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All sourcesNASA NTRSDOE OSTI
DOE OSTI2020

Evaluation in Swine of a Recombinant African Swine Fever Virus Lacking the MGF-360-1L Gene

The African swine fever (ASF) pandemic is currently affecting pigs throughout Eurasia, resulting in significant swine production losses. The causative agent, ASF virus (ASFV), is a large, structurally complex virus with a genome encoding more than 160 genes. The function of most of those genes remains unknown. Here, we presented the previously uncharacterized ASFV gene MGF360-1L, the first gene in the genome. The kinetic studies of virus RNA transcription demonstrated that the MGF360-1L gene was transcribed as a late virus protein. The essentiality of MGF360-1L to virus replication was evaluated by developing a recombinant ASFV lacking the gene (ASFV-G-ΔMGF360-1L). In primary swine macrophage cell cultures, ASFV-G-ΔMGF360-1L showed similar replication kinetics as the parental highly virulent field isolate Georgia2007 (ASFV-G). Domestic pigs experimentally infected with ASFV-G-ΔMGF360-1L presented with a clinical disease indistinguishable from that caused by ASFV-G, demonstrating that MGF360-1L was not involved in virulence in swine, the natural host of ASFV.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

The International Virus Bioinformatics Meeting 2020

The International Virus Bioinformatics Meeting 2020 was originally planned to take place in Bern, Switzerland, in March 2020. However, the COVID-19 pandemic put a spoke in the wheel of almost all conferences to be held in 2020. After moving the conference to 8–9 October 2020, we got hit by the second wave and finally decided at short notice to go fully online. On the other hand, the pandemic has made us even more aware of the importance of accelerating research in viral bioinformatics. Advances in bioinformatics have led to improved approaches to investigate viral infections and outbreaks. The International Virus Bioinformatics Meeting 2020 has attracted approximately 120 experts in virology and bioinformatics from all over the world to join the two-day virtual meeting. Despite concerns being raised that virtual meetings lack possibilities for face-to-face discussion, the participants from this small community created a highly interactive scientific environment, engaging in lively and inspiring discussions and suggesting new research directions and questions. The meeting featured five invited and twelve contributed talks, on the four main topics: (1) proteome and RNAome of RNA viruses, (2) viral metagenomics and ecology, (3) virus evolution and classification and (4) viral infections and immunology. Further, the meeting featured 20 oral poster presentations, all of which focused on specific areas of virus bioinformatics. This report summarizes the main research findings and highlights presented at the meeting.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

NCBI’s Virus Discovery Codeathon: Building “FIVE” —The Federated Index of Viral Experiments API Index

Viruses represent important test cases for data federation due to their genome size and the rapid increase in sequence data in publicly available databases. However, some consequences of previously decentralized (unfederated) data are lack of consensus or comparisons between feature annotations. Unifying or displaying alternative annotations should be a priority both for communities with robust entry representation and for nascent communities with burgeoning data sources. To this end, during this three-day continuation of the Virus Hunting Toolkit codeathon series (VHT-2), a new integrated and federated viral index was elaborated. This Federated Index of Viral Experiments (FIVE) integrates pre-existing and novel functional and taxonomy annotations and virus–host pairings. Variability in the context of viral genomic diversity is often overlooked in virus databases. As a proof-of-concept, FIVE was the first attempt to include viral genome variation for HIV, the most well-studied human pathogen, through viral genome diversity graphs. As per the publication of this manuscript, FIVE is the first implementation of a virus-specific federated index of such scope. FIVE is coded in BigQuery for optimal access of large quantities of data and is publicly accessible. Many projects of database or index federation fail to provide easier alternatives to access or query information. To this end, a Python API query system was developed to enhance the accessibility of FIVE.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Serum Neutralizing and Enhancing Effects on African Swine Fever Virus Infectivity in Adherent Pig PBMC

