Nucleocytoplasmic Large DNA Viruses Research Articles

ViralRecall-A Flexible Command-Line Tool for the Detection of Giant Virus Signatures in 'Omic Data.

Giant viruses are widespread in the biosphere and play important roles in biogeochemical cycling and host genome evolution. Also known as nucleo-cytoplasmic large DNA viruses (NCLDVs), these eukaryotic viruses harbor the largest and most complex viral genomes known. Studies have shown that NCLDVs are frequently abundant in metagenomic datasets, and that sequences derived from these viruses can also be found endogenized in diverse eukaryotic genomes. The accurate detection of sequences derived from NCLDVs is therefore of great importance, but this task is challenging owing to both the high level of sequence divergence between NCLDV families and the extraordinarily high diversity of genes encoded in their genomes, including some encoding for metabolic or translation-related functions that are typically found only in cellular lineages. Here, we present ViralRecall, a bioinformatic tool for the identification of NCLDV signatures in ‘omic data. This tool leverages a library of giant virus orthologous groups (GVOGs) to identify sequences that bear signatures of NCLDVs. We demonstrate that this tool can effectively identify NCLDV sequences with high sensitivity and specificity. Moreover, we show that it can be useful both for removing contaminating sequences in metagenome-assembled viral genomes as well as the identification of eukaryotic genomic loci that derived from NCLDV. ViralRecall is written in Python 3.5 and is freely available on GitHub: https://github.com/faylward/viralrecall.

Reassessing the mechanism of genome packaging in plant viruses with lessons from ATPase fold

Plant viruses cause various disease in crops and are responsible for huge economic losses. Understanding their mode of infection and spread is crucial for developing control strategies. Genome packaging is an important step in the process of viral maturation. Three systems of viral genome packaging are known till date. The type I packaging system, found in most of the small plant viruses, involves co-condensation of nucleic acid with viral capsid proteins (CPs) leading to the assembly of virion particles without utilizing ATP. The type II and III packaging systems, present in phages and nucleo-cytoplasmic large DNA viruses, exhibit genome translocation inside the prohead by utilizing ATP. Discovery of the ATPase fold in the CPs of many small plant viruses and the requirement of other ATPases during genome encapsidation have changed the perception about genome packaging in the type I system. Based on recent studies, it seems that the genome packaging mechanisms of plant viruses such as potexvirus have nothing in common with those of other well-characterized passive, energy-independent type I systems. Moreover, these studies have suggested that in these plant viruses, the genome encapsidation process is more intricately coupled with energy utilization than in other systems. In this comprehensive review, we present a novel, expanded sub-classification system for the type I system on the basis of ATP employed.

Investigation of starry sturgeon Acipencer stellatus in the Black Sea and Sea of Azov for AcIV-E infection

Specific sturgeon nucleocytoplasmic large DNA viruses (sNCLDV) infect several species of the Acipenseridae family. sNCLDV have previously been referred to as unclassified members of the family Iridoviridae. They have recently been moved from Iridoviridae to Mimiviridae family. One of these viruses, Acipenser iridovirus-European (AcIV-E), is present in farms across Europe where it has occasionally caused mild to severe losses in sturgeons. In this study, we provide data on AcIV-E search in a susceptible species such as starry sturgeon (Acipencer stellatus) from the Black sea and Sea of Azov. In 2020, starry sturgeons were sampled in Odessa region of the Black Sea and Zaporizhzhia region of the Sea of Azov. None of the sampled fish demonstrated pathological signs of disease and were healthy upon visual observation all individuals. Total DNA was extracted and submitted to a generic PCR targeting different fragments of major capsid protein (MCP) gene of AcIV-E. No virus-specific products were obtained in any starry sturgeon sample from both seas, while the expected products of MCP gene fragments as well as the fragments of beta-actin gene in control reactions were successfully amplified using fish and viral DNA of AcIV-E isolated from Siberian sturgeon in 2018–2019. Although AcIV-E is difficult to identify in asymptomatic wild fish, but it probably can play a role in starry sturgeon pathology across the Black Sea basin. A high risk of virus spread to wild populations is possible since this virus was identified in sturgeon farms upstream the Dnipro river. Therefore, AcIV-E, even in the presence of other pathogens, should be studied in sturgeon hatcheries as well as in possible vectors of disease, but the huge area of inspection could be a challenge.

