Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean

ABSTRACT The evolutionary interactions between viruses and their prokaryotic hosts remain a little-known aspect of microbial evolution. Most studies on this topic were carried out in pure cultures that challenge one virus with one bacterial clone at a time, which is very removed from real-life situa...

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Autores principales:	Felipe Hernandes Coutinho, Riccardo Rosselli, Francisco Rodríguez-Valera
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	metagenomics microdiversity marine virome depth gradient virus Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0fa899e8286c4e7897962607dcad07c2
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spelling	oai:doaj.org-article:0fa899e8286c4e7897962607dcad07c22021-12-02T19:46:17ZTrends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean10.1128/mSystems.00554-192379-5077https://doaj.org/article/0fa899e8286c4e7897962607dcad07c22019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00554-19https://doaj.org/toc/2379-5077ABSTRACT The evolutionary interactions between viruses and their prokaryotic hosts remain a little-known aspect of microbial evolution. Most studies on this topic were carried out in pure cultures that challenge one virus with one bacterial clone at a time, which is very removed from real-life situations. Few studies have addressed trends of microdiversity in marine viral communities throughout depth gradients. We analyzed metagenomes from both the cellular and viral fractions of Mediterranean seawater samples spanning the epipelagic to the bathypelagic zones at depths of 15, 45, 60, and 2,000 m during the summer stratification of the water column. We evaluated microdiversity patterns by measuring the accumulation of synonymous and nonsynonymous mutations in viral genes. Our results demonstrated clear depth-dependent trends in the frequency of polymorphic sites and nonsynonymous mutations among genes encoding metabolic, structural, and replication proteins. These differences were linked to changes in energy availability, host and viral densities, and the proportions of actively replicating viruses. We propose the hypothesis that in the energy-rich, high-host-density, euphotic depths, selection acts to favor diversity of the host recognition machinery to increase host range, while in energy-depleted aphotic waters, selection acts on viral replication fitness, enhancing diversity in auxiliary metabolic genes. IMPORTANCE Viruses are extremely abundant and diverse biological entities that contribute to the functioning of marine ecosystems. Despite their recognized importance, few studies have addressed trends of mutation accumulation in marine viral communities across depth gradients. By investigating these trends, we show that mutation frequencies differ among viral genes according to their molecular functions, with the highest microdiversity occurring among proteins related to host metabolism, followed by structural proteins and, lastly, genome replication proteins. This is in agreement with evolutionary theory that postulates that housekeeping genes are under strong purifying selection. We also observed a positive association between depth and microdiversity. One exception to this trend was the host recognition proteins from the deep chlorophyll maximum, which displayed strikingly high microdiversity, which we hypothesize to be associated with intraspecies competition for hosts. Finally, our data allowed us to propose a theoretical model for viral microdiversity across the depth gradient. These discoveries are of special relevance because many of the viral genomic sequences discovered here were predicted to infect some of the most abundant bacteria in marine ecosystems, such as “Candidatus Pelagibacter,” Puniceispirillum, and Prochlorococcus.Felipe Hernandes CoutinhoRiccardo RosselliFrancisco Rodríguez-ValeraAmerican Society for Microbiologyarticlemetagenomicsmicrodiversitymarineviromedepth gradientvirusMicrobiologyQR1-502ENmSystems, Vol 4, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	metagenomics microdiversity marine virome depth gradient virus Microbiology QR1-502
spellingShingle	metagenomics microdiversity marine virome depth gradient virus Microbiology QR1-502 Felipe Hernandes Coutinho Riccardo Rosselli Francisco Rodríguez-Valera Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean
description	ABSTRACT The evolutionary interactions between viruses and their prokaryotic hosts remain a little-known aspect of microbial evolution. Most studies on this topic were carried out in pure cultures that challenge one virus with one bacterial clone at a time, which is very removed from real-life situations. Few studies have addressed trends of microdiversity in marine viral communities throughout depth gradients. We analyzed metagenomes from both the cellular and viral fractions of Mediterranean seawater samples spanning the epipelagic to the bathypelagic zones at depths of 15, 45, 60, and 2,000 m during the summer stratification of the water column. We evaluated microdiversity patterns by measuring the accumulation of synonymous and nonsynonymous mutations in viral genes. Our results demonstrated clear depth-dependent trends in the frequency of polymorphic sites and nonsynonymous mutations among genes encoding metabolic, structural, and replication proteins. These differences were linked to changes in energy availability, host and viral densities, and the proportions of actively replicating viruses. We propose the hypothesis that in the energy-rich, high-host-density, euphotic depths, selection acts to favor diversity of the host recognition machinery to increase host range, while in energy-depleted aphotic waters, selection acts on viral replication fitness, enhancing diversity in auxiliary metabolic genes. IMPORTANCE Viruses are extremely abundant and diverse biological entities that contribute to the functioning of marine ecosystems. Despite their recognized importance, few studies have addressed trends of mutation accumulation in marine viral communities across depth gradients. By investigating these trends, we show that mutation frequencies differ among viral genes according to their molecular functions, with the highest microdiversity occurring among proteins related to host metabolism, followed by structural proteins and, lastly, genome replication proteins. This is in agreement with evolutionary theory that postulates that housekeeping genes are under strong purifying selection. We also observed a positive association between depth and microdiversity. One exception to this trend was the host recognition proteins from the deep chlorophyll maximum, which displayed strikingly high microdiversity, which we hypothesize to be associated with intraspecies competition for hosts. Finally, our data allowed us to propose a theoretical model for viral microdiversity across the depth gradient. These discoveries are of special relevance because many of the viral genomic sequences discovered here were predicted to infect some of the most abundant bacteria in marine ecosystems, such as “Candidatus Pelagibacter,” Puniceispirillum, and Prochlorococcus.
format	article
author	Felipe Hernandes Coutinho Riccardo Rosselli Francisco Rodríguez-Valera
author_facet	Felipe Hernandes Coutinho Riccardo Rosselli Francisco Rodríguez-Valera
author_sort	Felipe Hernandes Coutinho
title	Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean
title_short	Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean
title_full	Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean
title_fullStr	Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean
title_full_unstemmed	Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean
title_sort	trends of microdiversity reveal depth-dependent evolutionary strategies of viruses in the mediterranean
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/0fa899e8286c4e7897962607dcad07c2
work_keys_str_mv	AT felipehernandescoutinho trendsofmicrodiversityrevealdepthdependentevolutionarystrategiesofvirusesinthemediterranean AT riccardorosselli trendsofmicrodiversityrevealdepthdependentevolutionarystrategiesofvirusesinthemediterranean AT franciscorodriguezvalera trendsofmicrodiversityrevealdepthdependentevolutionarystrategiesofvirusesinthemediterranean
_version_	1718376006411091968

Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean

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