African swine fever virus (ASFV) causes hemorrhagic fever with mortality rates of up to 100% in domestic pigs. Currently, there are no commercial vaccines for the disease. Only some live-attenuated viruses have been able to protect pigs from ASFV infection. The immune mechanisms involved in the protection are unclear. Immune sera can neutralize ASFV but incompletely. The mechanisms involved are not fully understood. Currently, there is no standardized protocol for ASFV neutralization assays. In this study, a flow cytometry-based ASFV neutralization assay was developed and tested in pig adherent PBMC using a virulent ASFV containing a fluorescent protein gene as a substrate for neutralization. As with previous studies, the percentage of infected macrophages was approximately five time higher than that of infected monocytes, and nearly all infected cells displayed no staining with anti-CD16 antibodies. Sera from naïve pigs and pigs immunized with a live-attenuated ASFV and fully protected against parental virus were used in the assay. The sera displayed incomplete neutralization with MOI-dependent neutralizing efficacies. Extracellular, but not intracellular, virions suspended in naïve serum were more infectious than those in the culture medium, as reported for some enveloped viruses, suggesting a novel mechanism of ASFV infection in macrophages. Both the intracellular and extracellular virions could not be completely neutralized.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Prokaryotic viruses impact functional microorganisms in nutrient removal and carbon cycle in wastewater treatment plants

As one of the largest biotechnological applications, activated sludge (AS) systems in wastewater treatment plants (WWTPs) harbor enormous viruses, with 10-1,000-fold higher concentrations than in natural environments. However, the compositional variation and host-connections of AS viruses remain poorly explored. Here, we report a catalogue of ~50,000 prokaryotic viruses from six WWTPs, increasing the number of described viral species of AS by 23-fold, and showing the very high viral diversity which is largely unknown (98.4-99.6% of total viral contigs). Most viral genera are represented in more than one AS system with 53 identified across all. Viral infection widely spans 8 archaeal and 58 bacterial phyla, linking viruses with aerobic/anaerobic heterotrophs, and other functional microorganisms controlling nitrogen/phosphorous removal. Notably, Mycobacterium, notorious for causing AS foaming, is associated with 402 viral genera. Our findings expand the current AS virus catalogue and provide reference for the phage treatment to control undesired microorganisms in WWTPs.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2023

Cross-protective antibodies against common endemic respiratory viruses

Respiratory syncytial virus (RSV), human metapneumovirus (HMPV), and human parainfluenza virus types one (HPIV1) and three (HPIV3) can cause severe disease and death in immunocompromised patients, the elderly, and those with underlying lung disease. A protective monoclonal antibody exists for RSV, but clinical use is limited to high-risk infant populations. Hence, therapeutic options for these viruses in vulnerable patient populations are currently limited. Here, we present the discovery, in vitro characterization, and in vivo efficacy testing of two cross-neutralizing monoclonal antibodies, one targeting both HPIV3 and HPIV1 and the other targeting both RSV and HMPV. The 3 × 1 antibody is capable of targeting multiple parainfluenza viruses; the MxR antibody shares features with other previously reported monoclonal antibodies that are capable of neutralizing both RSV and HMPV. We obtained structures using cryo-electron microscopy of these antibodies in complex with their antigens at 3.62 Å resolution for 3 × 1 bound to HPIV3 and at 2.24 Å for MxR bound to RSV, providing a structural basis for in vitro binding and neutralization. Together, a cocktail of 3 × 1 and MxR could have clinical utility in providing broad protection against four of the respiratory viruses that cause significant morbidity and mortality in at-risk individuals.

60 APPLIED LIFE SCIENCES↗
DOE OSTI2023

A subset of viruses thrives following microbial resuscitation during rewetting of a seasonally dry California grassland soil

Viruses are abundant, ubiquitous members of soil communities that kill microbial cells, but how they respond to perturbation of soil ecosystems is essentially unknown. Here, we investigate lineage-specific virus-host dynamics in grassland soil following “wet-up”, when resident microbes are both resuscitated and lysed after a prolonged dry period. Quantitative isotope tracing, time-resolved metagenomics and viromic analyses indicate that dry soil holds a diverse but low biomass reservoir of virions, of which only a subset thrives following wet-up. Viral richness decreases by 50% within 24 h post wet-up, while viral biomass increases four-fold within one week. Though recent hypotheses suggest lysogeny predominates in soil, our evidence indicates that viruses in lytic cycles dominate the response to wet-up. We estimate that viruses drive a measurable and continuous rate of cell lysis, with up to 46% of microbial death driven by viral lysis one week following wet-up. Thus, viruses contribute to turnover of soil microbial biomass and the widely reported CO 2 efflux following wet-up of seasonally dry soils.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2025

Population ecology and biogeochemical implications of ssDNA and dsDNA viruses along a permafrost thaw gradient

