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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 principales: Arnau, Vicente, Díaz-Villanueva, Wladimiro, Mifsut Benet, Jorge, Villasante, Paula, Beamud, Beatriz, Mompó, Paula, Sanjuan, Rafael, González-Candelas, Fernando, Domingo-Calap, Pilar, Džunková, Mária
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10222151/
https://www.ncbi.nlm.nih.gov/pubmed/37243281
http://dx.doi.org/10.3390/v15051196
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author Arnau, Vicente
Díaz-Villanueva, Wladimiro
Mifsut Benet, Jorge
Villasante, Paula
Beamud, Beatriz
Mompó, Paula
Sanjuan, Rafael
González-Candelas, Fernando
Domingo-Calap, Pilar
Džunková, Mária
author_facet Arnau, Vicente
Díaz-Villanueva, Wladimiro
Mifsut Benet, Jorge
Villasante, Paula
Beamud, Beatriz
Mompó, Paula
Sanjuan, Rafael
González-Candelas, Fernando
Domingo-Calap, Pilar
Džunková, Mária
author_sort Arnau, Vicente
collection PubMed
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.
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spelling pubmed-102221512023-05-28 Inference of the Life Cycle of Environmental Phages from Genomic Signature Distances to Their Hosts Arnau, Vicente Díaz-Villanueva, Wladimiro Mifsut Benet, Jorge Villasante, Paula Beamud, Beatriz Mompó, Paula Sanjuan, Rafael González-Candelas, Fernando Domingo-Calap, Pilar Džunková, Mária Viruses Article 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. MDPI 2023-05-19 /pmc/articles/PMC10222151/ /pubmed/37243281 http://dx.doi.org/10.3390/v15051196 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Arnau, Vicente
Díaz-Villanueva, Wladimiro
Mifsut Benet, Jorge
Villasante, Paula
Beamud, Beatriz
Mompó, Paula
Sanjuan, Rafael
González-Candelas, Fernando
Domingo-Calap, Pilar
Džunková, Mária
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
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_short 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
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10222151/
https://www.ncbi.nlm.nih.gov/pubmed/37243281
http://dx.doi.org/10.3390/v15051196
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