Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts

The environmental impact of uncultured phages is shaped by their preferred life cycle (lytic or lysogenic). However, our ability to predict it is very limited. We aimed to discriminate between lytic and lysogenic phages by comparing the similarity of their genomic signatures to those of their hosts,...

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Autores: Arnau V, Díaz-Villanueva W, Mifsut Benet J, Villasante P, Beamud B, Mompó P, Sanjuan R, González-Candelas F, Domingo-Calap P, Džunková M
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Recursos:Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)
Repositorio:r-FISABIO. Repositorio Institucional de Producción Científica
OAI Identifier:oai:fisabio.fundanetsuite.com:p15269
Acesso em linha:https://fisabio.portalinvestigacion.com/publicaciones/15269
Access Level:acceso abierto
Palavra-chave:genomic signatures
bacteriophages
lytic phages
lysogenic phages
single-cell genomics
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spelling Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their HostsArnau VDíaz-Villanueva WMifsut Benet JVillasante PBeamud BMompó PSanjuan RGonzález-Candelas FDomingo-Calap PDžunková Mgenomic signaturesbacteriophageslytic phageslysogenic phagessingle-cell genomicsThe environmental impact of uncultured phages is shaped by their preferred life cycle (lytic or lysogenic). However, our ability to predict it is very limited. We aimed to discriminate between lytic and lysogenic phages by comparing the similarity of their genomic signatures to those of their hosts, reflecting their co-evolution. We tested two approaches: (1) similarities of tetramer relative frequencies, (2) alignment-free comparisons based on exact k = 14 oligonucleotide matches. First, we explored 5126 reference bacterial host strains and 284 associated phages and found an approximate threshold for distinguishing lysogenic and lytic phages using both oligonucleotide-based methods. The analysis of 6482 plasmids revealed the potential for horizontal gene transfer between different host genera and, in some cases, distant bacterial taxa. Subsequently, we experimentally analyzed combinations of 138 Klebsiella pneumoniae strains and their 41 phages and found that the phages with the largest number of interactions with these strains in the laboratory had the shortest genomic distances to K. pneumoniae. We then applied our methods to 24 single-cells from a hot spring biofilm containing 41 uncultured phage-host pairs, and the results were compatible with the lysogenic life cycle of phages detected in this environment. In conclusion, oligonucleotide-based genome analysis methods can be used for predictions of (1) life cycles of environmental phages, (2) phages with the broadest host range in culture collections, and (3) potential horizontal gene transfer by plasmids.MDPI2023info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttps://fisabio.portalinvestigacion.com/publicaciones/15269Viruses-BaselISSN: 19994915reponame:r-FISABIO. Repositorio Institucional de Producción Científicainstname:Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)Inglésinfo:eu-repo/semantics/openAccessoai:fisabio.fundanetsuite.com:p152692026-06-11T12:45:17Z
dc.title.none.fl_str_mv Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts
title Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts
spellingShingle Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts
Arnau V
genomic signatures
bacteriophages
lytic phages
lysogenic phages
single-cell genomics
title_short Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts
title_full Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts
title_fullStr Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts
title_full_unstemmed Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts
title_sort Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts
dc.creator.none.fl_str_mv Arnau V
Díaz-Villanueva W
Mifsut Benet J
Villasante P
Beamud B
Mompó P
Sanjuan R
González-Candelas F
Domingo-Calap P
Džunková M
author Arnau V
author_facet Arnau V
Díaz-Villanueva W
Mifsut Benet J
Villasante P
Beamud B
Mompó P
Sanjuan R
González-Candelas F
Domingo-Calap P
Džunková M
author_role author
author2 Díaz-Villanueva W
Mifsut Benet J
Villasante P
Beamud B
Mompó P
Sanjuan R
González-Candelas F
Domingo-Calap P
Džunková M
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv genomic signatures
bacteriophages
lytic phages
lysogenic phages
single-cell genomics
topic genomic signatures
bacteriophages
lytic phages
lysogenic phages
single-cell genomics
description The environmental impact of uncultured phages is shaped by their preferred life cycle (lytic or lysogenic). However, our ability to predict it is very limited. We aimed to discriminate between lytic and lysogenic phages by comparing the similarity of their genomic signatures to those of their hosts, reflecting their co-evolution. We tested two approaches: (1) similarities of tetramer relative frequencies, (2) alignment-free comparisons based on exact k = 14 oligonucleotide matches. First, we explored 5126 reference bacterial host strains and 284 associated phages and found an approximate threshold for distinguishing lysogenic and lytic phages using both oligonucleotide-based methods. The analysis of 6482 plasmids revealed the potential for horizontal gene transfer between different host genera and, in some cases, distant bacterial taxa. Subsequently, we experimentally analyzed combinations of 138 Klebsiella pneumoniae strains and their 41 phages and found that the phages with the largest number of interactions with these strains in the laboratory had the shortest genomic distances to K. pneumoniae. We then applied our methods to 24 single-cells from a hot spring biofilm containing 41 uncultured phage-host pairs, and the results were compatible with the lysogenic life cycle of phages detected in this environment. In conclusion, oligonucleotide-based genome analysis methods can be used for predictions of (1) life cycles of environmental phages, (2) phages with the broadest host range in culture collections, and (3) potential horizontal gene transfer by plasmids.
publishDate 2023
dc.date.none.fl_str_mv 2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://fisabio.portalinvestigacion.com/publicaciones/15269
url https://fisabio.portalinvestigacion.com/publicaciones/15269
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv MDPI
publisher.none.fl_str_mv MDPI
dc.source.none.fl_str_mv Viruses-Basel
ISSN: 19994915
reponame:r-FISABIO. Repositorio Institucional de Producción Científica
instname:Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)
instname_str Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)
reponame_str r-FISABIO. Repositorio Institucional de Producción Científica
collection r-FISABIO. Repositorio Institucional de Producción Científica
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,812429

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