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Applications of Next-Generation Sequencing in Virus Discovery 2.0

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "General Virology".

Deadline for manuscript submissions: closed (30 June 2023) | Viewed by 22622

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Dr. Leyi Wang

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1. Department of Veterinary Clinical Medicine, University of Illinois Urbana Champaign (UIUC), Champaign, IL 61820, USA
2. Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois Urbana Champaign (UIUC), Champaign, IL 61820, USA
Interests: animal viruses; coronavirus; picornavirus, influenza; diagnosis; new virus discovery; vaccine development
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Dr. Ganwu Li

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Vet Diagnostic & Production Animal Medicine, Veterinary Diagnostic Laboratory, College of Veterinary Medicine, Iowa State University, 1907 ISU C-Drive, VMRI#1, Ames, IA 50011, USA
Interests: new virus discovery; emerging and re-emerging infectious diseases; genomic epidemiology; molecular pathogenesis
Special Issues, Collections and Topics in MDPI journals

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Dear Colleagues,

In 2005, the emergence of next-generation sequencing (NGS) technology is mainly due to the disadvantages of the conventional Sanger sequencing method, including low throughput, labor-intensive, time-consuming, and high-cost. Since then, NGS has tremendously transformed the biomedical field and advanced diagnostic-related investigations to the next level. There are three categories of applications, including DNA sequencing, RNA sequencing, and protein sequencing. DNA sequencing consists of metagenomics sequencing, targeted genome sequencing, and whole genome sequencing; RNA sequencing has small RNA profiling and transcriptome sequencing; and protein sequencing includes ribosome profiling, CHIP-Seq, and DNA methylation sequencing. In the clinical microbiology field, NGS is commonly used.

Today, in addition to its routine application by public health officials for case investigations of food-borne bacteria, NGS has been frequently used to identify emerging and reemerging viral pathogens causing infectious diseases in human and animals. There are several viruses identified using NGS, including influenza D virus, porcine circovirus 3, porcine pegivirus, sparrow deltacoronavirus, and porcine nordavirus. NGS has also been successfully applied to the identification of viral variants, including PRRSV recombinants evolved from the wild type, and vaccine strains and PEDV variant with large deletion in the spike gene. In addition, viral gene sequencing is often used to study molecular epidemiology and/or the genetic relatedness of different viral strains. Compared to single and/or several gene(s) sequencing, whole genome sequencing of viruses is able to provide more comprehensive evidence reflecting viral evolution and differentiating viral strains.

In this issue, we would like to cover the applications of NGS for the discovery of new and reemerging viruses, the identification of new viral variants, and also for the better characterization of existing viruses.

Dr. Leyi Wang
Dr. Ganwu Li
Guest Editors

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

next-generation sequencing
virus discovery
emerging virus
remerging virus
human virus
animal virus

Published Papers (11 papers)

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Research

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25 pages, 6902 KiB

Open AccessArticle

Characterization of Diverse Anelloviruses, Cressdnaviruses, and Bacteriophages in the Human Oral DNA Virome from North Carolina (USA)

by Elise N. Paietta, Simona Kraberger, Joy M. Custer, Karla L. Vargas, Claudia Espy, Erin Ehmke, Anne D. Yoder and Arvind Varsani

Viruses 2023, 15(9), 1821; https://doi.org/10.3390/v15091821 - 26 Aug 2023

Viewed by 1666

Abstract

The diversity of viruses identified from the various niches of the human oral cavity—from saliva to dental plaques to the surface of the tongue—has accelerated in the age of metagenomics. This rapid expansion demonstrates that our understanding of oral viral diversity is incomplete, with only a few studies utilizing passive drool collection in conjunction with metagenomic sequencing methods. For this pilot study, we obtained 14 samples from healthy staff members working at the Duke Lemur Center (Durham, NC, USA) to determine the viral diversity that can be identified in passive drool samples from humans. The complete genomes of 3 anelloviruses, 9 cressdnaviruses, 4 Caudoviricetes large bacteriophages, 29 microviruses, and 19 inoviruses were identified in this study using high-throughput sequencing and viral metagenomic workflows. The results presented here expand our understanding of the vertebrate-infecting and microbe-infecting viral diversity of the human oral virome in North Carolina (USA). Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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17 pages, 647 KiB