Anthropogenic-driven climate change is accelerating permafrost thaw, threatening to release vast carbon stores through increased microbial activity. While microbial roles are increasingly studied, the contributions of viruses remain largely unexplored, in part due to soil-associated technical challenges that have hindered their detection and characterization. Here, we applied an optimized virion enrichment workflow along a permafrost thaw gradient, identifying 9,963 viral populations (vOTUs), including single- and double-stranded DNA viruses, with 99.9% novelty compared to other soils. Hosts were predicted for 38% of vOTUs, spanning nine archaeal, and 36 bacterial phyla, 22% of which were linked to metagenome-assembled genomes, including key carbon-cycling taxa. Genomic analyses revealed 811 putative auxiliary metabolic genes (AMGs) from 658 vOTUs, nearly half involved in carbon processing. These included 59 glycoside hydrolases (GH) across nine GH families, 45 for monosaccharide degradation, and seven involved in short-chain fatty acid and C1 metabolism, linking viruses to both early and late stages of carbon turnover. Additionally, six vOTUs carried racD, which may stabilize microbial necromass and promote long-term carbon storage. Viral and AMG functional diversity increased with thaw stage, indicating that viruses might participate in a broadening range of microbial metabolic processes as permafrost thaws. These findings expand our understanding of virus contributions in microbial carbon processing and suggest their important role in deciphering soil carbon fate under changing climate conditions.

Biological and medical sciences↗
DOE OSTI2023

Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats

Abstract Many microbes in nature reside in dense, metabolically interdependent communities. We investigated the nature and extent of microbe-virus interactions in relation to microbial density and syntrophy by examining microbe-virus interactions in a biomass dense, deep-sea hydrothermal mat. Using metagenomic sequencing, we find numerous instances where phylogenetically distant (up to domain level) microbes encode CRISPR-based immunity against the same viruses in the mat. Evidence of viral interactions with hosts cross-cutting microbial domains is particularly striking between known syntrophic partners, for example those engaged in anaerobic methanotrophy. These patterns are corroborated by proximity-ligation-based (Hi-C) inference. Surveys of public datasets reveal additional viruses interacting with hosts across domains in diverse ecosystems known to harbour syntrophic biofilms. We propose that the entry of viral particles and/or DNA to non-primary host cells may be a common phenomenon in densely populated ecosystems, with eco-evolutionary implications for syntrophic microbes and CRISPR-mediated inter-population augmentation of resilience against viruses.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Cut site preference allows influenza A virus PA-X to discriminate between host and viral mRNAs

Many viruses block host gene expression to take over the infected cell. This process, termed host shutoff, is thought to promote viral replication by preventing antiviral responses and redirecting cellular resources to viral processes. Several viruses from divergent families accomplish host shutoff through RNA degradation by endoribonucleases. However, viruses also need to ensure expression of their own genes. The influenza A virus endoribonuclease PA-X solves this problem by sparing viral mRNAs and some host RNAs necessary for viral replication. Here, to understand how PA-X distinguishes between RNAs, we characterized PA-X cut sites transcriptome-wide using 5' rapid amplification of complementary DNA ends coupled to high-throughput sequencing. This analysis, along with RNA structure predictions and validation experiments using reporters, shows that PA-Xs from multiple influenza strains preferentially cleave RNAs at GCUG tetramers in hairpin loops. Importantly, GCUG tetramers are enriched in the human but not the influenza transcriptome. Moreover, optimal PA-X cut sites inserted in the influenza A virus genome are quickly selected against during viral replication in cells. This finding suggests that PA-X evolved these cleavage characteristics to preferentially target host over viral mRNAs in a manner reminiscent of cellular self versus non-self discrimination.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Hot springs viruses at Yellowstone National Park have ancient origins and are adapted to thermophilic hosts

Geothermal springs house unicellular red algae in the class Cyanidiophyceae that dominate the microbial biomass at these sites. Little is known about host-virus interactions in these environments. We analyzed the virus community associated with red algal mats in three neighboring habitats (creek, endolithic, soil) at Lemonade Creek, Yellowstone National Park (YNP), USA. We find that despite proximity, each habitat houses a unique collection of viruses, with the giant viruses, Megaviricetes, dominant in all three. The early branching phylogenetic position of genes encoded on metagenome assembled virus genomes (vMAGs) suggests that the YNP lineages are of ancient origin and not due to multiple invasions from mesophilic habitats. The existence of genomic footprints of adaptation to thermophily in the vMAGs is consistent with this idea. The Cyanidiophyceae at geothermal sites originated ca. 1.5 Bya and are therefore relevant to understanding biotic interactions on the early Earth.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

iVirus 2.0: Cyberinfrastructure-supported tools and data to power DNA virus ecology