A novel function of African Swine Fever Virus pE66L in inhibition of host translation by the PKR/eIF2α pathway.

African swine fever virus (ASFV) is one of the most contagious and lethal viruses infecting pigs. This virus is endemic in many countries and has very recently spread to China, but no licensed vaccines or treatments are currently available. Despite extensive research, the basic question of how ASFV-encoded proteins inhibit host translation remains. Here, we examined how ASFV interfered with host translation and optimized viral gene expression. We found that 14 ASFV proteins inhibited Renilla luciferase (Rluc) activity greater than 5-fold, and the protein with the strongest inhibitory effect was pE66L, which was not previously reported. Combined with bioinformatical analysis and biochemical experiment, we determined that the transmembrane (TM) domain (amino acids 13-34) of pE66L was required for the inhibition of host gene expression. Notably, we constructed a recombinant plasmid with the TM domain linked to enhanced green fluorescent protein (EGFP) and further demonstrated that this domain broadly inhibited protein synthesis. Confocal and biochemical analyses indicated that the TM domain might help proteins locate to the endoplasmic reticulum (ER) to suppress translation though the PKR/eIF2α pathway. Deletion of the E66L gene had little effect on virus replication in macrophages, but significantly recovered host gene expression. Taken together, our findings complement studies on the host translation of ASFV proteins and suggest that ASFV pE66L induces host translation shutoff, which is dependent on activation of the PKR/eIF2α pathway.Importance African swine fever virus (ASFV) is a member of the nucleocytoplasmic large DNA virus superfamily that predominantly replicates in the cytoplasm of infected cells. The ASFV double-stranded DNA genome varies in length from approximately 170 to 193 kbp depending on the isolate and contains between 150 and 167 open reading frames (ORFs), of which half the encoded proteins have not been explored. Our study showed that 14 proteins had an obvious inhibitory effect on Renilla luciferase (Rluc) gene synthesis, with pE66L showing the most significant effect. Furthermore, the transmembrane (TM) domain of pE66L broadly inhibited host protein synthesis in a PKR/eIF2a pathway-dependent manner. Loss of pE66L during ASFV infection had little effect on virus replication, but significantly recovered host protein synthetic. Based on the above results, our findings expand our view of ASFV in determining the fate of host-pathogen interactions.

Structure-Based Deep Mining Reveals First-Time Annotations for 46 Percent of the Dark Annotation Space of the 9,671-Member Superproteome of the Nucleocytoplasmic Large DNA Viruses.

We conducted an exhaustive search for three-dimensional structural homologs to the proteins of 20 key phylogenetically distinct nucleocytoplasmic DNA viruses (NCLDV). Structural matches covered 429 known protein domain superfamilies, with the most highly represented being ankyrin repeat, P-loop NTPase, F-box, protein kinase, and membrane occupation and recognition nexus (MORN) repeat. Domain superfamily diversity correlated with genome size, but a diversity of around 200 superfamilies appeared to correlate with an abrupt switch to paralogization. Extensive structural homology was found across the range of eukaryotic RNA polymerase II subunits and their associated basal transcription factors, with the coordinated gain and loss of clusters of subunits on a virus-by-virus basis. The total number of predicted endonucleases across the 20 NCLDV was nearly quadrupled from 36 to 132, covering much of the structural and functional diversity of endonucleases throughout the biosphere in DNA restriction, repair, and homing. Unexpected findings included capsid protein-transcription factor chimeras; endonuclease chimeras; enzymes for detoxification; antimicrobial peptides and toxin-antitoxin systems associated with symbiosis, immunity, and addiction; and novel proteins for membrane abscission and protein turnover.IMPORTANCE We extended the known annotation space for the NCLDV by 46%, revealing high-probability structural matches for fully 45% of the 9,671 query proteins and confirming up to 98% of existing annotations per virus. The most prevalent protein families included ankyrin repeat- and MORN repeat-containing proteins, many of which included an F-box, suggesting extensive host cell modulation among the NCLDV. Regression suggested a minimum requirement for around 36 protein structural superfamilies for a viable NCLDV, and beyond around 200 superfamilies, genome expansion by the acquisition of new functions was abruptly replaced by paralogization. We found homologs to herpesvirus surface glycoprotein gB in cytoplasmic viruses. This study provided the first prediction of an endonuclease in 10 of the 20 viruses examined; the first report in a virus of a phenolic acid decarboxylase, proteasomal subunit, or cysteine knot (defensin) protein; and the first report of a prokaryotic-type ribosomal protein in a eukaryotic virus.