Open AccessArticle

Unbiased Virus Detection in a Danish Zoo Using a Portable Metagenomic Sequencing System

by Anna S. Fomsgaard, Stamatios A. Tahas, Katja Spiess, Charlotta Polacek, Jannik Fonager and Graham J. Belsham

Viruses 2023, 15(6), 1399; https://doi.org/10.3390/v15061399 - 20 Jun 2023

Viewed by 2029

Abstract

Metagenomic next-generation sequencing (mNGS) is receiving increased attention for the detection of new viruses and infections occurring at the human–animal interface. The ability to actively transport and relocate this technology enables in situ virus identification, which could reduce response time and enhance disease management. In a previous study, we developed a straightforward mNGS procedure that greatly enhances the detection of RNA and DNA viruses in human clinical samples. In this study, we improved the mNGS protocol with transportable battery-driven equipment for the portable, non-targeted detection of RNA and DNA viruses in animals from a large zoological facility, to simulate a field setting for point-of-incidence virus detection. From the resulting metagenomic data, we detected 13 vertebrate viruses from four major virus groups: (+)ssRNA, (+)ssRNA-RT, dsDNA and (+)ssDNA, including avian leukosis virus in domestic chickens (Gallus gallus), enzootic nasal tumour virus in goats (Capra hircus) and several small, circular, Rep-encoding, ssDNA (CRESS DNA) viruses in several mammal species. More significantly, we demonstrate that the mNGS method is able to detect potentially lethal animal viruses, such as elephant endotheliotropic herpesvirus in Asian elephants (Elephas maximus) and the newly described human-associated gemykibivirus 2, a human-to-animal cross-species virus, in a Linnaeus two-toed sloth (Choloepus didactylus) and its enclosure, for the first time. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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17 pages, 5083 KiB

Open AccessArticle

Investigation of the Molecular Epidemiology and Evolution of Circulating Severe Acute Respiratory Syndrome Coronavirus 2 in Thailand from 2020 to 2022 via Next-Generation Sequencing

by Jiratchaya Puenpa, Vorthon Sawaswong, Pattaraporn Nimsamer, Sunchai Payungporn, Patthaya Rattanakomol, Nutsada Saengdao, Jira Chansaenroj, Ritthideach Yorsaeng, Kamol Suwannakarn and Yong Poovorawan

Viruses 2023, 15(6), 1394; https://doi.org/10.3390/v15061394 - 19 Jun 2023

Cited by 4 | Viewed by 1340

Abstract

Coronavirus disease 2019 (COVID-19) is an infectious condition caused by the severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), which surfaced in Thailand in early 2020. The current study investigated the SARS-CoV-2 lineages circulating in Thailand and their evolutionary history. Complete genome sequencing of 210 SARS-CoV-2 samples collected from collaborating hospitals and the Institute of Urban Disease Control and Prevention over two years, from December 2020 to July 2022, was performed using next-generation sequencing technology. Multiple lineage introductions were observed before the emergence of the B.1.1.529 omicron variant, including B.1.36.16, B.1.351, B.1.1, B.1.1.7, B.1.524, AY.30, and B.1.617.2. The B.1.1.529 omicron variant was subsequently detected between January 2022 and June 2022. The evolutionary rate for the spike gene of SARS-CoV-2 was estimated to be between 0.87 and 1.71 × 10⁻³ substitutions per site per year. There was a substantial prevalence of the predominant mutations C25672T (L94F), C25961T (T190I), and G26167T (V259L) in the ORF3a gene during the Thailand outbreaks. Complete genome sequencing can enhance the prediction of future variant changes in viral genomes, which is crucial to ensuring that vaccine strains are protective against worldwide outbreaks. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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20 pages, 919 KiB

