Viral Metagenomics and Metatranscriptomics: Virus Discovery, Ecology, and Evolution

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Virology".

Deadline for manuscript submissions: closed (31 October 2021) | Viewed by 25346

Special Issue Editors

Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
Interests: virus discovery and evolution; arboviruses; vector range, genetic traits, and phylogeography of arboviruses; metagenomics; metatranscriptomics
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues, 

Several human pathogenic viruses, such as Dengue, Ebola, Zika, and, recently, SARS-CoV2, originated from the sylvatic environment. The emergence of a virus into a new host is known as spillover or host jump/shift and depends on several ecological, viral, and host factors. The advances in next-generation sequencing technology and the development of high-performance bioinformatics platforms have substantially improved our understanding of viral communities, including the ‘dark matter’ of highly divergent viruses associated with insects’ vectors, mammalian hosts, and avian hosts. These new data will facilitate a better understanding of the complexity of the evolutionary and ecological processes that shape the viral pathogenesis that might lead to disease emergence.

This Special Issue of Microorganisms will be dedicated, within the topic of viral metagenomics and metatranscriptomics, to the following themes: the virome in insect vectors and their mammalian and avian hosts; the virome in co-infection with known viral pathogens; the bat virome and other vertebrates; virus–host coevolution; virus population genetics and phylodynamics; virus quasispecies; virus host range evolution and emergence; evolution of virus genome structures; and origins of virus genes. Uncovering the complex virosphere and understanding its ecology and evolution is essential to virus epidemiological surveillance, early warning system and emergence prediction, diagnostic tools, and vaccine and antiviral drug development, which are essential to public/animal health and conservation.

The major aims of this Special Issue are to communicate the latest research data and reviews on the broad range of topics relating to virus discovery, ecology, and evolution.

Dr. Daniel Cadar
Dr. Krisztián Bányai
Guest Editors

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Keywords

  • virome
  • viral evolution
  • host range/jump
  • metatranscriptomics
  • phylodynamics
  • emergence
  • recombination–reassortment
  • insect vectors
  • virus ecology

Published Papers (8 papers)