Widespread endogenization of giant viruses shapes genomes of green algae.

Endogenous viral elements (EVEs)-viruses that have integrated their genomes into those of their hosts-are prevalent in eukaryotes and have an important role in genome evolution1,2. The vast majority of EVEs that have been identified to date are small genomic regions comprising a few genes2, but recent evidence suggests that some large double-stranded DNA viruses may also endogenize into the genome of the host1. Nucleocytoplasmic large DNA viruses (NCLDVs) have recently become of great interest owing to their large genomes and complex evolutionary origins3-6, but it is not yet known whether they are a prominent component of eukaryotic EVEs. Here we report the widespread endogenization of NCLDVs in diverse green algae; these giant EVEs reached sizes greater than 1 million base pairs and contained as many as around 10% of the total open reading frames in some genomes, substantially increasing the scale of known viral genes in eukaryotic genomes. These endogenized elements often shared genes with host genomic loci and contained numerous spliceosomal introns and large duplications, suggesting tight assimilation into host genomes. NCLDVs contain large and mosaic genomes with genes derived from multiple sources, and their endogenization represents an underappreciated conduit of new genetic material into eukaryotic lineages that can substantially impact genome composition.

Zooming on dynamics of marine microbial communities in the phycosphere of Akashiwo sanguinea (Dinophyta) blooms.

Characterizing ecological relationships between viruses, bacteria and phytoplankton in the ocean is critical to understanding the ecosystem; however, these relationships are infrequently investigated together. To understand the dynamics of microbial communities and environmental factors in harmful algal blooms (HABs), we examined the environmental factors and microbial communities during Akashiwo sanguinea HABs in the Jangmok coastal waters of South Korea by metagenomics. Specific bacterial species showed complex synergistic and antagonistic relationships with the A. sanguinea bloom. The endoparasitic dinoflagellate Amoebophrya sp. 1 controlled the bloom dynamics and correlated with HAB decline. Among nucleocytoplasmic large DNA viruses (NCLDVs), two Pandoraviruses and six Phycodnaviruses were strongly and positively correlated with the HABs. Operational taxonomic units of microbial communities and environmental factors associated with A. sanguinea were visualized by network analysis: A. sanguinea–Amoebophrya sp. 1 (r = .59, time lag: 2 days) and A. sanguinea–Ectocarpus siliculosus virus 1 in Phycodnaviridae (0.50, 4 days) relationships showed close associations. The relationship between A. sanguinea and dissolved inorganic phosphorus relationship also showed a very close correlation (0.74, 0 day). Microbial communities and the environment changed dynamically during the A. sanguinea bloom, and the rapid turnover of microorganisms responded to ecological interactions. A. sanguinea bloom dramatically changes the environments by exuding dissolved carbohydrates via autotrophic processes, followed by changes in microbial communities involving host‐specific viruses, bacteria and parasitoids. Thus, the microbial communities in HAB are composed of various organisms that interact in a complex manner.

Viral rhodopsins 1 are\xa0an unique family of light-gated cation channels

Phytoplankton is the base of the marine food chain as well as oxygen and carbon cycles and thus plays a global role in climate and ecology. Nucleocytoplasmic Large DNA Viruses that infect phytoplankton organisms and regulate the phytoplankton dynamics encompass genes of rhodopsins of two distinct families. Here, we present a functional and structural characterization of two proteins of viral rhodopsin group 1, OLPVR1 and VirChR1. Functional analysis of VirChR1 shows that it is a highly selective, Na+/K+-conducting channel and, in contrast to known cation channelrhodopsins, it is impermeable to Ca2+ ions. We show that, upon illumination, VirChR1 is able to drive neural firing. The 1.4 Å resolution structure of OLPVR1 reveals remarkable differences from the known channelrhodopsins and a unique ion-conducting pathway. Thus, viral rhodopsins 1 represent a unique, large group of light-gated channels (viral channelrhodopsins, VirChR1s). In nature, VirChR1s likely mediate phototaxis of algae enhancing the host anabolic processes to support virus reproduction, and therefore, might play a major role in global phytoplankton dynamics. Moreover, VirChR1s have unique potential for optogenetics as they lack possibly noxious Ca2+ permeability.

The Role of Tape Measure Protein in Nucleocytoplasmic Large DNA Virus Capsid Assembly.