Open AccessArticle

Virus Pop—Expanding Viral Databases by Protein Sequence Simulation

by Julia Kende, Massimiliano Bonomi, Sarah Temmam, Béatrice Regnault, Philippe Pérot, Marc Eloit and Thomas Bigot

Viruses 2023, 15(6), 1227; https://doi.org/10.3390/v15061227 - 24 May 2023

Viewed by 1275

Abstract

The improvement of our knowledge of the virosphere, which includes unknown viruses, is a key area in virology. Metagenomics tools, which perform taxonomic assignation from high throughput sequencing datasets, are generally evaluated with datasets derived from biological samples or in silico spiked samples containing known viral sequences present in public databases, resulting in the inability to evaluate the capacity of these tools to detect novel or distant viruses. Simulating realistic evolutionary directions is therefore key to benchmark and improve these tools. Additionally, expanding current databases with realistic simulated sequences can improve the capacity of alignment-based searching strategies for finding distant viruses, which could lead to a better characterization of the “dark matter” of metagenomics data. Here, we present Virus Pop, a novel pipeline for simulating realistic protein sequences and adding new branches to a protein phylogenetic tree. The tool generates simulated sequences with substitution rate variations that are dependent on protein domains and inferred from the input dataset, allowing for a realistic representation of protein evolution. The pipeline also infers ancestral sequences corresponding to multiple internal nodes of the input data phylogenetic tree, enabling new sequences to be inserted at various points of interest in the group studied. We demonstrated that Virus Pop produces simulated sequences that closely match the structural and functional characteristics of real protein sequences, taking as an example the spike protein of sarbecoviruses. Virus Pop also succeeded at creating sequences that resemble real sequences not included in the databases, which facilitated the identification of a novel pathogenic human circovirus not included in the input database. In conclusion, Virus Pop is helpful for challenging taxonomic assignation tools and could help improve databases to better detect distant viruses. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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19 pages, 5033 KiB

Open AccessArticle

Metagenomic Detection of Divergent Insect- and Bat-Associated Viruses in Plasma from Two African Individuals Enrolled in Blood-Borne Surveillance

by Gregory S. Orf, Ana Olivo, Barbara Harris, Sonja L. Weiss, Asmeeta Achari, Guixia Yu, Scot Federman, Dora Mbanya, Linda James, Samuel Mampunza, Charles Y. Chiu, Mary A. Rodgers, Gavin A. Cloherty and Michael G. Berg

Viruses 2023, 15(4), 1022; https://doi.org/10.3390/v15041022 - 21 Apr 2023

Cited by 3 | Viewed by 2587

Abstract

Metagenomic next-generation sequencing (mNGS) has enabled the high-throughput multiplexed identification of sequences from microbes of potential medical relevance. This approach has become indispensable for viral pathogen discovery and broad-based surveillance of emerging or re-emerging pathogens. From 2015 to 2019, plasma was collected from 9586 individuals in Cameroon and the Democratic Republic of the Congo enrolled in a combined hepatitis virus and retrovirus surveillance program. A subset (n = 726) of the patient specimens was analyzed by mNGS to identify viral co-infections. While co-infections from known blood-borne viruses were detected, divergent sequences from nine poorly characterized or previously uncharacterized viruses were also identified in two individuals. These were assigned to the following groups by genomic and phylogenetic analyses: densovirus, nodavirus, jingmenvirus, bastrovirus, dicistrovirus, picornavirus, and cyclovirus. Although of unclear pathogenicity, these viruses were found circulating at high enough concentrations in plasma for genomes to be assembled and were most closely related to those previously associated with bird or bat excrement. Phylogenetic analyses and in silico host predictions suggested that these are invertebrate viruses likely transmitted through feces containing consumed insects or through contaminated shellfish. This study highlights the power of metagenomics and in silico host prediction in characterizing novel viral infections in susceptible individuals, including those who are immunocompromised from hepatitis viruses and retroviruses, or potentially exposed to zoonotic viruses from animal reservoir species. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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16 pages, 2408 KiB

