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Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements.

ABSTRACT: Phage satellites are mobile genetic elements that propagate by parasitizing bacteriophage replication. We report here the discovery of abundant and diverse phage satellites that were packaged as concatemeric repeats within naturally occurring bacteriophage particles in seawater. These same phage-parasitizing mobile elements were found integrated in the genomes of dominant co-occurring bacterioplankton species. Like known phage satellites, many marine phage satellites encoded genes for integration, DNA replication, phage interference, and capsid assembly. Many also contained distinctive gene suites indicative of unique virus hijacking, phage immunity, and mobilization mechanisms. Marine phage satellite sequences were widespread in local and global oceanic virioplankton populations, reflecting their ubiquity, abundance, and temporal persistence in marine planktonic communities worldwide. Their gene content and putative life cycles suggest they may impact host-cell phage immunity and defense, lateral gene transfer, bacteriophage-induced cell mortality and cellular host and virus productivity. Given that marine phage satellites cannot be distinguished from bona fide viral particles via commonly used microscopic techniques, their predicted numbers (∼3.2 × 10²⁶ in the ocean) may influence current estimates of virus densities, production, and virus-induced mortality. In total, the data suggest that marine phage satellites have potential to significantly impact the ecology and evolution of bacteria and their viruses throughout the oceans. We predict that any habitat that harbors bacteriophage will also harbor similar phage satellites, making them a ubiquitous feature of most microbiomes on Earth.

SUBMITTER: Eppley JM

PROVIDER: S-EPMC9618062 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements.

Eppley John M JM Biller Steven J SJ Luo Elaine E Burger Andrew A DeLong Edward F EF

Proceedings of the National Academy of Sciences of the United States of America 20221018 43

Phage satellites are mobile genetic elements that propagate by parasitizing bacteriophage replication. We report here the discovery of abundant and diverse phage satellites that were packaged as concatemeric repeats within naturally occurring bacteriophage particles in seawater. These same phage-parasitizing mobile elements were found integrated in the genomes of dominant co-occurring bacterioplankton species. Like known phage satellites, many marine phage satellites encoded genes for integratio ...[more]

PMID: 36256808

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Project description:Bacillus pumilus exhibits substantial economic significance, with its metabolism, adaptability, and ecological functions regulated by its bacteriophages. Here, we isolated and characterized a novel temperate phage vB_BpuM-ZY1 from B. pumilus derived from mangrove sediments by mitomycin C induction. Phage vB_BpuM-ZY1 is a typical myophage, which has an icosahedral head with a diameter of 43.34 ± 2.14 nm and a long contractible tail with a length of 238.58 ± 5.18 nm. Genomic analysis indicated that vB_BpuM-ZY1 encodes genes for lysogeny control, and its life cycle may be intricately regulated by multiple mechanisms. vB_BpuM-ZY1 was predicted to employ P2-like 5'-extended-cos packaging strategy. In addition, genome-wide phylogenetic tree and proteome tree analyses indicated that vB_BpuM-ZY1 belongs to the Peduoviridae family but forms a separate branch at a deeper taxonomic level. Particularly, the comparative genomic analysis showed that vB_BpuM-ZY1 has less than 70% intergenomic similarities with its most similar phages. Thus, we propose that vB_BpuM-ZY1 is a novel Bacillus phage belonging to a new genus under the Peduoviridae family. The protein-sharing network analysis identified 44 vB_BpuM-ZY1-related phages. Interestingly, these evolutionarily related myophages infect a broad range of hosts across different phyla, which may be explained by the high structural variations of the host recognition domain in their central spike proteins. Collectively, our study will contribute to our understanding of Bacillus phage diversity and Bacillus-phage interactions, as well as provide essential knowledge for the industrial application of B. pumilus.ImportanceAlthough recent metagenomics research has obtained a wealth of phage genetic information, much of it is considered "dark matter" because of the lack of similarity with known sequences in the database. Therefore, the isolation and characterization of novel phages will help to interpret the vast unknown viral metagenome data and improve our understanding of phage diversity and phage-host interactions. Bacillus pumilus shows high economic relevance due to its wide applications in biotechnology, industry, biopharma, and environmental sectors. Since phages influence the abundance, metabolism, evolution, fitness, and ecological functions of bacteria through complex interactions, the significance of isolation and characterization of novel phages infecting B. pumilus is apparent. In this study, we isolated and characterized a B. pumilus phage belonging to a novel viral genus, which provides essential knowledge for phage biology as well as the industrial application of B. pumilus.

Dataset Information

Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements.

Publications

Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements.

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