Transient eco-evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long-term evolution of bacterial defences.
Organisms have evolved a range of constitutive (always active) and inducible (elicited by parasites) defence mechanisms, but we have limited understanding of what drives the evolution of these orthogonal defence strategies. Bacteria and their phages offer a tractable system to study this: Bacteria c...
Main Authors: | , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Public Library of Science (PLoS)
2023-09-01
|
Series: | PLoS Biology |
Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002122&type=printable |
_version_ | 1827777323857870848 |
---|---|
author | Bridget Nora Janice Watson Elizabeth Pursey Sylvain Gandon Edze Rients Westra |
author_facet | Bridget Nora Janice Watson Elizabeth Pursey Sylvain Gandon Edze Rients Westra |
author_sort | Bridget Nora Janice Watson |
collection | DOAJ |
description | Organisms have evolved a range of constitutive (always active) and inducible (elicited by parasites) defence mechanisms, but we have limited understanding of what drives the evolution of these orthogonal defence strategies. Bacteria and their phages offer a tractable system to study this: Bacteria can acquire constitutive resistance by mutation of the phage receptor (surface mutation, sm) or induced resistance through their CRISPR-Cas adaptive immune system. Using a combination of theory and experiments, we demonstrate that the mechanism that establishes first has a strong advantage because it weakens selection for the alternative resistance mechanism. As a consequence, ecological factors that alter the relative frequencies at which the different resistances are acquired have a strong and lasting impact: High growth conditions promote the evolution of sm resistance by increasing the influx of receptor mutation events during the early stages of the epidemic, whereas a high infection risk during this stage of the epidemic promotes the evolution of CRISPR immunity, since it fuels the (infection-dependent) acquisition of CRISPR immunity. This work highlights the strong and lasting impact of the transient evolutionary dynamics during the early stages of an epidemic on the long-term evolution of constitutive and induced defences, which may be leveraged to manipulate phage resistance evolution in clinical and applied settings. |
first_indexed | 2024-03-11T14:16:43Z |
format | Article |
id | doaj.art-ee9d75b08b8b4b6e99cbfded0f92bca0 |
institution | Directory Open Access Journal |
issn | 1544-9173 1545-7885 |
language | English |
last_indexed | 2024-03-11T14:16:43Z |
publishDate | 2023-09-01 |
publisher | Public Library of Science (PLoS) |
record_format | Article |
series | PLoS Biology |
spelling | doaj.art-ee9d75b08b8b4b6e99cbfded0f92bca02023-11-01T05:30:51ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-09-01219e300212210.1371/journal.pbio.3002122Transient eco-evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long-term evolution of bacterial defences.Bridget Nora Janice WatsonElizabeth PurseySylvain GandonEdze Rients WestraOrganisms have evolved a range of constitutive (always active) and inducible (elicited by parasites) defence mechanisms, but we have limited understanding of what drives the evolution of these orthogonal defence strategies. Bacteria and their phages offer a tractable system to study this: Bacteria can acquire constitutive resistance by mutation of the phage receptor (surface mutation, sm) or induced resistance through their CRISPR-Cas adaptive immune system. Using a combination of theory and experiments, we demonstrate that the mechanism that establishes first has a strong advantage because it weakens selection for the alternative resistance mechanism. As a consequence, ecological factors that alter the relative frequencies at which the different resistances are acquired have a strong and lasting impact: High growth conditions promote the evolution of sm resistance by increasing the influx of receptor mutation events during the early stages of the epidemic, whereas a high infection risk during this stage of the epidemic promotes the evolution of CRISPR immunity, since it fuels the (infection-dependent) acquisition of CRISPR immunity. This work highlights the strong and lasting impact of the transient evolutionary dynamics during the early stages of an epidemic on the long-term evolution of constitutive and induced defences, which may be leveraged to manipulate phage resistance evolution in clinical and applied settings.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002122&type=printable |
spellingShingle | Bridget Nora Janice Watson Elizabeth Pursey Sylvain Gandon Edze Rients Westra Transient eco-evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long-term evolution of bacterial defences. PLoS Biology |
title | Transient eco-evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long-term evolution of bacterial defences. |
title_full | Transient eco-evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long-term evolution of bacterial defences. |
title_fullStr | Transient eco-evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long-term evolution of bacterial defences. |
title_full_unstemmed | Transient eco-evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long-term evolution of bacterial defences. |
title_short | Transient eco-evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long-term evolution of bacterial defences. |
title_sort | transient eco evolutionary dynamics early in a phage epidemic have strong and lasting impact on the long term evolution of bacterial defences |
url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002122&type=printable |
work_keys_str_mv | AT bridgetnorajanicewatson transientecoevolutionarydynamicsearlyinaphageepidemichavestrongandlastingimpactonthelongtermevolutionofbacterialdefences AT elizabethpursey transientecoevolutionarydynamicsearlyinaphageepidemichavestrongandlastingimpactonthelongtermevolutionofbacterialdefences AT sylvaingandon transientecoevolutionarydynamicsearlyinaphageepidemichavestrongandlastingimpactonthelongtermevolutionofbacterialdefences AT edzerientswestra transientecoevolutionarydynamicsearlyinaphageepidemichavestrongandlastingimpactonthelongtermevolutionofbacterialdefences |