Characterization and comparative genomic analysis of a marine Bacillus phage reveal a novel viral genus

Abstract

ABSTRACT 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.

Keywords

• Bacillus phage
• Bacillus pumilus
• myophages
• novel genus