Nucleocytoplasmic large DNA viruses (NCLDVs) are a group of large viruses that infect a wide range of hosts, from animals to protists. These viruses are grouped together in NCLDV based on genomic sequence analyses. They share a set of essential genes for virion morphogenesis and replication. Most NCLDVs generally have large physical sizes while their morphologies vary in different families, such as icosahedral, brick, or oval shape, raising the question of the possible regulatory factor on their morphogenesis. The capsids of icosahedral NCLDVs are assembled from small building blocks, named capsomers, which are the trimeric form of the major capsid proteins. Note that the capsids of immature poxvirus are spherical even though they are assembled from capsomers that share high structural conservation with those icosahedral NCLDVs. The recently published high resolution structure of NCLDVs, Paramecium bursaria Chlorella virus 1 and African swine fever virus, described the intensive network of minor capsid proteins that are located underneath the capsomers. Among these minor proteins is the elongated tape measure protein (TmP) that spans from one icosahedral fivefold vertex to another. In this study, we focused on the critical roles that TmP plays in the assembly of icosahedral NCLDV capsids, answering a question raised in a previously proposed spiral mechanism. Interestingly, basic local alignment search on the TmPs showed no significant hits in poxviruses, which might be the factor that differentiates poxviruses and icosahedral NCLDVs in their morphogenesis.

Coral Bleaching Phenotypes Associated With Differential Abundances of Nucleocytoplasmic Large DNA Viruses

Eukaryotic viruses and bacteriophage have been implicated in disease and bleaching in corals, but the compositional and functional diversity of these viruses in healthy and compromised hosts remains underexplored. To investigate whether viral assemblages differ in concert with coral bleaching, we collected bleached and non-bleached conspecific pairs of corals during a minor bleaching event in 2016 from reefs on the island of Mo’orea, French Polynesia. Using electron microscopy (EM), we identified several viral particle types, all reminiscent of medium to large-sized nucleocytoplasmic large DNA viruses (NCLDV). We also found that viral metagenomes from bleached corals have significantly more eukaryotic virus sequences, whereas bacteriophage sequences are significantly more abundant in viral metagenomes from non-bleached colonies. In this study, we also initiated the assembly of the first eukaryotic dsDNA coral virus genome. Based on our EM imagery and our taxonomic annotations of viral metagenome sequences, we hypothesize that this genome represents a novel, phylogenetically distinct member of the NCLDVs, with its closest sequenced relative being a distant marine flagellate-associated virus. We also showed that this NCLDV is abundant in bleached corals, but it is also present in apparently healthy corals, suggesting it plays a role in the onset and/or severity of coral bleaching.

Viral ecogenomics across the Porifera

BackgroundViruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea.ResultsViromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts.ConclusionsOur results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts.3fNQJtcyRuwttbnAh9LNMAVideo

Biogeography of marine giant viruses reveals their interplay with eukaryotes and ecological functions.

Nucleocytoplasmic large DNA viruses (NCLDVs) are ubiquitous in marine environments and infect diverse eukaryotes. However, little is known about their biogeography and ecology in the ocean. By leveraging the Tara Oceans pole-to-pole metagenomic data set, we investigated the distribution of NCLDVs across size fractions, depths and biomes, as well as their associations with eukaryotic communities. Our analyses reveal a heterogeneous distribution of NCLDVs across oceans, and a higher proportion of unique NCLDVs in the polar biomes. The community structures of NCLDV families correlate with specific eukaryotic lineages, including many photosynthetic groups. NCLDV communities are generally distinct between surface and mesopelagic zones, but at some locations they exhibit a high similarity between the two depths. This vertical similarity correlates to surface phytoplankton biomass but not to physical mixing processes, which suggests a potential role of vertical transport in structuring mesopelagic NCLDV communities. These results underscore the importance of the interactions between NCLDVs and eukaryotes in biogeochemical processes in the ocean.

First genetic characterization of sturgeon mimiviruses in Ukraine.

