Cargando…

Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss

The study of bacteriophages is experiencing a resurgence owing to their antibacterial efficacy, lack of side effects, and low production cost. Nonetheless, the interactions between Staphylococcus aureus bacteriophages and their hosts remain unexplored. In this study, whole-genome sequences of 188 S....

Descripción completa

Detalles Bibliográficos
Autores principales: Zhou, Wenyuan, Wen, Hua, Li, Yajie, Gao, Yajun, Zheng, Xiangfeng, Yuan, Lei, Zhu, Guoqiang, Yang, Zhenquan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9230882/
https://www.ncbi.nlm.nih.gov/pubmed/35746669
http://dx.doi.org/10.3390/v14061199
_version_ 1784735183556050944
author Zhou, Wenyuan
Wen, Hua
Li, Yajie
Gao, Yajun
Zheng, Xiangfeng
Yuan, Lei
Zhu, Guoqiang
Yang, Zhenquan
author_facet Zhou, Wenyuan
Wen, Hua
Li, Yajie
Gao, Yajun
Zheng, Xiangfeng
Yuan, Lei
Zhu, Guoqiang
Yang, Zhenquan
author_sort Zhou, Wenyuan
collection PubMed
description The study of bacteriophages is experiencing a resurgence owing to their antibacterial efficacy, lack of side effects, and low production cost. Nonetheless, the interactions between Staphylococcus aureus bacteriophages and their hosts remain unexplored. In this study, whole-genome sequences of 188 S. aureus bacteriophages—20 Podoviridae, 56 Herelleviridae, and 112 Siphoviridae—were obtained from the National Center for Biotechnology Information (NCBI, USA) genome database. A phylogenetic tree was constructed to estimate their genetic relatedness using single-nucleotide polymorphism analysis. Comparative analysis was performed to investigate the structural diversity and ortholog groups in the subdividing clusters. Mosaic structures and gene content were compared in relation to phylogeny. Phylogenetic analysis revealed that the bacteriophages could be distinguished into three lineages (I–III), including nine subdividing clusters and seven singletons. The subdividing clusters shared similar mosaic structures and core ortholog clusters, including the genes involved in bacteriophage morphogenesis and DNA packaging. Notably, several functional modules of bacteriophages 187 and 2368A shared more than 95% nucleotide sequence identity with prophages in the S. aureus strain RJ1267 and the Staphylococcus pseudintermedius strain SP_11306_4, whereas other modules exhibited little nucleotide sequence similarity. Moreover, the cluster phages shared similar types of holins, lysins, and DNA packaging genes and harbored diverse genes associated with DNA replication and virulence. The data suggested that the genetic diversity of S. aureus bacteriophages was likely due to gene replacement, acquisition, and loss among staphylococcal phages, which may have crossed species barriers. Moreover, frequent module exchanges likely occurred exclusively among the subdividing cluster phages. We hypothesize that during evolution, the S. aureus phages enhanced their DNA replication in host cells and the adaptive environment of their host.
format Online
Article
Text
id pubmed-9230882
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-92308822022-06-25 Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss Zhou, Wenyuan Wen, Hua Li, Yajie Gao, Yajun Zheng, Xiangfeng Yuan, Lei Zhu, Guoqiang Yang, Zhenquan Viruses Article The study of bacteriophages is experiencing a resurgence owing to their antibacterial efficacy, lack of side effects, and low production cost. Nonetheless, the interactions between Staphylococcus aureus bacteriophages and their hosts remain unexplored. In this study, whole-genome sequences of 188 S. aureus bacteriophages—20 Podoviridae, 56 Herelleviridae, and 112 Siphoviridae—were obtained from the National Center for Biotechnology Information (NCBI, USA) genome database. A phylogenetic tree was constructed to estimate their genetic relatedness using single-nucleotide polymorphism analysis. Comparative analysis was performed to investigate the structural diversity and ortholog groups in the subdividing clusters. Mosaic structures and gene content were compared in relation to phylogeny. Phylogenetic analysis revealed that the bacteriophages could be distinguished into three lineages (I–III), including nine subdividing clusters and seven singletons. The subdividing clusters shared similar mosaic structures and core ortholog clusters, including the genes involved in bacteriophage morphogenesis and DNA packaging. Notably, several functional modules of bacteriophages 187 and 2368A shared more than 95% nucleotide sequence identity with prophages in the S. aureus strain RJ1267 and the Staphylococcus pseudintermedius strain SP_11306_4, whereas other modules exhibited little nucleotide sequence similarity. Moreover, the cluster phages shared similar types of holins, lysins, and DNA packaging genes and harbored diverse genes associated with DNA replication and virulence. The data suggested that the genetic diversity of S. aureus bacteriophages was likely due to gene replacement, acquisition, and loss among staphylococcal phages, which may have crossed species barriers. Moreover, frequent module exchanges likely occurred exclusively among the subdividing cluster phages. We hypothesize that during evolution, the S. aureus phages enhanced their DNA replication in host cells and the adaptive environment of their host. MDPI 2022-05-31 /pmc/articles/PMC9230882/ /pubmed/35746669 http://dx.doi.org/10.3390/v14061199 Text en © 2022 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
Zhou, Wenyuan
Wen, Hua
Li, Yajie
Gao, Yajun
Zheng, Xiangfeng
Yuan, Lei
Zhu, Guoqiang
Yang, Zhenquan
Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss
title Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss
title_full Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss
title_fullStr Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss
title_full_unstemmed Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss
title_short Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss
title_sort whole-genome analysis reveals that bacteriophages promote environmental adaptation of staphylococcus aureus via gene exchange, acquisition, and loss
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9230882/
https://www.ncbi.nlm.nih.gov/pubmed/35746669
http://dx.doi.org/10.3390/v14061199
work_keys_str_mv AT zhouwenyuan wholegenomeanalysisrevealsthatbacteriophagespromoteenvironmentaladaptationofstaphylococcusaureusviageneexchangeacquisitionandloss
AT wenhua wholegenomeanalysisrevealsthatbacteriophagespromoteenvironmentaladaptationofstaphylococcusaureusviageneexchangeacquisitionandloss
AT liyajie wholegenomeanalysisrevealsthatbacteriophagespromoteenvironmentaladaptationofstaphylococcusaureusviageneexchangeacquisitionandloss
AT gaoyajun wholegenomeanalysisrevealsthatbacteriophagespromoteenvironmentaladaptationofstaphylococcusaureusviageneexchangeacquisitionandloss
AT zhengxiangfeng wholegenomeanalysisrevealsthatbacteriophagespromoteenvironmentaladaptationofstaphylococcusaureusviageneexchangeacquisitionandloss
AT yuanlei wholegenomeanalysisrevealsthatbacteriophagespromoteenvironmentaladaptationofstaphylococcusaureusviageneexchangeacquisitionandloss
AT zhuguoqiang wholegenomeanalysisrevealsthatbacteriophagespromoteenvironmentaladaptationofstaphylococcusaureusviageneexchangeacquisitionandloss
AT yangzhenquan wholegenomeanalysisrevealsthatbacteriophagespromoteenvironmentaladaptationofstaphylococcusaureusviageneexchangeacquisitionandloss