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Giant Viruses—Big Surprises

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Giant Viruses—Big Surprises viruses Review Giant Viruses—Big Surprises Nadav Brandes 1 and Michal Linial 2,* 1 The Rachel and Selim Benin School of Computer Science and Engineering, The Hebrew University of Jerusalem, Jerusalem 91904, Israel; [email protected] 2 Department of Biological Chemistry, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel * Correspondence: [email protected]; Tel.: +972-02-6585425 Received: 22 March 2019; Accepted: 23 April 2019; Published: 30 April 2019 Abstract: Viruses are the most prevalent infectious agents, populating almost every ecosystem on earth. Most viruses carry only a handful of genes supporting their replication and the production of capsids. It came as a great surprise in 2003 when the first giant virus was discovered and found to have a >1 Mbp genome encoding almost a thousand proteins. Following this first discovery, dozens of giant virus strains across several viral families have been reported. Here, we provide an updated quantitative and qualitative view on giant viruses and elaborate on their shared and variable features. We review the complexity of giant viral proteomes, which include functions traditionally associated only with cellular organisms. These unprecedented functions include components of the translation machinery, DNA maintenance, and metabolic enzymes. We discuss the possible underlying evolutionary processes and mechanisms that might have shaped the diversity of giant viruses and their genomes, highlighting their remarkable capacity to hijack genes and genomic sequences from their hosts and environments. This leads us to examine prominent theories regarding the origin of giant viruses. Finally, we present the emerging ecological view of giant viruses, found across widespread habitats and ecological systems, with respect to the environment and human health. Keywords: Amebae viruses; viral evolution; protein domains; mimivirus; dsdna viruses; translation machinery; pandoravirus; NCLDV 1. Giant Viruses and the Viral World Viruses are cell infecting agents present in almost every ecosystem. Questions the regarding viral origin and early evolution alongside all living organisms (bacteria, archaea and eukarya) are still wide open, and relevant theories remain speculative [1–5]. As viruses are exceptionally diverse and undergo rapid changes, it is impossible to construct an ancestral lineage tree for the viral world [6–10]. Instead, virus families are categorized according to the nature of their genetic material, mode of replication, pathogenicity, and structural properties [11]. At present, the viral world is represented by over 8,000 reference genomes [12]. The International Committee on Taxonomy of Viruses (ICTV) provides a universal virus taxonomical classification proposal that covers ~150 families and ~850 genera, with many viruses yet unclassified [13]. This collection provides a comprehensive, compact set of virus representatives. Inspection of viral genomes reveals that most known viruses have genomes encoding only a few proteins. Actually, 69% of all known viruses have less than 10 proteins encoded in their genomes (Figure1). It is a common assumption that viruses demonstrate near-optimal genome packing and information compression, presumably in order to maximize their replication rate, number of progenies, and other parameters that increase infectivity [14,15]. However, a debate is still ongoing over the generality of these phenomena [16], and there is a non-negligible percentage of larger viruses (Figure1). Viruses 2019, 11, 404; doi:10.3390/v11050404 www.mdpi.com/journal/viruses Viruses 2019, 11, 404 2 of 12 Viruses 2019, 11, x FOR PEER REVIEW 2 of 12 On the far end of the distribution, there are viruses with hundreds of genes, most of them are considered aregiant considered viruses. While giant only viruses. 0.3% While of the knownonly 0.3% viral of proteomes the known contain viral 500proteomes or more proteins,contain 500 they or encode more proteins,as much asthey 7.5% encode of the as total much number as 7.5% of of viral the proteinstotal number (Figure of1 viralB). proteins (Figure 1B). Figure 1. Number of proteins encoded by viruses. (A) The number of encoded proteins (y-axis) in all Figure 1. Number of proteins encoded by viruses. (A) The number of encoded proteins (y-axis) in all 7,959 viral representatives, ranked in descending order. (B) Partitioning of the 7959 viral proteomes 7,959 viral representatives, ranked in descending order. (B) Partitioning of the 7959 viral proteomes by the number of encoded proteins. The 0.3% viral proteomes with the highest number of proteins by the number of encoded proteins. The 0.3% viral proteomes with the highest number of proteins (over 500) encode 7.5% of the total number of viral proteins. (over 500) encode 7.5% of the total number of viral proteins. 