, each of which individually is a “loser.” This counterintuitive result is analogous to Parrondo’s paradox in game theory, whereby individually losing strategies combine to produce a winning outcome. The results suggest that evolution of phages optimizes the ratio between the lysis and lysogeny propensities rather than the phage burst size in any individual phase. These findings are likely to broadly apply to the evolution of host–parasite interactions.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.2115145119DOIArticle
https://www.pnas.org/doi/suppl/10.1073/pnas.2115145119/suppl_file/pnas.2115145119.sapp.pdfPublisherSupporting Information
https://osf.io/vth96/?view_only=c61c0a312ef04624acbeb41d071e70dfRelated ItemSource code
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9060511/PubMed CentralArticle
ORCID:
AuthorORCID
Cheong, Kang Hao0000-0002-4475-5451
Benler, Sean0000-0001-7985-1294
Koh, Jin Ming0000-0002-6130-5591
Koonin, Eugene V.0000-0003-3943-8299
Additional Information:© 2022 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Received: August 16, 2021. Accepted: January 15, 2022. Published online: March 22, 2022. Published in issue: March 29, 2022. K.H.C., T.W., and J.M.K. are supported by Singapore University of Technology and Design Grant SRG SCI 2019 142. S.B. and E.V.K. are supported by the Intramural Research Program of the NIH (National Library of Medicine). Data Availability. The source code used in this work can be accessed at Open Science Framework (https://osf.io/vth96/?view_only=c61c0a312ef04624acbeb41d071e70df). All other data are included in the manuscript and/or SI Appendix. Author contributions: K.H.C. and E.V.K. designedresearch; K.H.C., T.W., S.B., and E.V.K. performedresearch; K.H.C., T.W., S.B., J.M.K., and E.V.K. analyzeddata; and K.H.C., T.W., S.B., J.M.K., and E.V.K. wrote the paper. K.H.C. and T.W. contributed equally to this work. This article contains supporting information online athttp://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2115145119/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Singapore University of Technology and DesignSRG SCI 2019 142
National Library of MedicineUNSPECIFIED
Subject Keywords:bacteriophages; lysis; lysogeny; game theory; Parrondo's paradox
Issue or Number:13
PubMed Central ID:PMC9060511
DOI:10.1073/pnas.2115145119
Record Number:CaltechAUTHORS:20220323-704173000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220323-704173000
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:114021
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:24 Mar 2022 22:52
Last Modified:05 May 2022 16:07

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