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Phylogenomics of five Pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer

BACKGROUND: Along with the fast development and urbanization in developing countries, the waterbodies aside the growing cities become heavily polluted and highly eutrophic, thus leading to the seasonal outbreak of cyanobacterial bloom. Systematic isolation and characterization of freshwater cyanopha...

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Autores principales: Zhu, Jie, Yang, Feng, Du, Kang, Wei, Zi-Lu, Wu, Qing-Fa, Chen, Yuxing, Li, Wei-Fang, Li, Qiong, Zhou, Cong-Zhao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9837993/
https://www.ncbi.nlm.nih.gov/pubmed/36639816
http://dx.doi.org/10.1186/s40793-023-00461-5
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author Zhu, Jie
Yang, Feng
Du, Kang
Wei, Zi-Lu
Wu, Qing-Fa
Chen, Yuxing
Li, Wei-Fang
Li, Qiong
Zhou, Cong-Zhao
author_facet Zhu, Jie
Yang, Feng
Du, Kang
Wei, Zi-Lu
Wu, Qing-Fa
Chen, Yuxing
Li, Wei-Fang
Li, Qiong
Zhou, Cong-Zhao
author_sort Zhu, Jie
collection PubMed
description BACKGROUND: Along with the fast development and urbanization in developing countries, the waterbodies aside the growing cities become heavily polluted and highly eutrophic, thus leading to the seasonal outbreak of cyanobacterial bloom. Systematic isolation and characterization of freshwater cyanophages might provide a biological solution to control the awful blooms. However, genomic sequences and related investigations on the freshwater cyanophages remain very limited to date. RESULTS: Following our recently reported five cyanophages Pam1~Pam5 from Lake Chaohu in China, here we isolated another five cyanophages, termed Pan1~Pan5, which infect the cyanobacterium Pseudanabaena sp. Chao 1811. Whole-genome sequencing showed that they all contain a double-stranded DNA genome of 37.2 to 72.0 kb in length, with less than half of the putative open reading frames annotated with known functions. Remarkably, the siphophage Pan1 encodes an auxiliary metabolic gene phoH and constitutes, together with the host, a complete queuosine modification pathway. Proteomic analyses revealed that although Pan1~Pan5 are distinct from each other in evolution, Pan1 and Pan3 are somewhat similar to our previously identified cyanophages Pam3 and Pam1 at the genomic level, respectively. Moreover, phylogenetic analyses suggested that Pan1 resembles the α-proteobacterial phage vB_DshS-R5C, revealing direct evidence for phage-mediated horizontal gene transfer between cyanobacteria and α-proteobacteria. CONCLUSION: In addition to the previous reports of Pam1~Pam5, the present findings on Pan1~Pan5 largely enrich the library of reference freshwater cyanophages. The abundant genomic information provides a pool to identify novel genes and proteins of unknown function. Moreover, we found for the first time the evolutionary traces in the cyanophage that horizontal gene transfer might occur at the level of not only inter-species, but even inter-phylum. It indicates that the bacteriophage or cyanophage could be developed as a powerful tool for gene manipulation among various species or phyla. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00461-5.
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spelling pubmed-98379932023-01-14 Phylogenomics of five Pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer Zhu, Jie Yang, Feng Du, Kang Wei, Zi-Lu Wu, Qing-Fa Chen, Yuxing Li, Wei-Fang Li, Qiong Zhou, Cong-Zhao Environ Microbiome Research BACKGROUND: Along with the fast development and urbanization in developing countries, the waterbodies aside the growing cities become heavily polluted and highly eutrophic, thus leading to the seasonal outbreak of cyanobacterial bloom. Systematic isolation and characterization of freshwater cyanophages might provide a biological solution to control the awful blooms. However, genomic sequences and related investigations on the freshwater cyanophages remain very limited to date. RESULTS: Following our recently reported five cyanophages Pam1~Pam5 from Lake Chaohu in China, here we isolated another five cyanophages, termed Pan1~Pan5, which infect the cyanobacterium Pseudanabaena sp. Chao 1811. Whole-genome sequencing showed that they all contain a double-stranded DNA genome of 37.2 to 72.0 kb in length, with less than half of the putative open reading frames annotated with known functions. Remarkably, the siphophage Pan1 encodes an auxiliary metabolic gene phoH and constitutes, together with the host, a complete queuosine modification pathway. Proteomic analyses revealed that although Pan1~Pan5 are distinct from each other in evolution, Pan1 and Pan3 are somewhat similar to our previously identified cyanophages Pam3 and Pam1 at the genomic level, respectively. Moreover, phylogenetic analyses suggested that Pan1 resembles the α-proteobacterial phage vB_DshS-R5C, revealing direct evidence for phage-mediated horizontal gene transfer between cyanobacteria and α-proteobacteria. CONCLUSION: In addition to the previous reports of Pam1~Pam5, the present findings on Pan1~Pan5 largely enrich the library of reference freshwater cyanophages. The abundant genomic information provides a pool to identify novel genes and proteins of unknown function. Moreover, we found for the first time the evolutionary traces in the cyanophage that horizontal gene transfer might occur at the level of not only inter-species, but even inter-phylum. It indicates that the bacteriophage or cyanophage could be developed as a powerful tool for gene manipulation among various species or phyla. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00461-5. BioMed Central 2023-01-13 /pmc/articles/PMC9837993/ /pubmed/36639816 http://dx.doi.org/10.1186/s40793-023-00461-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zhu, Jie
Yang, Feng
Du, Kang
Wei, Zi-Lu
Wu, Qing-Fa
Chen, Yuxing
Li, Wei-Fang
Li, Qiong
Zhou, Cong-Zhao
Phylogenomics of five Pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer
title Phylogenomics of five Pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer
title_full Phylogenomics of five Pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer
title_fullStr Phylogenomics of five Pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer
title_full_unstemmed Phylogenomics of five Pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer
title_short Phylogenomics of five Pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer
title_sort phylogenomics of five pseudanabaena cyanophages and evolutionary traces of horizontal gene transfer
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9837993/
https://www.ncbi.nlm.nih.gov/pubmed/36639816
http://dx.doi.org/10.1186/s40793-023-00461-5
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