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Research

24 pages, 7878 KiB  
Article
Diverse Single-Stranded DNA Viruses Identified in Chicken Buccal Swabs
by Klaudia Chrzastek, Simona Kraberger, Kara Schmidlin, Rafaela S. Fontenele, Arun Kulkarni, Len Chappell, Louise Dufour-Zavala, Darrell R. Kapczynski and Arvind Varsani
Microorganisms 2021, 9(12), 2602; https://doi.org/10.3390/microorganisms9122602 - 16 Dec 2021
Cited by 6 | Viewed by 2395
Abstract
High-throughput sequencing approaches offer the possibility to better understand the complex microbial communities associated with animals. Viral metagenomics has facilitated the discovery and identification of many known and unknown viruses that inhabit mucosal surfaces of the body and has extended our knowledge related [...] Read more.
High-throughput sequencing approaches offer the possibility to better understand the complex microbial communities associated with animals. Viral metagenomics has facilitated the discovery and identification of many known and unknown viruses that inhabit mucosal surfaces of the body and has extended our knowledge related to virus diversity. We used metagenomics sequencing of chicken buccal swab samples and identified various small DNA viruses with circular genome organization. Out of 134 putative circular viral-like circular genome sequences, 70 are cressdnaviruses and 26 are microviruses, whilst the remaining 38 most probably represent sub-genomic molecules. The cressdnaviruses found in this study belong to the Circoviridae, Genomoviridae and Smacoviridae families as well as previously described CRESS1 and naryavirus groups. Among these, genomoviruses and smacoviruses were the most prevalent across the samples. Interestingly, we also identified 26 bacteriophages that belong to the Microviridae family, whose members are known to infect enterobacteria. Full article
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9 pages, 741 KiB  
Article
SARS-CoV-2 Evolution among Oncological Population: In-Depth Virological Analysis of a Clinical Cohort
by Florian Laubscher, Samuel Cordey, Alex Friedlaender, Cecilia Schweblin, Sarah Noetzlin, Pierre-François Simand, Natacha Bordry, Filipe De Sousa, Fiona Pigny, Stephanie Baggio, Laurent Getaz, Pierre-Yves Dietrich, Laurent Kaiser and Diem-Lan Vu
Microorganisms 2021, 9(10), 2145; https://doi.org/10.3390/microorganisms9102145 - 14 Oct 2021
Cited by 3 | Viewed by 1456
Abstract
Background: Oncological patients have a higher risk of prolonged SARS-CoV-2 shedding, which, in turn, can lead to evolutionary mutations and emergence of novel viral variants. The aim of this study was to analyze biological samples of a cohort of oncological patients by deep [...] Read more.
Background: Oncological patients have a higher risk of prolonged SARS-CoV-2 shedding, which, in turn, can lead to evolutionary mutations and emergence of novel viral variants. The aim of this study was to analyze biological samples of a cohort of oncological patients by deep sequencing to detect any significant viral mutations. Methods: High-throughput sequencing was performed on selected samples from a SARS-CoV-2-positive oncological patient cohort. Analysis of variants and minority variants was performed using a validated bioinformatics pipeline. Results: Among 54 oncological patients, we analyzed 12 samples of 6 patients, either serial nasopharyngeal swab samples or samples from the upper and lower respiratory tracts, by high-throughput sequencing. We identified amino acid changes D614G and P4715L as well as mutations at nucleotide positions 241 and 3037 in all samples. There were no other significant mutations, but we observed intra-host evolution in some minority variants, mainly in the ORF1ab gene. There was no significant mutation identified in the spike region and no minority variants common to several hosts. Conclusions: There was no major and rapid evolution of viral strains in this oncological patient cohort, but there was minority variant evolution, reflecting a dynamic pattern of quasi-species replication. Full article
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9 pages, 1380 KiB  
Communication
No Metagenomic Evidence of Causative Viral Pathogens in Postencephalitic Parkinsonism Following Encephalitis Lethargica
by Dániel Cadar, Kurt A. Jellinger, Peter Riederer, Sabrina Strobel, Camelia-Maria Monoranu and Dennis Tappe
Microorganisms 2021, 9(8), 1716; https://doi.org/10.3390/microorganisms9081716 - 12 Aug 2021
Cited by 8 | Viewed by 2462
Abstract
Postencephalitic parkinsonism (PEP) is a disease of unknown etiology and pathophysiology following encephalitis lethargica (EL), an acute-onset polioencephalitis of cryptic cause in the 1920s. PEP is a tauopathy with multisystem neuronal loss and gliosis, clinically characterized by bradykinesia, rigidity, rest tremor, and oculogyric [...] Read more.
Postencephalitic parkinsonism (PEP) is a disease of unknown etiology and pathophysiology following encephalitis lethargica (EL), an acute-onset polioencephalitis of cryptic cause in the 1920s. PEP is a tauopathy with multisystem neuronal loss and gliosis, clinically characterized by bradykinesia, rigidity, rest tremor, and oculogyric crises. Though a viral cause of EL is likely, past polymerase chain reaction-based investigations in the etiology of both PEP and EL were negative. PEP might be caused directly by an unknown viral pathogen or the consequence of a post-infectious immunopathology. The development of metagenomic next-generation sequencing in conjunction with bioinformatic techniques has generated a broad-range tool for the detection of unknown pathogens in the recent past. Retrospective identification and characterization of pathogens responsible for past infectious diseases can be successfully performed with formalin-fixed paraffin-embedded (FFPE) tissue samples. In this study, we analyzed 24 FFPE brain samples from six patients with PEP by unbiased metagenomic next-generation sequencing. Our results show that no evidence for the presence of a specific or putative (novel) viral pathogen was found, suggesting a likely post-infectious immune-mediated etiology of PEP. Full article
