Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles

ABSTRACT Temperate phages can associate with their bacterial host to form a lysogen, often modifying the phenotype of the host. Lysogens are dominant in the microbially dense environment of the mammalian gut. This observation contrasts with the long-standing hypothesis of lysogeny being favored at l...

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Autores principales:	Antoni Luque, Cynthia B. Silveira
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	stochastic biophysical model lysogeny microbial abundance multiplicity of infection adsorption rates commitment time Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dc5f1164caea408c91b2b0f883b45746
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spelling	oai:doaj.org-article:dc5f1164caea408c91b2b0f883b457462021-12-02T19:47:33ZQuantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles10.1128/mSystems.00353-202379-5077https://doaj.org/article/dc5f1164caea408c91b2b0f883b457462020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00353-20https://doaj.org/toc/2379-5077ABSTRACT Temperate phages can associate with their bacterial host to form a lysogen, often modifying the phenotype of the host. Lysogens are dominant in the microbially dense environment of the mammalian gut. This observation contrasts with the long-standing hypothesis of lysogeny being favored at low microbial densities, such as in oligotrophic marine environments. Here, we hypothesized that phage coinfections—a well-understood molecular mechanism of lysogenization—increase at high microbial abundances. To test this hypothesis, we developed a biophysical model of coinfection for marine and gut microbiomes. The model stochastically sampled ranges of phage and bacterial concentrations, adsorption rates, lysogenic commitment times, and community diversity from each environment. In 90% of the sampled marine communities, less than 10% of the bacteria were predicted to be lysogenized via coinfection. In contrast, 25% of the sampled gut communities displayed more than 25% of lysogenization. The probability of lysogenization in the gut was a consequence of the higher densities and higher adsorption rates. These results suggest that, on average, coinfections can form two trillion lysogens in the human gut every day. In marine microbiomes, which were characterized by lower densities and phage adsorption rates, lysogeny via coinfection was still possible for communities with long lysogenic commitment times. Our study indicates that different physical factors causing coinfections can reconcile the traditional view of lysogeny at poor host growth (long commitment times) and the recent Piggyback-the-Winner framework proposing that lysogeny is favored in rich environments (high densities and adsorption rates). IMPORTANCE The association of temperate phages and bacterial hosts during lysogeny manipulates microbial dynamics from the oceans to the human gut. Lysogeny is well studied in laboratory models, but its environmental drivers remain unclear. Here, we quantified the probability of lysogenization caused by phage coinfections, a well-known trigger of lysogeny, in marine and gut microbial environments. Coinfections were quantified by developing a biophysical model that incorporated the traits of viral and bacterial communities. Lysogenization via coinfection was more frequent in highly productive environments like the gut, due to higher microbial densities and higher phage adsorption rates. At low cell densities, lysogenization occurred in bacteria with long duplication times. These results bridge the molecular understanding of lysogeny with the ecology of complex microbial communities.Antoni LuqueCynthia B. SilveiraAmerican Society for Microbiologyarticlestochastic biophysical modellysogenymicrobial abundancemultiplicity of infectionadsorption ratescommitment timeMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	stochastic biophysical model lysogeny microbial abundance multiplicity of infection adsorption rates commitment time Microbiology QR1-502
spellingShingle	stochastic biophysical model lysogeny microbial abundance multiplicity of infection adsorption rates commitment time Microbiology QR1-502 Antoni Luque Cynthia B. Silveira Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles
description	ABSTRACT Temperate phages can associate with their bacterial host to form a lysogen, often modifying the phenotype of the host. Lysogens are dominant in the microbially dense environment of the mammalian gut. This observation contrasts with the long-standing hypothesis of lysogeny being favored at low microbial densities, such as in oligotrophic marine environments. Here, we hypothesized that phage coinfections—a well-understood molecular mechanism of lysogenization—increase at high microbial abundances. To test this hypothesis, we developed a biophysical model of coinfection for marine and gut microbiomes. The model stochastically sampled ranges of phage and bacterial concentrations, adsorption rates, lysogenic commitment times, and community diversity from each environment. In 90% of the sampled marine communities, less than 10% of the bacteria were predicted to be lysogenized via coinfection. In contrast, 25% of the sampled gut communities displayed more than 25% of lysogenization. The probability of lysogenization in the gut was a consequence of the higher densities and higher adsorption rates. These results suggest that, on average, coinfections can form two trillion lysogens in the human gut every day. In marine microbiomes, which were characterized by lower densities and phage adsorption rates, lysogeny via coinfection was still possible for communities with long lysogenic commitment times. Our study indicates that different physical factors causing coinfections can reconcile the traditional view of lysogeny at poor host growth (long commitment times) and the recent Piggyback-the-Winner framework proposing that lysogeny is favored in rich environments (high densities and adsorption rates). IMPORTANCE The association of temperate phages and bacterial hosts during lysogeny manipulates microbial dynamics from the oceans to the human gut. Lysogeny is well studied in laboratory models, but its environmental drivers remain unclear. Here, we quantified the probability of lysogenization caused by phage coinfections, a well-known trigger of lysogeny, in marine and gut microbial environments. Coinfections were quantified by developing a biophysical model that incorporated the traits of viral and bacterial communities. Lysogenization via coinfection was more frequent in highly productive environments like the gut, due to higher microbial densities and higher phage adsorption rates. At low cell densities, lysogenization occurred in bacteria with long duplication times. These results bridge the molecular understanding of lysogeny with the ecology of complex microbial communities.
format	article
author	Antoni Luque Cynthia B. Silveira
author_facet	Antoni Luque Cynthia B. Silveira
author_sort	Antoni Luque
title	Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles
title_short	Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles
title_full	Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles
title_fullStr	Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles
title_full_unstemmed	Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles
title_sort	quantification of lysogeny caused by phage coinfections in microbial communities from biophysical principles
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/dc5f1164caea408c91b2b0f883b45746
work_keys_str_mv	AT antoniluque quantificationoflysogenycausedbyphagecoinfectionsinmicrobialcommunitiesfrombiophysicalprinciples AT cynthiabsilveira quantificationoflysogenycausedbyphagecoinfectionsinmicrobialcommunitiesfrombiophysicalprinciples
_version_	1718375994371342336

Quantification of Lysogeny Caused by Phage Coinfections in Microbial Communities from Biophysical Principles

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