Open AccessArticle

Whole-Genome-Sequence-Based Evolutionary Analyses of HoBi-like Pestiviruses Reveal Insights into Their Origin and Evolutionary History

by Semmannan Kalaiyarasu, Niranjan Mishra, Saravanan Subramaniam, Dashprakash Moorthy, Shashi Bhusan Sudhakar, Vijendra Pal Singh and Aniket Sanyal

Viruses 2023, 15(3), 733; https://doi.org/10.3390/v15030733 - 11 Mar 2023

Viewed by 1649

Abstract

HoBi-like pestivirus (HoBiPeV), classified under Pestivirus H species, is an emerging cattle pathogen of high economic impact. However, the origin and evolution of HoBiPeV are not very clear due to a lack of full genomic sequences from diverse clades. This study aimed to determine full-genome sequences of HoBiPeV strains of three novel clades (c, d and e) and perform full-genome-based genetic and evolutionary analyses. Bayesian phylogenetic analyses herein confirmed the existence and independent evolution of four main HoBiPeV clades (a, c, d and e) globally, with genetic divergence ranging from 13.0% to 18.2%. Our Bayesian molecular clock estimates revealed that HoBiPeV most likely originated in India, with a dated tMRCA of 1938 (1762–2000), evidencing a more recent origin of HoBiPeV. The evolution rate of HoBiPeV was estimated to be 2.133 × 10⁻³ subs/site/year at full-genome level but varied widely among individual genes. Selection pressure analyses identified most of the positively selected sites in E2. Additionally, 21.8% of the ORF codon sites were found under strong episodic diversifying selection, providing first evidence of negative selection in HoBiPeV evolution. No recombination event was evident for HoBiPeV-c, d and e strains. These findings provide new insights into HoBiPeV origin and evolutionary history for better understanding the epidemiology and host–pathogen interactions and stimulate vaccine research. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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13 pages, 932 KiB

Open AccessArticle

Enhanced Viral Metagenomics with Lazypipe 2

by Ilya Plyusnin, Olli Vapalahti, Tarja Sironen, Ravi Kant and Teemu Smura

Viruses 2023, 15(2), 431; https://doi.org/10.3390/v15020431 - 04 Feb 2023

Cited by 5 | Viewed by 2227

Abstract

Viruses are the main agents causing emerging and re-emerging infectious diseases. It is therefore important to screen for and detect them and uncover the evolutionary processes that support their ability to jump species boundaries and establish themselves in new hosts. Metagenomic next-generation sequencing (mNGS) is a high-throughput, impartial technology that has enabled virologists to detect either known or novel, divergent viruses from clinical, animal, wildlife and environmental samples, with little a priori assumptions. mNGS is heavily dependent on bioinformatic analysis, with an emerging demand for integrated bioinformatic workflows. Here, we present Lazypipe 2, an updated mNGS pipeline with, as compared to Lazypipe1, significant improvements in code stability and transparency, with added functionality and support for new software components. We also present extensive benchmarking results, including evaluation of a novel canine simulated metagenome, precision and recall of virus detection at varying sequencing depth, and a low to extremely low proportion of viral genetic material. Additionally, we report accuracy of virus detection with two strategies: homology searches using nucleotide or amino acid sequences. We show that Lazypipe 2 with nucleotide-based annotation approaches near perfect detection for eukaryotic viruses and, in terms of accuracy, outperforms the compared pipelines. We also discuss the importance of homology searches with amino acid sequences for the detection of highly divergent novel viruses. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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12 pages, 2185 KiB

