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A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas

Members from the Inoviridae family with striking features are widespread, highly diverse, and ecologically pervasive across multiple hosts and environments. However, a small number of inoviruses have been isolated and studied. Here, a filamentous phage infecting Alteromonas abrolhosensis, designated...

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Autores principales: Jia, Kuntong, Peng, Yongyi, Chen, Xueji, Jian, Huahua, Jin, Min, Yi, Zhiwei, Su, Ming, Dong, Xiyang, Yi, Meisheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769780/
https://www.ncbi.nlm.nih.gov/pubmed/36301121
http://dx.doi.org/10.1128/spectrum.03388-22
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author Jia, Kuntong
Peng, Yongyi
Chen, Xueji
Jian, Huahua
Jin, Min
Yi, Zhiwei
Su, Ming
Dong, Xiyang
Yi, Meisheng
author_facet Jia, Kuntong
Peng, Yongyi
Chen, Xueji
Jian, Huahua
Jin, Min
Yi, Zhiwei
Su, Ming
Dong, Xiyang
Yi, Meisheng
author_sort Jia, Kuntong
collection PubMed
description Members from the Inoviridae family with striking features are widespread, highly diverse, and ecologically pervasive across multiple hosts and environments. However, a small number of inoviruses have been isolated and studied. Here, a filamentous phage infecting Alteromonas abrolhosensis, designated ϕAFP1, was isolated from the South China Sea and represented a novel genus of Inoviridae. ϕAFP1 consisted of a single-stranded DNA genome (5986 bp), encoding eight putative ORFs. Comparative analyses revealed ϕAFP1 could be regarded as genetic mosaics having homologous sequences with Ralstonia and Stenotrophomonas phages. The temporal transcriptome analysis of A. abrolhosensis to ϕAFP1 infection revealed that 7.78% of the host genes were differentially expressed. The genes involved in translation processes, ribosome pathways, and degradation of multiple amino acid pathways at the plateau period were upregulated, while host material catabolic and bacterial motility-related genes were downregulated, indicating that ϕAFP1 might hijack the energy of the host for the synthesis of phage proteins. ϕAFP1 exerted step-by-step control on host genes through the appropriate level of utilizing host resources. Our study provided novel information for a better understanding of filamentous phage characteristics and phage-host interactions. IMPORTANCE Alteromonas is widely distributed and plays a vital role in biogeochemical in marine environments. However, little information about Alteromonas phages is available. Here, we isolated and characterized the biological characteristics and genome sequence of a novel inovirus infecting Alteromonas abrolhosensis, designated ϕAFP1, representing a novel viral genus of Inoviridae. We then presented a comprehensive view of the ϕAFP1 phage-Alteromonas abrolhosensis interactions, elucidating reprogramed host metabolism and motility. Our study provided novel information for better comprehension of filamentous phage characteristics and phage-host interactions.
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spelling pubmed-97697802022-12-22 A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas Jia, Kuntong Peng, Yongyi Chen, Xueji Jian, Huahua Jin, Min Yi, Zhiwei Su, Ming Dong, Xiyang Yi, Meisheng Microbiol Spectr Research Article Members from the Inoviridae family with striking features are widespread, highly diverse, and ecologically pervasive across multiple hosts and environments. However, a small number of inoviruses have been isolated and studied. Here, a filamentous phage infecting Alteromonas abrolhosensis, designated ϕAFP1, was isolated from the South China Sea and represented a novel genus of Inoviridae. ϕAFP1 consisted of a single-stranded DNA genome (5986 bp), encoding eight putative ORFs. Comparative analyses revealed ϕAFP1 could be regarded as genetic mosaics having homologous sequences with Ralstonia and Stenotrophomonas phages. The temporal transcriptome analysis of A. abrolhosensis to ϕAFP1 infection revealed that 7.78% of the host genes were differentially expressed. The genes involved in translation processes, ribosome pathways, and degradation of multiple amino acid pathways at the plateau period were upregulated, while host material catabolic and bacterial motility-related genes were downregulated, indicating that ϕAFP1 might hijack the energy of the host for the synthesis of phage proteins. ϕAFP1 exerted step-by-step control on host genes through the appropriate level of utilizing host resources. Our study provided novel information for a better understanding of filamentous phage characteristics and phage-host interactions. IMPORTANCE Alteromonas is widely distributed and plays a vital role in biogeochemical in marine environments. However, little information about Alteromonas phages is available. Here, we isolated and characterized the biological characteristics and genome sequence of a novel inovirus infecting Alteromonas abrolhosensis, designated ϕAFP1, representing a novel viral genus of Inoviridae. We then presented a comprehensive view of the ϕAFP1 phage-Alteromonas abrolhosensis interactions, elucidating reprogramed host metabolism and motility. Our study provided novel information for better comprehension of filamentous phage characteristics and phage-host interactions. American Society for Microbiology 2022-10-27 /pmc/articles/PMC9769780/ /pubmed/36301121 http://dx.doi.org/10.1128/spectrum.03388-22 Text en Copyright © 2022 Jia et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Jia, Kuntong
Peng, Yongyi
Chen, Xueji
Jian, Huahua
Jin, Min
Yi, Zhiwei
Su, Ming
Dong, Xiyang
Yi, Meisheng
A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas
title A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas
title_full A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas
title_fullStr A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas
title_full_unstemmed A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas
title_short A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas
title_sort novel inovirus reprograms metabolism and motility of marine alteromonas
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769780/
https://www.ncbi.nlm.nih.gov/pubmed/36301121
http://dx.doi.org/10.1128/spectrum.03388-22
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