A group of pathogenic nucleocytoplasmic large DNA viruses (NCLDVs) related to the Mimiviridae family infect farmed sturgeons across Europe, causing mild-to-severe losses. One of these viruses, Acipenser iridovirus-European (AcIV-E), was identified in six sturgeon species. During the 2018-2019 period, nine sick Siberian (A.baerii) and Russian (A.gueldenstaedtii) sturgeons were sampled in Ukrainian farms and tested for the presence of AcIV-E using real-time PCR. The presence of AcIV-E was confirmed in some samples. High-resolution melting (HRM) assay and Sanger sequencing demonstrated the presence in three farms of two alleles of the major capsid protein (MCP) gene, called var1 and var2. Five samples carried both var1 and var2 at varying ratios, and the sixth sample was infected with only var1. These results constitute the first detection of AcIV-E in Ukraine and the first detection of a sample carrying only var1. The full-length sequences of the MCP genes confirmed the existence of two genetic lineages of AcIV-E, tentatively named V1 and V2, each displaying multiple substitutions in the MCP gene. Some of the MCP sequences showed a genetic relationship to both V1 and V2 lineages, depending on the fragment examined. Most likely, these sequences resulted from recombination events.

Transcriptome view of a killer: African swine fever virus.

African swine fever virus (ASFV) represents a severe threat to global agriculture with the world's domestic pig population reduced by a quarter following recent outbreaks in Europe and Asia. Like other nucleocytoplasmic large DNA viruses, ASFV encodes a transcription apparatus including a eukaryote-like RNA polymerase along with a combination of virus-specific, and host-related transcription factors homologous to the TATA-binding protein (TBP) and TFIIB. Despite its high impact, the molecular basis and temporal regulation of ASFV transcription is not well understood. Our lab recently applied deep sequencing approaches to characterise the viral transcriptome and gene expression during early and late ASFV infection. We have characterised the viral promoter elements and termination signatures, by mapping the RNA-5′ and RNA-3′ termini at single nucleotide resolution. In this review, we discuss the emerging field of ASFV transcripts, transcription, and transcriptomics.

Evolution of a major virion protein of the giant pandoraviruses from an inactivated bacterial glycoside hydrolase.

The diverse viruses in the phylum Nucleocytoviricota (also known as NLCDVs, Nucleo-cytoplasmic Large DNA Viruses) typically possess large icosahedral virions. However, in several families of Nucleocytoviricota, the icosahedral capsid was replaced by irregular particle shapes, most notably, the amphora-like virions of pandoraviruses and pithoviruses, the largest known virus particles in the entire virosphere. Pandoraviruses appear to be the most highly derived viruses in this phylum because their evolution involved not only the change in the virion shape, but also, the actual loss of the gene encoding double-jelly roll major capsid protein (DJR MCP), the main building block of icosahedral capsids in this virus assemblage. Instead, pandoravirus virions are built of unrelated abundant proteins. Here we show that the second most abundant virion protein of pandoraviruses, major virion protein 2 (MVP2), evolved from an inactivated derivative of a bacterial glycoside hydrolase of the GH16 family. The ancestral form of MVP2 was apparently acquired early in the evolution of the Nucleocytoviricota, to become a minor virion protein. After a duplication in the common ancestor of pandoraviruses and molliviruses, one of the paralogs displaces DJR MCP in pandoraviruses, conceivably, opening the way for a major increase in the size of the virion and the genome. Exaptation of a carbohydrate-binding protein for the function of the MVP is a general trend in virus evolution and might underlie the transformation of the virion shape in other groups of the Nucleocytoviricota as well.

Advantages and Limits of Metagenomic Assembly and Binning of a Giant Virus.

Giant viruses have large genomes, often within the size range of cellular organisms. This distinguishes them from most other viruses and demands additional effort for the successful recovery of their genomes from environmental sequence data. Here, we tested the performance of genome-resolved metagenomics on a recently isolated giant virus, Fadolivirus, by spiking it into an environmental sample from which two other giant viruses were isolated. At high spike-in levels, metagenome assembly and binning led to the successful genomic recovery of Fadolivirus from the sample. A complementary survey of the major capsid protein indicated the presence of other giant viruses in the sample matrix but did not detect the two isolated from this sample. Our results indicate that genome-resolved metagenomics is a valid approach for the recovery of near-complete giant virus genomes given that sufficient clonal particles are present. However, our data also underline that a vast majority of giant viruses remain currently undetected, even in an era of terabase-scale metagenomics.IMPORTANCE The discovery of large and giant nucleocytoplasmic large DNA viruses (NCLDV) with genomes in the megabase range and equipped with a wide variety of features typically associated with cellular organisms was one of the most unexpected, intriguing, and spectacular breakthroughs in virology. Recent studies suggest that these viruses are highly abundant in the oceans, freshwater, and soil, impact the biology and ecology of their eukaryotic hosts, and ultimately affect global nutrient cycles. Genome-resolved metagenomics is becoming an increasingly popular tool to assess the diversity and coding potential of giant viruses, but this approach is currently lacking validation.