Microbes drive myriad ecosystem processes, but under strong influence from viruses. Because studying viruses in complex systems requires different tools than those for microbes, they remain underexplored. To combat this, we previously aggregated double-stranded DNA (dsDNA) virus analysis capabilities and resources into ‘iVirus’ on the CyVerse collaborative cyberinfrastructure. Here we substantially expand iVirus’s functionality and accessibility, to iVirus 2.0, as follows. First, core iVirus apps were integrated into the Department of Energy’s Systems Biology KnowledgeBase (KBase) to provide an additional analytical platform. Second, at CyVerse, 20 software tools (apps) were upgraded or added as new tools and capabilities. Third, nearly 20-fold more sequence reads were aggregated to capture new data and environments. Finally, documentation, as “live” protocols, was updated to maximize user interaction with and contribution to infrastructure development. Together, iVirus 2.0 serves as a uniquely central and accessible analytical platform for studying how viruses, particularly dsDNA viruses, impact diverse microbial ecosystems.

Bolduc, Benjamin (ORCID:0000000324200755)↗
DOE OSTI2020

Fungi and viruses as important players in microbial mats

ABSTRACT Microbial mats are compacted, surface-associated microbial ecosystems reminiscent of the first living communities on early Earth. While often considered predominantly prokaryotic, recent findings show that both fungi and viruses are ubiquitous in microbial mats, albeit their functional roles remain unknown. Fungal research has mostly focused on terrestrial and freshwater ecosystems where fungi are known as important recyclers of organic matter, whereas viruses are exceptionally abundant and important in aquatic ecosystems. Here, viruses have shown to affect organic matter cycling and the diversity of microbial communities by facilitating horizontal gene transfer and cell lysis. We hypothesise fungi and viruses to have similar roles in microbial mats. Based on the analysis of previous research in terrestrial and aquatic ecosystems, we outline novel hypotheses proposing strong impacts of fungi and viruses on element cycling, food web structure and function in microbial mats, and outline experimental approaches for studies needed to understand these interactions.

Carreira, Cátia↗
DOE OSTI2022

IMG/VR v4: an expanded database of uncultivated virus genomes within a framework of extensive functional, taxonomic, and ecological metadata

Viruses are widely recognized as critical members of all microbiomes. Metagenomics enables large-scale exploration of the global virosphere, progressively revealing the extensive genomic diversity of viruses on Earth and highlighting the myriad of ways by which viruses impact biological processes. IMG/VR provides access to the largest collection of viral sequences obtained from (meta)genomes, along with functional annotation and rich metadata. A web interface enables users to efficiently browse and search viruses based on genome features and/or sequence similarity. Here, for this work, we present the fourth version of IMG/VR, composed of >15 million virus genomes and genome fragments, a ≈6-fold increase in size compared to the previous version. These clustered into 8.7 million viral operational taxonomic units, including 231 408 with at least one high-quality representative. Viral sequences in IMG/VR are now systematically identified from genomes, metagenomes, and metatranscriptomes using a new detection approach (geNomad), and IMG standard annotation are complemented with genome quality estimation using CheckV, taxonomic classification reflecting the latest taxonomic standards, and microbial host taxonomy prediction. IMG/VR v4 is available at https://img.jgi.doe.gov/vr, and the underlying data are available to download at https://genome.jgi.doe.gov/portal/IMG_VR.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2026

VirJenDB: a FAIR (meta)data and bioinformatics platform for all viruses

High-throughput sequencing has generated an unprecedented volume of data. However, researcher-submitted data in repositories requires extensive curation and quality control for reuse. These tasks are hindered by the multiplicity of repositories, the sheer volume of the data, and the complexity of virus (meta)data curation. To address these challenges, VirJenDB offers a user-friendly platform to facilitate versioned, community-driven curation, and ontology development. Virus sequences were ingested from 16 sources, including ~200 fields of metadata or standards, covering taxonomy, sample, and host information. Up to 85 metadata fields have undergone at least one round of curation, and are linked to 15.4 million virus sequences, with 88 % from those infecting eukaryotes and the remaining infecting prokaryotes. Subsets were created, including a novel collection of 0.91 million viral operational taxonomic unit (vOTU) sequences across all viruses, while keeping the original sequences from each vOTU to facilitate downstream analyses, e.g. sequence variation. The VirJenDB web portal (https://www.virjendb.org) provides HTTPS and Application Programming Interface (API) access to the sequence datasets and metadata, offering a search engine, filtering, download, visualizations, and documentation. VirJenDB aims to connect the phage and eukaryotic virus research communities by supporting webtool integration, meta-analyses, and metadata schema extensions.

