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A New Family of Hybrid Virophages from an Animal Gut Metagenome Natalya Yutin, Vladimir V Kapitonov and Eugene V Koonin*

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A New Family of Hybrid Virophages from an Animal Gut Metagenome Natalya Yutin, Vladimir V Kapitonov and Eugene V Koonin* Yutin et al. Biology Direct (2015) 10:19 DOI 10.1186/s13062-015-0054-9 DISCOVERY NOTES Open Access A new family of hybrid virophages from an animal gut metagenome Natalya Yutin, Vladimir V Kapitonov and Eugene V Koonin* Abstract Search of metagenomics sequence databases for homologs of virophage capsid proteins resulted in the discovery of a new family of virophages in the sheep rumen metagenome. The genomes of the rumen virophages (RVP) encode a typical virophage major capsid protein, ATPase and protease combined with a Polinton-type, protein primed family B DNA polymerase. The RVP genomes appear to be linear molecules, with terminal inverted repeats. Thus, the RVP seem to represent virophage-Polinton hybrids that are likely capable of formation of infectious virions. Virion proteins of mimiviruses were detected in the same metagenomes as the RVP suggesting that the virophages of the new family parasitize on giant viruses that infect protist inhabitants of the rumen. This article was reviewed by Mart Krupovic and Kenneth Stedman; for complete reviews, see the Reviewers’ Reports section. Findings been isolated as infectious particles and shown to be associ- With the rapid increase of the quantity and quality of ated with different members of the family Mimiviridae available metagenomics sequences, metagenomes have [11-13], and 9 additional virophage genomes have been as- become a rich source for the discovery of novel viruses sembled from aquatic metagenomes [14-16]. The first vir- [1-3]. A prominent case in point is the recent discovery ophage, named Sputnik, was discovered as a parasite of of a novel, abundant and diversified group of viruses that Acanthamoeba castellani mimivirus [11], and reproduction are chimeras of genes from single-stranded DNA and of the related Zamilon virophage is supported by several positive-strand RNA viruses [4-7]. So far none of these mimiviruses [13]. The third identified virophage, denoted viruses has been isolated in the form of infectious parti- Mavirus, is a parasite of the giant virus that infects the fla- cles but metagenomic sequence analysis suggests that gellate Cafeteria roenbergensis [12]. Sputnik and Mavirus are they might be major components of viromes in various prototypes of two distinct families of virophages; the found- environments. Equally striking is the assembly of a novel ing member of a third family is Organic Lake Virophage bacteriophage that apparently accounts for a substantial (OLV) whose genome has been assembled from a metagen- part of the human gut virome but remained unknown ome and that is thought to parasitize on Organic Lake phy- until the advent of metagenomics [8]. These success codnaviruses [14] that subsequently have been reclassified stories prompt focused mining of metagenomic data- as putative members of the extended family Mimiviridae bases for novel genetic elements. [17,18]. So far all (putative) virophage genomes assem- We were interested in mining metagenomes to explore bled from metagenomes fall into one of the above three the diversity of virophages, an unusual group of viruses families [19]. that parasitize on giant viruses of the family Mimiviridae. The genomes of Mavirus [12] and the related Ace The known virophages possess double-stranded, typically Lake Mavirus (ALM) virophage [15] contain two genes circular DNA genomes of about 20 kilobase pairs (kbp) and that are missing in other virophages, namely a protein- icosahedral virions comprised of highly derived double primed family B DNA polymerase (pPolB) and an integrase, jelly-roll capsid proteins [9,10]. So far 3 virophages have both of which are most closely related to the respective homologous genes of a vast family of large eukaryotic self-synthesizing DNA transposons known as Polintons * Correspondence: [email protected] (Mavericks) [20,21]. The sharing of these two genes be- National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA tween Mavirus and Polintons along with the conservation © 2015 Yutin et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Yutin et al. Biology Direct (2015) 10:19 Page 2 of 9 of genes encoding predicted protease and ATPase in all for phylogenetic tree construction. In the resulting tree, Polintons suggested an evolutionary relationship between the putative virophage proteins from the sludge and bio- these two classes of selfish genetic elements [12,19]. Fur- reactor metagenomes clustered within the Sputnik-like ther analysis of the Polinton genomes buttressed this hy- virophage family whereas those from the marine meta- pothesis by showing that most of these transposons genome fell within the OLV-like family (Figure 1). In actually encode homologs of the major and minor capsid contrast, the putative virophage MCPs from the gut proteins of icosahedral viruses [22]. Thus, Polintons are metagenome (more specifically, all these sequences ori- most likely capable of forming virions and lead a dual life- ginate from the sheep rumen, so hereinafter we refer to style that combines features of transposons and viruses. this sequence collection as the rumen metagenome) These findings have prompted a broad-scale evolutionary formed a distinct, strongly supported group (Figure 1). scenario according to which the Polintons (Polintoviruses) We further examined the metagenomic sequence contigs were the ancestors of the virophages and several other that encompassed the putative virophage MCP genes groups of dsDNA viruses, including the large and giant (see Additional file 1). The contigs from the sludge, mar- viruses of the proposed order “Megavirales”, and dsDNA ine and bioreactor metagenomes were short and, with a plasmids of eukaryotes [23]. Under this scenario, the single exception, did not contain additional genes. In Polintons comprise a pool of diverse genetic elements, contrast, the rumen metagenome contigs were longer, up and various other eukaryotic parasitic elements, in par- to 26,209 basepairs. The ORFs present in these contigs ticular adenoviruses, virophages, and fungal cytoplasmic were translated and searched against the non-redundant plasmids, evolved from different groups of polintons [23]. protein sequence database at the NCBI, resulting in the We sought to harness the potential of metagenomics identification of a typical virophage morphogenetic module for the discovery of substantially novel virophages, dis- (Figure 1). tinct from the Sputnik, Mavirus and OLV families. All Phylogenetic analysis of the putative virophage sequenced virophage genomes encompass a conserved ATPases and proteases supported the monophyly of the gene module that encodes proteins involved in virion “rumen” group and its association with other virophages morphognesis, namely major and minor capsid proteins, (see Additional file 2). The three longest contigs from packaging ATPase and capsid maturation protease, but the rumen metagenome encoded an additional putative otherwise, possess highly variably gene repertoires [19]. protein that in database searches showed the highest simi- Among the four conserved proteins of the virophages, larity to pPolBs from diverse Polintons. Phylogenetic ana- the protease and the ATPase share significant sequence lysis of these putative pPolBs confidently placed them into similarity with homologs from diverse viruses whereas the clade known as Polinton family 2, without any indica- the sequence of the minor capsid protein is poorly con- tion of clustering with the Mavirus pPolB (Figure 2). Thus, served even among the virophages. Thus, the best probe the results of phylogenetic analysis reported here are com- for discovery of putative new virophages is the major patible with the previously described evolutionary trend capsid protein (MCP) which adopts a derived double whereby different groups of eukaryotic selfish elements jelly-roll fold [10] and is well-conserved in the viro- evolved from within the diversity of the Polintons [23]. phages but shows no significant similarity to any non- The remaining ORFs in the putative rumen virophage virophage proteins [19]. (RVP) genomes encoded proteins without significant We used four MCP sequences from diverse virophages similarities in the current databases, with the sole excep- to search the metagenomic nucleotide databases that tion of a putative polynucleotide kinase encoded in one are available via GenBank and detected multiple hits of the contigs (see Additional file 1). (E-value < 10). The respective metagenomic sequences We attempted to extend the assembly of the rumen were translated and used as queries for BLASTP to search metagenome contigs to further characterize the putative the non-redundant protein sequence database, in order to novel virophages. Identification of several overlapping further ascertain their provenance. As a result of this contigs and terminal inverted repeats (TIRs) allowed us to search, 35 Open Reading Frames (ORFs) and ORF frag- assemble 3 long virophage genomes (see Additional file 3). ments from 6 metagenomics databases, namely, Activated Two of these assemblies
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