The structural basis of African swine fever virus pA104R binding to DNA and its inhibition by stilbene derivatives

African swine fever virus (ASFV) is a highly contagious nucleocytoplasmic large DNA virus (NCLDV) that causes nearly 100% mortality in swine. The development of effective vaccines and drugs against this virus is urgently needed. pA104R, an ASFV-derived histone-like protein, shares sequence and functional similarity with bacterial HU/IHF family members and is essential for viral replication. Herein, we solved the crystal structures of pA104R in its apo state as well as in complex with DNA. Apo-pA104R forms a homodimer and folds into an architecture conserved in bacterial heat-unstable nucleoid proteins/integration host factors (HUs/IHFs). The pA104R-DNA complex structure, however, uncovers that pA104R has a DNA binding pattern distinct from its bacterial homologs, that is, the β-ribbon arms of pA104R stabilize DNA binding by contacting the major groove instead of the minor groove. Mutations of the basic residues at the base region of the β-strand DNA binding region (BDR), rather than those in the β-ribbon arms, completely abolished DNA binding, highlighting the major role of the BDR base in DNA binding. An overall DNA bending angle of 93.8° is observed in crystal packing of the pA104R-DNA complex structure, which is close to the DNA bending angle in the HU-DNA complex. Stilbene derivatives SD1 and SD4 were shown to disrupt the binding between pA104R and DNA and inhibit the replication of ASFV in primary porcine alveolar macrophages. Collectively, these results reveal the structural basis of pA104R binding to DNA highlighting the importance of the pA104R-DNA interaction in the ASFV replication cycle and provide inhibitor leads for ASFV chemotherapy.

Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses

The discovery of eukaryotic giant viruses has transformed our understanding of the limits of viral complexity, but the extent of their encoded metabolic diversity remains unclear. Here we generate 501 metagenome-assembled genomes of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) from environments around the globe, and analyze their encoded functional capacity. We report a remarkable diversity of metabolic genes in widespread giant viruses, including many involved in nutrient uptake, light harvesting, and nitrogen metabolism. Surprisingly, numerous NCLDV encode the components of glycolysis and the TCA cycle, suggesting that they can re-program fundamental aspects of their host’s central carbon metabolism. Our phylogenetic analysis of NCLDV metabolic genes and their cellular homologs reveals distinct clustering of viral sequences into divergent clades, indicating that these genes are virus-specific and were acquired in the distant past. Overall our findings reveal that giant viruses encode complex metabolic capabilities with evolutionary histories largely independent of cellular life, strongly implicating them as important drivers of global biogeochemical cycles.

The "Neglected Viruses" of Taihu: Abundant Transcripts for Viruses Infecting Eukaryotes and Their Potential Role in Phytoplankton Succession.

Drivers of algal bloom dynamics remain poorly understood, but viruses have been implicated as important players. Research addressing bloom dynamics has generally been restricted to the virus-infection of the numerically dominant (i.e. bloom forming) taxa. Yet this approach neglects a broad diversity of viral groups, limiting our knowledge of viral interactions and constraints within these systems. We examined hallmark virus marker genes in metatranscriptomic libraries from a seasonal and spatial survey of a Microcystis aeruginosa bloom in Lake Tai (Taihu) China to identify active infections by nucleocytoplasmic large DNA viruses (NCLDVs), RNA viruses, ssDNA viruses, bacteriophage, and virophage. Phylogenetic analyses revealed a diverse virus population with seasonal and spatial variability. We observed disproportionately high expression of markers associated with NCLDVs and ssRNA viruses (consistent with viruses that infect photosynthetic protists) relative to bacteriophage infecting heterotrophic bacteria or cyanobacteria during the height of the Microcystis bloom event. Under a modified kill-the-winner scheme, we hypothesize viruses infecting protists help suppress the photosynthetic eukaryotic community and allow for the proliferation of cyanobacteria such as Microcystis. Our observations provide a foundation for a little considered factor promoting algal blooms.

Learning the diversity of giant viruses.

Researchers identify a broad phylogenetic diversity of nucleocytoplasmic large DNA viruses by mining global-scale metagenomics datasets.