Saghaei, Shahram↗
DOE OSTI2022

Soil viruses: Understudied agents of soil ecology

Over the past couple decades there has been intense exploration of the soil microbiome using modern sequencing and bioinformatics approaches. These studies have revealed a vast diversity of microorganisms across a variety of habitats (Thompson et al., 2017) and how differences in the environment, for example with climate change, influence the soil microbial community composition (Jansson and Hofmockel, 2020). The focus of these studies has primarily been on microbial cellular organisms, including bacteria, archaea and fungi. By contrast, in depth study of soil viruses has been largely neglected, until recently. There are several reasons that soil viruses are less studied, including difficulties with extraction of viruses from soil particles, difficulties with classification of soil viruses based on microscopic imaging, and reliance on the small proportion of microbial hosts that can be cultivated. Now that comprehensive soil metagenomes are available the current trend has been to survey the metagenomes for viral sequences. This approach has revealed that soil viruses are incredibly abundant, highly diverse, and largely uncharacterized (Paez-Espino et al., 2016). This so-called ‘viral dark matter’ presents an incredible research opportunity for the future. Here I will highlight some of these potential research avenues based on what is known to date.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2020

Molecular Architecture of Early Dissemination and Massive Second Wave of the SARS-CoV-2 Virus in a Major Metropolitan Area

We sequenced the genomes of 5,085 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains causing two coronavirus disease 2019 (COVID-19) disease waves in metropolitan Houston, TX, an ethnically diverse region with 7 million residents. The genomes were from viruses recovered in the earliest recognized phase of the pandemic in Houston and from viruses recovered in an ongoing massive second wave of infections. The virus was originally introduced into Houston many times independently. Virtually all strains in the second wave have a Gly614 amino acid replacement in the spike protein, a polymorphism that has been linked to increased transmission and infectivity. Patients infected with the Gly614 variant strains had significantly higher virus loads in the nasopharynx on initial diagnosis. We found little evidence of a significant relationship between virus genotype and altered virulence, stressing the linkage between disease severity, underlying medical conditions, and host genetics. Some regions of the spike protein—the primary target of global vaccine efforts—are replete with amino acid replacements, perhaps indicating the action of selection. We exploited the genomic data to generate defined single amino acid replacements in the receptor binding domain of spike protein that, importantly, produced decreased recognition by the neutralizing monoclonal antibody CR3022. Our report represents the first analysis of the molecular architecture of SARS-CoV-2 in two infection waves in a major metropolitan region. The findings will help us to understand the origin, composition, and trajectory of future infection waves and the potential effect of the host immune response and therapeutic maneuvers on SARS-CoV-2 evolution.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Diversity, taxonomy, and evolution of archaeal viruses of the class Caudoviricetes

The archaeal tailed viruses (arTV), evolutionarily related to tailed double-stranded DNA (dsDNA) bacteriophages of the class Caudoviricetes , represent the most common isolates infecting halophilic archaea. Only a handful of these viruses have been genomically characterized, limiting our appreciation of their ecological impacts and evolution. Here, we present 37 new genomes of haloarchaeal tailed virus isolates, more than doubling the current number of sequenced arTVs. Analysis of all 63 available complete genomes of arTVs, which we propose to classify into 14 new families and 3 orders, suggests ancient divergence of archaeal and bacterial tailed viruses and points to an extensive sharing of genes involved in DNA metabolism and counterdefense mechanisms, illuminating common strategies of virus–host interactions with tailed bacteriophages. Coupling of the comparative genomics with the host range analysis on a broad panel of haloarchaeal species uncovered 4 distinct groups of viral tail fiber adhesins controlling the host range expansion. The survey of metagenomes using viral hallmark genes suggests that the global architecture of the arTV community is shaped through recurrent transfers between different biomes, including hypersaline, marine, and anoxic environments.

59 BASIC BIOLOGICAL SCIENCES↗