2. The Discovery of Giant Viruses 2. The Discovery of Giant Viruses The first giant virus, Acanthamoeba polyphaga mimivirus (APMV), was discovered in 2003 [17]. Its sizeThe was first unprecedented, giant virus, Acanthamoeba being on thepolyphaga scale ofmimivirus small bacteria (APMV), or was archaea discovered cells [18 in]. 2003 Unlike [17]. any Its sizepreviously was unprecedented, identified virus, being APMV on couldthe scale be seenof small with bacteria a lightmicroscope or archaea [19cells,20 ].[18]. Initially Unlike it wasany previouslymistaken for identified a bacterium virus, and APMV recognized could asbe a seen virus with only a ten light years microscope after its isolation [19,20]. [Initially21]. Up it to was this mistakenday, most for of itsa bacterium proteins remain and recognized uncharacterized as a virus [22 ,only23]. Notably,ten years even after more its isolation than a decade[21]. Up after to this the day,discovery most of APMV,its proteins the identification remain uncharacterized of giant viruses [22,23]. still Notably, sometimes even involves more confusion,than a decade as illustrated after the discoveryin the discovery of APMV, of the Pandoravirusthe identification inopinatum of giant[24], viruses which was still initially sometimes described involves as an confusion, endoparasitic as illustratedorganism, andin thePithovirus discovery sibericum of the Pandoravirus[25], which was inopinatum also misinterpreted [24], which aswas an initially archaeal described endosymbiont as an endoparasitic(see discussion organism, in References and [Pithovirus21,26]). sibericum [25], which was also misinterpreted as an archaeal endosymbiontIn the following (see discussion years after in References the initial discovery [21,26]). of APMV, many additional giant viral species haveIn been the identifiedfollowing and years their after genomes the initial fully discovery sequenced. of MostAPMV, giant many viral additional genomes havegiant been viral obtained species havefrom large-scalebeen identified metagenomic and their sequencing genomes projectsfully sequenced. covering aquaticMost giant ecosystems viral genomes (e.g., oceans, have pools,been obtainedlakes and from cooling large-scale wastewater metagenomic units) [27, 28sequencing]; others have projects been covering sequenced aquatic from samplesecosystems extracted (e.g., oceans,from underexplored pools, lakes and geographical cooling wastewater and ecological units) [27,28]; niches others (e.g., thehave Amazon been sequenced River, deep from seassamples and extractedforest soils) from [29 –underexplored32]. Despite the geographical accumulation and of ecological many more niches giant (e.g., virus the representatives, Amazon River, the deep fraction seas andof uncharacterized forest soils) [29–32]. proteins Despite in their the proteomesaccumulation remains of many exceptionally more giant highvirus [ 33representatives,]. Many of these the fractionuncharacterized of uncharacterized proteins were proteins also considered in their proteomes orphan genes remains (ORFans), exceptionally i.e., no significanthigh [33]. matchMany of to theseany other uncharacterized sequence was proteins identified. were also For considered example, 93% orphan of the genesPandoravirus (ORFans), salinus i.e. no proteins,significant the match first torepresentative any other sequence of this family was identified. [34] were For reported example, as ORFans. 93% of the Pandoravirus salinus proteins, the first representative of this family [34] were reported as ORFans. At present, there are over a hundred giant virus isolates, which reveal fascinating and unexpected characteristics. These extreme instances on the viral landscape challenge the current Viruses 2019, 11, 404 3 of 12 At present, there are over a hundred giant virus isolates, which reveal fascinating and unexpected Viruses 2019, 11, x FOR PEER REVIEW 3 of 12 characteristics. These extreme instances on the viral landscape challenge the current theories on genome size and compactness in viruses, and provide a new perspective on the very concept of a virus theories on genome size and compactness in viruses, and provide a new perspective on the very and viral origin [4,20,28,35–37]. concept of a virus and viral origin [4,20,28,35–37]. 3. Definition of Giant Viruses 3. Definition of Giant Viruses Attempts to distinguish giant viruses from other large viruses remain somewhat fuzzy [38,39]. Attempts to distinguish giant viruses from other large viruses remain somewhat fuzzy [38,39]. Any definition for giant viruses would necessarily involve some arbitrary threshold, as virus size, Any definition for giant viruses would necessarily
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