Open AccessArticle

A Novel Rhabdovirus Associated with the Idaho Population of Potato Cyst Nematode Globodera pallida

by Joanna Kud, Jennifer Dahan, Gardenia E. Orellana, Louise-Marie Dandurand and Alexander V. Karasev

Viruses 2022, 14(12), 2718; https://doi.org/10.3390/v14122718 - 05 Dec 2022

Cited by 1 | Viewed by 2203

Abstract

Globodera pallida, a potato cyst nematode (PCN), is a quarantine endoparasitic pest of potato (Solanum tuberosum) in the US due to its effects on yield and quality of potato tubers. A new rhabdovirus, named potato cyst nematode rhabdovirus (PcRV), was revealed and characterized in the G. pallida populations collected in Idaho through use of high-throughput sequencing (HTS) and RT-PCR and found to be most closely related to soybean cyst nematode rhabdovirus (ScRV). PcRV has a 13,604 bp long, single-stranded RNA genome encoding five open reading frames, including four rhabdovirus-specific genes, N, P, G, and L, and one unknown gene. PcRV was found present in eggs, invasive second-stage juveniles, and parasitic females of G. pallida, implying a vertical transmission mode. RT-PCR and partial sequencing of PcRV in laboratory-reared G. pallida populations maintained over five years suggested that the virus is highly persistent and genetically stable. Two other Globodera spp. reproducing on potato and reported in the US, G. rostochiensis and G. ellingtonae, tested negative for PcRV presence. To the best of our knowledge, PcRV is the first virus experimentally found infecting G. pallida. Based on their similar genome organizations, the phylogeny of their RNA-dependent RNA polymerase domains (L gene), and relatively high identity levels in their protein products, PcRV and ScRV are proposed to form a new genus, provisionally named “Gammanemrhavirus”, within the family Rhabdoviridae. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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Review

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15 pages, 349 KiB

Open AccessReview

Bioinformatic Tools for NGS-Based Metagenomics to Improve the Clinical Diagnosis of Emerging, Re-Emerging and New Viruses

by Marta Ibañez-Lligoña, Sergi Colomer-Castell, Alejandra González-Sánchez, Josep Gregori, Carolina Campos, Damir Garcia-Cehic, Cristina Andrés, Maria Piñana, Tomàs Pumarola, Francisco Rodríguez-Frias, Andrés Antón and Josep Quer

Viruses 2023, 15(2), 587; https://doi.org/10.3390/v15020587 - 20 Feb 2023

Cited by 6 | Viewed by 4051

Abstract

Epidemics and pandemics have occurred since the beginning of time, resulting in millions of deaths. Many such disease outbreaks are caused by viruses. Some viruses, particularly RNA viruses, are characterized by their high genetic variability, and this can affect certain phenotypic features: tropism, antigenicity, and susceptibility to antiviral drugs, vaccines, and the host immune response. The best strategy to face the emergence of new infectious genomes is prompt identification. However, currently available diagnostic tests are often limited for detecting new agents. High-throughput next-generation sequencing technologies based on metagenomics may be the solution to detect new infectious genomes and properly diagnose certain diseases. Metagenomic techniques enable the identification and characterization of disease-causing agents, but they require a large amount of genetic material and involve complex bioinformatic analyses. A wide variety of analytical tools can be used in the quality control and pre-processing of metagenomic data, filtering of untargeted sequences, assembly and quality control of reads, and taxonomic profiling of sequences to identify new viruses and ones that have been sequenced and uploaded to dedicated databases. Although there have been huge advances in the field of metagenomics, there is still a lack of consensus about which of the various approaches should be used for specific data analysis tasks. In this review, we provide some background on the study of viral infections, describe the contribution of metagenomics to this field, and place special emphasis on the bioinformatic tools (with their capabilities and limitations) available for use in metagenomic analyses of viral pathogens. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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7 pages, 1258 KiB

