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Virus Found in a Boreal Lake Links Ssdna and Dsdna Viruses

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Virus Found in a Boreal Lake Links Ssdna and Dsdna Viruses Virus found in a boreal lake links ssDNA and dsDNA viruses Elina Laantoa,b,1, Sari Mäntynena,b,1, Luigi De Colibusc,1, Jenni Marjakangasa,b, Ashley Gillumc, David I. Stuartc,d, Janne J. Ravanttia,b,e, Juha T. Huiskonenc,e,2, and Lotta-Riina Sundberga,b,2 aCentre of Excellence in Biological Interactions, Department of Biological and Environmental Science, University of Jyväskylä, 40014 Jyväskylä, Finland; bNanoscience Center, University of Jyväskylä, 40014 Jyväskylä, Finland; cDivision of Structural Biology, Welcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, United Kingdom; dDiamond Light Source, Didcot OX11 0DE, United Kingdom; and eDepartment of Biosciences, University of Helsinki, 00014 Helsinki, Finland Edited by James L. Van Etten, University of Nebraska–Lincoln, Lincoln, NE, and approved June 5, 2017 (received for review March 8, 2017) Viruses have impacted the biosphere in numerous ways since the it has been suggested, that the major capsid protein (MCP) fold dawn of life. However, the evolution, genetic, structural, and taxo- and overall virion structure could be used to classify viruses and nomic diversity of viruses remain poorly understood, in part because track down their deeper evolutionary relationships (17). sparse sampling of the virosphere has concentrated mostly on We describe here an icosahedral virus with an ssDNA genome “ ” exploring the abundance and diversity of dsDNA viruses. Further- and an internal lipid membrane designated FLiP (Flavobacterium- more, viral genomes are highly diverse, and using only the current infecting, lipid-containing phage). The 9,174-nt-long genome of sequence-based methods for classifying viruses and studying FLiP has limited sequence similarities with previously identified their phylogeny is complicated. Here we describe a virus, FLiP viruses. Based on cryo-electron microscopy (cryo-EM) at 4-Å resolution, the virion structure of FLiP displays the pseudo tri- (Flavobacterium-infecting, lipid-containing phage), with a circular angulation number (T) = 21 dextro organization previously shown ssDNA genome and an internal lipid membrane enclosed in the only for the marine dsDNA phage PM2. The MCP consists of icosahedral capsid. The 9,174-nt-long genome showed limited se- two β-barrels with jellyroll topology and closely resembles quence similarity to other known viruses. The genetic data imply dsDNA viruses of the PRD1–adenovirus lineage. Thus, these that this virus might use replication mechanisms similar to those structural data indicate evolutionary relatedness between some found in other ssDNA replicons. However, the structure of the viral ssDNA and dsDNA viruses and suggest that it would be bene- major capsid protein, elucidated at near-atomic resolution using ficial to complement traditional sequence-based systems with cryo-electron microscopy, is strikingly similar to that observed in structure-based approaches. dsDNA viruses of the PRD1–adenovirus lineage, characterized by a major capsid protein bearing two β-barrels. The strong similarity Results between FLiP and another member of the structural lineage, bac- FLiP Is a Phage That Infects Flavobacterium. The virus designated teriophage PM2, extends to the capsid organization (pseudo T = 21 FLiP was isolated together with the host bacterium from a boreal dextro) despite the difference in the genetic material packaged and freshwater habitat in Central Finland in September, 2010. The the lack of significant sequence similarity. Significance cryo-electron microscopy | Flavobacterium | lipids | genome | structure We describe the phage FLiP, an ssDNA virus with an icosahedral lthough conservative calculations estimate that the number capsid and an internal lipid membrane. The FLiP genome shows 31 Aof viruses in the biome exceed 10 virions (1), this enor- limited similarity to known sequences, although an ssDNA repli- mous group of biological entities is largely unexplored because cation mechanism was implied by genome analysis. However, only a fraction of viruses have been studied in detail. In recent because the capsid protein fold indicates relatedness with the years, the enormous diversity of the viral world (2) has been re- dsDNA viruses of the PRD1–adenovirus lineage, FLiP exhibits a vealed by high-throughput sequencing of viral genomes. Although unique combination of structural and replication modules. It is the traditionally used virus detection methods (epifluorescence suggested that the capsid protein structure could be used to microscopy, pulse-field gel electrophoresis, and early metagenomic complement the sequence data when classifying viruses and in studies) have been selective for dsDNA viruses (3–5), recent met- detecting their deep evolutionary relationships, especially in the agenomic studies have revealed that the number of ssDNA viruses absence of sequence similarities. Furthermore, these findings in nature has been grossly underestimated. In fact, ssDNA viruses demonstrate the value of characterizing unknown viruses from are widespread and may predominate in certain habitats, including diverse environmental sources to understand the diversity of the the oceans and arctic freshwaters (6–10). However, only a few microbial world. ssDNA viruses have been cultivated in laboratory conditions, and therefore detailed structural and biochemical analyses of distinct Author contributions: J.J.R., J.T.H., and L.