Linking Light-Dependent Life History Traits with Population Dynamics for <italic toggle="yes">Prochlorococcus</italic> and Cyanophage

ABSTRACT Prochlorococcus cyanobacteria grow in diurnal rhythms driven by diel cycles. Their ecology depends on light, nutrients, and top-down mortality processes, including lysis by viruses. Cyanophage, viruses that infect cyanobacteria, are also impacted by light. For example, the extracellular via...

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Autores principales: David Demory, Riyue Liu, Yue Chen, Fangxin Zhao, Ashley R. Coenen, Qinglu Zeng, Joshua S. Weitz
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:dfd7441ecda74231aa27882b4f8211da2021-12-02T18:44:38ZLinking Light-Dependent Life History Traits with Population Dynamics for <italic toggle="yes">Prochlorococcus</italic> and Cyanophage10.1128/mSystems.00586-192379-5077https://doaj.org/article/dfd7441ecda74231aa27882b4f8211da2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00586-19https://doaj.org/toc/2379-5077ABSTRACT Prochlorococcus cyanobacteria grow in diurnal rhythms driven by diel cycles. Their ecology depends on light, nutrients, and top-down mortality processes, including lysis by viruses. Cyanophage, viruses that infect cyanobacteria, are also impacted by light. For example, the extracellular viability and intracellular infection kinetics of some cyanophage vary between light and dark conditions. Nonetheless, it remains unclear whether light-dependent viral life history traits scale up to influence population-level dynamics. Here, we examined the impact of diel forcing on both cellular- and population-scale dynamics in multiple Prochlorococcus-phage systems. To do so, we developed a light-driven population model, including both cellular growth and viral infection dynamics. We then tested the model against measurements of experimental infection dynamics with diel forcing to examine the extent to which population level changes in both viral and host abundances could be explained by light-dependent life history traits. Model-data integration reveals that light-dependent adsorption can improve fits to population dynamics for some virus-host pairs. However, light-dependent variation alone does not fully explain realized host and virus population dynamics. Instead, we show evidence consistent with lysis saturation at relatively high virus-to-cell ratios. Altogether, our study represents a quantitative approach to integrate mechanistic models to reconcile Prochlorococcus-virus dynamics spanning cellular-to-population scales. IMPORTANCE The cyanobacterium Prochlorococcus is an essential member of global ocean ecosystems. Light rhythms drive Prochlorococcus photosynthesis, ecology, and interactions with potentially lethal viruses. At present, the impact of light on Prochlorococcus-virus interactions is not well understood. Here, we analyzed Prochlorococcus and virus population dynamics with a light-driven population model and compared our results with experimental data. Our approach revealed that light profoundly drives both cellular- and population-level dynamics for some host-virus systems. However, we also found that additional mechanisms, including lysis saturation, are required to explain observed host-virus dynamics at the population scale. This study provides the basis for future work to understand the intertwined fates of Prochlorococcus and associated viruses in the surface ocean.David DemoryRiyue LiuYue ChenFangxin ZhaoAshley R. CoenenQinglu ZengJoshua S. WeitzAmerican Society for Microbiologyarticlecyanobacteriacyanophagediurnal rhythmlight-dark cyclemodelingvirusMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution DOAJ
collection DOAJ
language EN
topic cyanobacteria
cyanophage
diurnal rhythm
light-dark cycle
modeling
virus
Microbiology
QR1-502
spellingShingle cyanobacteria
cyanophage
diurnal rhythm
light-dark cycle
modeling
virus
Microbiology
QR1-502
David Demory
Riyue Liu
Yue Chen
Fangxin Zhao
Ashley R. Coenen
Qinglu Zeng
Joshua S. Weitz
Linking Light-Dependent Life History Traits with Population Dynamics for <italic toggle="yes">Prochlorococcus</italic> and Cyanophage
description ABSTRACT Prochlorococcus cyanobacteria grow in diurnal rhythms driven by diel cycles. Their ecology depends on light, nutrients, and top-down mortality processes, including lysis by viruses. Cyanophage, viruses that infect cyanobacteria, are also impacted by light. For example, the extracellular viability and intracellular infection kinetics of some cyanophage vary between light and dark conditions. Nonetheless, it remains unclear whether light-dependent viral life history traits scale up to influence population-level dynamics. Here, we examined the impact of diel forcing on both cellular- and population-scale dynamics in multiple Prochlorococcus-phage systems. To do so, we developed a light-driven population model, including both cellular growth and viral infection dynamics. We then tested the model against measurements of experimental infection dynamics with diel forcing to examine the extent to which population level changes in both viral and host abundances could be explained by light-dependent life history traits. Model-data integration reveals that light-dependent adsorption can improve fits to population dynamics for some virus-host pairs. However, light-dependent variation alone does not fully explain realized host and virus population dynamics. Instead, we show evidence consistent with lysis saturation at relatively high virus-to-cell ratios. Altogether, our study represents a quantitative approach to integrate mechanistic models to reconcile Prochlorococcus-virus dynamics spanning cellular-to-population scales. IMPORTANCE The cyanobacterium Prochlorococcus is an essential member of global ocean ecosystems. Light rhythms drive Prochlorococcus photosynthesis, ecology, and interactions with potentially lethal viruses. At present, the impact of light on Prochlorococcus-virus interactions is not well understood. Here, we analyzed Prochlorococcus and virus population dynamics with a light-driven population model and compared our results with experimental data. Our approach revealed that light profoundly drives both cellular- and population-level dynamics for some host-virus systems. However, we also found that additional mechanisms, including lysis saturation, are required to explain observed host-virus dynamics at the population scale. This study provides the basis for future work to understand the intertwined fates of Prochlorococcus and associated viruses in the surface ocean.
format article
author David Demory
Riyue Liu
Yue Chen
Fangxin Zhao
Ashley R. Coenen
Qinglu Zeng
Joshua S. Weitz
author_facet David Demory
Riyue Liu
Yue Chen
Fangxin Zhao
Ashley R. Coenen
Qinglu Zeng
Joshua S. Weitz
author_sort David Demory
title Linking Light-Dependent Life History Traits with Population Dynamics for <italic toggle="yes">Prochlorococcus</italic> and Cyanophage
title_short Linking Light-Dependent Life History Traits with Population Dynamics for <italic toggle="yes">Prochlorococcus</italic> and Cyanophage
title_full Linking Light-Dependent Life History Traits with Population Dynamics for <italic toggle="yes">Prochlorococcus</italic> and Cyanophage
title_fullStr Linking Light-Dependent Life History Traits with Population Dynamics for <italic toggle="yes">Prochlorococcus</italic> and Cyanophage
title_full_unstemmed Linking Light-Dependent Life History Traits with Population Dynamics for <italic toggle="yes">Prochlorococcus</italic> and Cyanophage
title_sort linking light-dependent life history traits with population dynamics for <italic toggle="yes">prochlorococcus</italic> and cyanophage
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/dfd7441ecda74231aa27882b4f8211da
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