Open AccessBrief Report

Successful Confirmation of Dual Genital Herpes Co-Infection with Herpes Simplex Virus 1 and Herpes Simplex Virus 2 Using Unbiased Metagenomic Next-Generation Sequencing

by Chun Kiat Lee, Sau Yoke Ng, Chean Nee Chai, Yu Feng Lim, Tiffany Jingyan Hu, Ogestelli Fabia Lee and Gabriel Yan

Viruses 2023, 15(9), 1957; https://doi.org/10.3390/v15091957 - 20 Sep 2023

Viewed by 1077

Abstract

Dual co-infection with both HSV-1 and HSV-2 is rare, with few cases reported in the literature. In this case report, we describe the successful use of unbiased metagenomic next-generation sequencing (mNGS) as a rapid and alternative method for confirming dual genital herpes co-infection. Our case involves a 74-year-old woman who presented with genital lesions and initially tested positive for both HSV-1 and HSV-2 via the Luminex ARIES HSV 1&2 assay. The entire mNGS process, from nucleic acid extraction to result analysis, was completed in less than 48 h. Using mNGS, we identified mapped reads specific to either HSV-1 or HSV-2 and screened the sequences to rule out mis-genotyping by the Luminex ARIES assay. Notably, the generated sequences can reveal sequence variations within multiple gene regions, demonstrating the potential of mNGS for identifying novel HSV-1 and HSV-2 variants. Our findings suggest that mNGS can serve as a rapid and reliable alternative confirmatory method for dual genital herpes infections, providing valuable information to guide appropriate treatment options for patients. By eliminating the need for prior knowledge of causative agents, mNGS offers an unbiased approach for detecting and characterizing viral co-infections. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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6 pages, 998 KiB

Open AccessBrief Report

Matrix-Encoding Gene Diversity of 624 Influenza A/H3N2 Genomes Does Not Show Association with Impaired Viral Detection by Commercialized qPCR Assays

by Lorlane Le Targa, Houmadi Hikmat, Céline Boschi, Bernard La Scola and Philippe Colson

Viruses 2022, 14(12), 2683; https://doi.org/10.3390/v14122683 - 30 Nov 2022

Viewed by 1164

Abstract

As for the case of SARS-CoV-2, genome sequencing of influenza viruses is of potential interest to raise and address virological issues. Recently, false-negativity of real-time reverse transcription-PCR (qPCR) assays that detect influenza A/H3N2 virus RNA were reported and associated with two mutations (A37T and C161T) in the Matrix-encoding (M1) gene located on viral segment 7. This triggered a national alert in France. The present study sought to assess the association between the presence of these mutations and potential false negative results of influenza A/H3N2 virus RNA detection by commercialized qPCR assays at the clinical virology laboratory of our university hospitals in southern France. This study focused on the genetic diversity in the M1 gene and segment 7 of 624 influenza A/H3N2 virus genomes obtained from respiratory samples having tested qPCR-positive with M1 gene-targeting assays in our clinical virology laboratory. A total of 585 among the 624 influenza A/H3N2 virus genomes (93.7%) were of clade 3C.2a1b.2a.2, and 39 (6.3%) were of clade 3C.2a1b.1a. M1 gene substitutions A37T and C161T were both present in 582 (93.3%) genomes, only of clade 3C.2a1b.2a.2. Substitution A37T was present in 621 (99.5%) genomes. Substitution C161T was present in 585 genomes (93.8%), all of clade 3C.2a1b.2a.2. Moreover, 21 other nucleotide positions were mutated in ≥90% of the genomes. The present study shows that A37T/C and C161T mutations, and other mutations in the M1 gene and segment 7, were widely present in influenza A/H3N2 virus genomes recovered from respiratory samples diagnosed qPCR-positive with commercialized assays. Full article

(This article belongs to the Special Issue Applications of Next-Generation Sequencing in Virus Discovery 2.0)

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