-R.S. designed research; E.L., S.M., L.D.C., J.M., ssDNA viruses are mostly lacking. Detailed characterization of and A.G. performed research; D.I.S. and L.-R.S. contributed new reagents/analytic tools; E.L., S.M., L.D.C., J.M., A.G., J.J.R., and J.T.H. analyzed data; E.L., S.M., L.D.C., and J.T.H. novel virus isolates is essential to expand our understanding of wrote the paper; and D.I.S., J.J.R., and L.-R.S. supervised the project. evolutionary relationships among viruses and their role in mi- The authors declare no conflict of interest. crobial communities (11). This article is a PNAS Direct Submission. Using solely sequence-based methods for virus classification and phylogeny is complicated because of the enormous genetic Data deposition: The genome sequence of FLiP has been submitted to GenBank (accession no. MF361639). The cryo-electron microscopy 3D reconstruction map of FLiP has been diversity among viruses (11, 12). However, essential viral struc- deposited with the Electron Microscopy Data Bank (EMDB) (accession code EMD-3771). tures and functions are often strongly conserved (13, 14). There The modeled structure of the virus MCP shell has been deposited with the Protein Data seem to be only a limited number of folds a functional protein Bank (PDB) (accession code 5OAC). may adopt, and stringent structural constraints further decrease 1E.L., S.M., and L.D.C. contributed equally to this work. the number of folds suitable for forming a capsid protein. These 2To whom correspondence may be addressed. Email: [email protected] or lotta-riina. constraints make the serendipitous invention of new architec- [email protected]. tures very unlikely, so that only a very limited number of lineages This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. of virion architecture have been observed (15, 16). Therefore, 1073/pnas.1703834114/-/DCSupplemental. 8378–8383 | PNAS | August 1, 2017 | vol. 114 | no. 31 www.pnas.org/cgi/doi/10.1073/pnas.1703834114 Downloaded by guest on September 28, 2021 host bacterium was identified as a member of genus Flavobacterium (Bacteroidetes) by 16S rRNA gene sequencing. Flavobacterium species are important members of freshwater bacterial communities in the boreal regions (18, 19). The greatest similarity to the obtained 1,422-bp-long 16S rRNA gene sequence was to several Flavobacterium sp. strains (99%). Accordingly, the host bacte- rium strain of FLiP was designated as Flavobacterium sp. B330. FLiP virions were collected for purification from plate lysate. Phage particles were concentrated from the filtered lysate with PEG-NaCl precipitation and then were purified by rate zonal and equilibrium centrifugation to near homogeneity. The rate zonal centrifugation was optimized using different gradient ma- terials (iodixanol, glycerol, and sucrose). The phage yield was significantly higher in the sucrose gradient; therefore this gra- dient material was used routinely for purification in both rate zonal and equilibrium centrifugation. This method yielded highly purified particles with specific infectivity of 1.28 × 1012 pfu/mg of protein. The typical recovery and specific infectivity for each purification step are presented in Table S1. The FLiP Genome Is a Circular ssDNA Molecule with 16 Putative ORFs. FLiP genomic nucleic acid was extracted from purified virions. Nuclease treatments (Fig. S1) revealed that the genome is an ssDNA molecule. Genome sequencing resulted in a 9,174-nt- long molecule, with an overall guanine–cytosine (GC) content Fig. 2. 3D cryo-EM reconstruction of the FLiP virion. (A) Surface rendering of 34% (Fig. 1A). A total of 16 putative ORFs were identified of the FLiP virion. The MCPs are colored yellow, green, blue, and red. Other from the genome using the programs Glimmer (20) and Gene- structural components are colored gray. The icosahedral twofold (ellipse), Mark (21). All the ORFs were oriented in the same direction. threefold (triangle), and fivefold (pentagons) axes of symmetry are in- Most of the ORFs showed limited similarity to other sequences dicated. The triangulation number T = 21 of the icosahedral
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