Dataset Information

Genomic Analysis of Mic1 Reveals a Novel Freshwater Long-Tailed Cyanophage.

ABSTRACT: Lake Chaohu, one of the five largest freshwater lakes in China, has been suffering from severe cyanobacterial blooms in the summer for many years. Cyanophages, the viruses that specifically infect cyanobacteria, play a key role in modulating cyanobacterial population, and thus regulate the emergence and decline of cyanobacterial blooms. Here we report a long-tailed cyanophage isolated from Lake Chaohu, termed Mic1, which specifically infects the cyanobacterium Microcystis aeruginosa. Mic1 has an icosahedral head of 88 nm in diameter and a long flexible tail of 400 nm. It possesses a circular genome of 92,627 bp, which contains 98 putative open reading frames. Genome sequence analysis enabled us to define a novel terminase large subunit that consists of two types of intein, indicating that the genome packaging of Mic1 is under fine control via posttranslational maturation of the terminase. Moreover, phylogenetic analysis suggested Mic1 and mitochondria share a common evolutionary origin of DNA polymerase ? gene. All together, these findings provided a start-point for investigating the co-evolution of cyanophages and its cyanobacterial hosts.

SUBMITTER: Yang F

PROVIDER: S-EPMC7156551 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Genomic Analysis of Mic1 Reveals a Novel Freshwater Long-Tailed Cyanophage.

Yang Feng F Jin Hua H Wang Xiao-Qian XQ Li Qiong Q Zhang Jun-Tao JT Cui Ning N Jiang Yong-Liang YL Chen Yuxing Y Wu Qing-Fa QF Zhou Cong-Zhao CZ Li Wei-Fang WF

Frontiers in microbiology 20200408

Lake Chaohu, one of the five largest freshwater lakes in China, has been suffering from severe cyanobacterial blooms in the summer for many years. Cyanophages, the viruses that specifically infect cyanobacteria, play a key role in modulating cyanobacterial population, and thus regulate the emergence and decline of cyanobacterial blooms. Here we report a long-tailed cyanophage isolated from Lake Chaohu, termed Mic1, which specifically infects the cyanobacterium <i>Microcystis aeruginosa</i>. Mic1 ...[more]

PMID: 32322241

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Project description:A worldwide ecological issue, cyanobacterial blooms in marine and freshwater have caused enormous losses in both the economy and the environment. Virulent cyanophages-specifically, infecting and lysing cyanobacteria-are key ecological factors involved in limiting the overall extent of the population development of cyanobacteria. Over the past three decades, reports have mainly focused on marine Prochlorococcus and Synechococcus cyanophages, while information on freshwater cyanophages remained largely unknown. In this study, a novel freshwater cyanophage, named Lbo240-yong1, was isolated via the double-layer agar plate method using Leptolyngbya boryana FACHB-240 as a host. Transmission electron microscopy observation illustrated the icosahedral head (50 ± 5 nm in diameter) and short tail (20 ± 5 nm in length) of Lbo240-yong1. Experimental infection against 37 cyanobacterial strains revealed that host-strain-specific Lbo240-yong1 could only lyse FACHB-240. The complete genome of Lbo240-yong1 is a double-stranded DNA of 39,740 bp with a G+C content of 51.99%, and it harbors 44 predicted open reading frames (ORFs). A Lbo240-yong1 ORF shared the highest identity with a gene of a filamentous cyanobacterium, hinting at a gene exchange between the cyanophage and cyanobacteria. A BLASTn search illustrated that Lbo240-yong1 had the highest sequence similarity with the Phormidium cyanophage Pf-WMP4 (89.67% identity, 84% query coverage). In the proteomic tree based on genome-wide sequence similarities, Lbo240-yong1, three Phormidium cyanophages (Pf-WMP4, Pf-WMP3, and PP), one Anabaena phage (A-4L), and one unclassified Arthronema cyanophage (Aa-TR020) formed a monophyletic group that was more deeply diverging than several other families. Pf-WMP4 is the only member of the independent genus Wumpquatrovirus that belongs to the Caudovircetes class. Pf-WMP3 and PP formed the independent genus Wumptrevirus. Anabaena phage A-4L is the only member of the independent Kozyakovvirus genus. The six cyanopodoviruses share similar gene arrangements. Eight core genes were found in them. We propose, here, to set up a new taxonomic family comprising the six freshwater cyanopodoviruses infecting filamentous cyanobacteria. This study enriched the field's knowledge of freshwater cyanophages.

Project description:While filamentous cyanobacteria play a crucial role in food web dynamics and biogeochemical cycling of many aquatic ecosystems around the globe, the knowledge regarding the phages infecting them is limited. Here, we describe the complete genome of the virulent cyanophage vB_AphaS-CL131 (here, CL 131), a Siphoviridae phage that infects the filamentous diazotrophic bloom-forming cyanobacterium Aphanizomenon flos-aquae in the brackish Baltic Sea. CL 131 features a 112,793-bp double-stranded DNA (dsDNA) genome encompassing 149 putative open reading frames (ORFs), of which the majority (86%) lack sequence homology to genes with known functions in other bacteriophages or bacteria. Phylogenetic analysis revealed that CL 131 possibly represents a new evolutionary lineage within the group of cyanophages infecting filamentous cyanobacteria, which form a separate cluster from phages infecting unicellular cyanobacteria. CL 131 encodes a putative type V-U2 CRISPR-Cas system with one spacer (out of 10) targeting a DNA primase pseudogene in a cyanobacterium and a putative type II toxin-antitoxin system, consisting of a GNAT family N-acetyltransferase and a protein of unknown function containing the PRK09726 domain (characteristic of HipB antitoxins). Comparison of CL 131 proteins to reads from Baltic Sea and other available fresh- and brackish-water metagenomes and analysis of CRISPR-Cas arrays in publicly available A. flos-aquae genomes demonstrated that phages similar to CL 131 are present and dynamic in the Baltic Sea and share a common history with their hosts dating back at least several decades. In addition, different CRISPR-Cas systems within individual A. flos-aquae genomes targeted several sequences in the CL 131 genome, including genes related to virion structure and morphogenesis. Altogether, these findings revealed new genomic information for exploring viral diversity and provide a model system for investigation of virus-host interactions in filamentous cyanobacteria.IMPORTANCE The genomic characterization of novel cyanophage vB_AphaS-CL131 and the analysis of its genomic features in the context of other viruses, metagenomic data, and host CRISPR-Cas systems contribute toward a better understanding of aquatic viral diversity and distribution in general and of brackish-water cyanophages infecting filamentous diazotrophic cyanobacteria in the Baltic Sea in particular. The results of this study revealed previously undescribed features of cyanophage genomes (e.g., self-excising intein-containing putative dCTP deaminase and putative cyanophage-encoded CRISPR-Cas and toxin-antitoxin systems) and can therefore be used to predict potential interactions between bloom-forming cyanobacteria and their cyanophages.

Dataset Information

Genomic Analysis of Mic1 Reveals a Novel Freshwater Long-Tailed Cyanophage.

Publications

Genomic Analysis of Mic1 Reveals a Novel Freshwater Long-Tailed Cyanophage.

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