Collective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles

ABSTRACT A growing number of studies report that viruses can spread in groups in so-called collective infectious units. By increasing the cellular multiplicity of infection, collective dispersal may allow for social-like interactions, such as cooperation or cheating. Yet, little is known about how s...

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Autores principales:	Iván Andreu-Moreno, Rafael Sanjuán
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	collective infectious units defective interfering particles experimental evolution social evolution vesicular stomatitis virus Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/42d791d46cdb4267ac7360fdb6c98b94
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spelling	oai:doaj.org-article:42d791d46cdb4267ac7360fdb6c98b942021-11-15T15:56:57ZCollective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles10.1128/mBio.02156-192150-7511https://doaj.org/article/42d791d46cdb4267ac7360fdb6c98b942020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02156-19https://doaj.org/toc/2150-7511ABSTRACT A growing number of studies report that viruses can spread in groups in so-called collective infectious units. By increasing the cellular multiplicity of infection, collective dispersal may allow for social-like interactions, such as cooperation or cheating. Yet, little is known about how such interactions evolve. In previous work with vesicular stomatitis virus, we showed that virion aggregation accelerates early infection stages in most cell types, providing a short-term fitness benefit to the virus. Here, we examine the effects of virion aggregation over several infection cycles. Flow cytometry, deep sequencing, infectivity assays, reverse transcription-quantitative PCR, and electron microscopy revealed that virion aggregation rapidly promotes the emergence of defective interfering particles. Therefore, virion aggregation provides immediate fitness benefits to the virus but incurs fitness costs after a few viral generations. This suggests that an optimal strategy for the virus is to undergo virion aggregation only episodically, for instance, during interhost transmission. IMPORTANCE Recent insights have revealed that viruses use a highly diverse set of strategies to release multiple viral genomes into the same target cells, allowing the emergence of beneficial, but also detrimental, interactions among viruses inside infected cells. This has prompted interest among microbial ecologists and evolutionary biologists in studying how collective dispersal impacts the outcome of viral infections. Here, we have used vesicular stomatitis virus as a model system to study the evolutionary implications of collective dissemination mediated by viral aggregates, since this virus can spontaneously aggregate in the presence of saliva. We find that saliva-driven aggregation has a dual effect on viral fitness; whereas aggregation tends to increase infectivity in the very short term, virion aggregates are highly susceptible to invasion by noncooperative defective variants after a few viral generations.Iván Andreu-MorenoRafael SanjuánAmerican Society for Microbiologyarticlecollective infectious unitsdefective interfering particlesexperimental evolutionsocial evolutionvesicular stomatitis virusMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	collective infectious units defective interfering particles experimental evolution social evolution vesicular stomatitis virus Microbiology QR1-502
spellingShingle	collective infectious units defective interfering particles experimental evolution social evolution vesicular stomatitis virus Microbiology QR1-502 Iván Andreu-Moreno Rafael Sanjuán Collective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles
description	ABSTRACT A growing number of studies report that viruses can spread in groups in so-called collective infectious units. By increasing the cellular multiplicity of infection, collective dispersal may allow for social-like interactions, such as cooperation or cheating. Yet, little is known about how such interactions evolve. In previous work with vesicular stomatitis virus, we showed that virion aggregation accelerates early infection stages in most cell types, providing a short-term fitness benefit to the virus. Here, we examine the effects of virion aggregation over several infection cycles. Flow cytometry, deep sequencing, infectivity assays, reverse transcription-quantitative PCR, and electron microscopy revealed that virion aggregation rapidly promotes the emergence of defective interfering particles. Therefore, virion aggregation provides immediate fitness benefits to the virus but incurs fitness costs after a few viral generations. This suggests that an optimal strategy for the virus is to undergo virion aggregation only episodically, for instance, during interhost transmission. IMPORTANCE Recent insights have revealed that viruses use a highly diverse set of strategies to release multiple viral genomes into the same target cells, allowing the emergence of beneficial, but also detrimental, interactions among viruses inside infected cells. This has prompted interest among microbial ecologists and evolutionary biologists in studying how collective dispersal impacts the outcome of viral infections. Here, we have used vesicular stomatitis virus as a model system to study the evolutionary implications of collective dissemination mediated by viral aggregates, since this virus can spontaneously aggregate in the presence of saliva. We find that saliva-driven aggregation has a dual effect on viral fitness; whereas aggregation tends to increase infectivity in the very short term, virion aggregates are highly susceptible to invasion by noncooperative defective variants after a few viral generations.
format	article
author	Iván Andreu-Moreno Rafael Sanjuán
author_facet	Iván Andreu-Moreno Rafael Sanjuán
author_sort	Iván Andreu-Moreno
title	Collective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles
title_short	Collective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles
title_full	Collective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles
title_fullStr	Collective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles
title_full_unstemmed	Collective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles
title_sort	collective viral spread mediated by virion aggregates promotes the evolution of defective interfering particles
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/42d791d46cdb4267ac7360fdb6c98b94
work_keys_str_mv	AT ivanandreumoreno collectiveviralspreadmediatedbyvirionaggregatespromotestheevolutionofdefectiveinterferingparticles AT rafaelsanjuan collectiveviralspreadmediatedbyvirionaggregatespromotestheevolutionofdefectiveinterferingparticles
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Collective Viral Spread Mediated by Virion Aggregates Promotes the Evolution of Defective Interfering Particles

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