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21 pages, 3661 KiB  
Article
The Sisal Virome: Uncovering the Viral Diversity of Agave Varieties Reveals New and Organ-Specific Viruses
by Gabriel Quintanilha-Peixoto, Paula Luize Camargos Fonseca, Fábio Trigo Raya, Marina Pupke Marone, Dener Eduardo Bortolini, Piotr Mieczkowski, Roenick Proveti Olmo, Marcelo Falsarella Carazzolle, Christian A. Voigt, Ana Cristina Fermino Soares, Gonçalo Amarante Guimarães Pereira, Aristóteles Góes-Neto and Eric Roberto Guimarães Rocha Aguiar
Microorganisms 2021, 9(8), 1704; https://doi.org/10.3390/microorganisms9081704 - 10 Aug 2021
Cited by 8 | Viewed by 3154
Abstract
Sisal is a common name for different plant varieties in the genus Agave (especially Agave sisalana) used for high-quality natural leaf fiber extraction. Despite the economic value of these plants, we still lack information about the diversity of viruses (virome) in non- [...] Read more.
Sisal is a common name for different plant varieties in the genus Agave (especially Agave sisalana) used for high-quality natural leaf fiber extraction. Despite the economic value of these plants, we still lack information about the diversity of viruses (virome) in non-tequilana species from the genus Agave. In this work, by associating RNA and DNA deep sequencing we were able to identify 25 putative viral species infecting A. sisalana, A. fourcroydes, and Agave hybrid 11648, including one strain of Cowpea Mild Mottle Virus (CPMMV) and 24 elements likely representing new viruses. Phylogenetic analysis indicated they belong to at least six viral families: Alphaflexiviridae, Betaflexiviridae, Botourmiaviridae, Closteroviridae, Partitiviridae, Virgaviridae, and three distinct unclassified groups. We observed higher viral taxa richness in roots when compared to leaves and stems. Furthermore, leaves and stems are very similar diversity-wise, with a lower number of taxa and dominance of a single viral species. Finally, approximately 50% of the identified viruses were found in all Agave organs investigated, which suggests that they likely produce a systemic infection. This is the first metatranscriptomics study focused on viral identification in species from the genus Agave. Despite having analyzed symptomless individuals, we identified several viruses supposedly infecting Agave species, including organ-specific and systemic species. Surprisingly, some of these putative viruses are probably infecting microorganisms composing the plant microbiota. Altogether, our results reinforce the importance of unbiased strategies for the identification and monitoring of viruses in plant species, including those with asymptomatic phenotypes. Full article
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28 pages, 10806 KiB  
Article
Uncovering the Worldwide Diversity and Evolution of the Virome of the Mosquitoes Aedes aegypti and Aedes albopictus
by Rhys Parry, Maddie E James and Sassan Asgari
Microorganisms 2021, 9(8), 1653; https://doi.org/10.3390/microorganisms9081653 - 03 Aug 2021
Cited by 17 | Viewed by 6646
Abstract
Aedes aegypti, the yellow fever mosquito, and Aedes albopictus, the Asian tiger mosquito, are the most significant vectors of dengue, Zika, and Chikungunya viruses globally. Studies examining host factors that control arbovirus transmission demonstrate that insect-specific viruses (ISVs) can modulate mosquitoes’ [...] Read more.
Aedes aegypti, the yellow fever mosquito, and Aedes albopictus, the Asian tiger mosquito, are the most significant vectors of dengue, Zika, and Chikungunya viruses globally. Studies examining host factors that control arbovirus transmission demonstrate that insect-specific viruses (ISVs) can modulate mosquitoes’ susceptibility to arbovirus infection in both in vivo and in vitro co-infection models. While research is ongoing to implicate individual ISVs as proviral or antiviral factors, we have a limited understanding of the composition and diversity of the Aedes virome. To address this gap, we used a meta-analysis approach to uncover virome diversity by analysing ~3000 available RNA sequencing libraries representing a worldwide geographic range for both mosquitoes. We identified ten novel viruses and previously characterised viruses, including mononegaviruses, orthomyxoviruses, negeviruses, and a novel bi-segmented negev-like group. Phylogenetic analysis suggests close relatedness to mosquito viruses implying likely insect host range except for one arbovirus, the multi-segmented Jingmen tick virus (Flaviviridae) in an Italian colony of Ae. albopictus. Individual mosquito transcriptomes revealed remarkable inter-host variation of ISVs within individuals from the same colony and heterogeneity between different laboratory strains. Additionally, we identified striking virus diversity in Wolbachia infected Aedes cell lines. This study expands our understanding of the virome of these important vectors. It provides a resource for further assessing the ecology, evolution, and interaction of ISVs with their mosquito hosts and the arboviruses they transmit. Full article
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13 pages, 1276 KiB  
Article
Genomic Diversity of CRESS DNA Viruses in the Eukaryotic Virome of Swine Feces
by Enikő Fehér, Eszter Mihalov-Kovács, Eszter Kaszab, Yashpal S. Malik, Szilvia Marton and Krisztián Bányai
Microorganisms 2021, 9(7), 1426; https://doi.org/10.3390/microorganisms9071426 - 01 Jul 2021
Cited by 8 | Viewed by 2797
Abstract
Replication-associated protein (Rep)-encoding single-stranded DNA (CRESS DNA) viruses are a diverse group of viruses, and their persistence in the environment has been studied for over a decade. However, the persistence of CRESS DNA viruses in herds of domestic animals has, in some cases, [...] Read more.
Replication-associated protein (Rep)-encoding single-stranded DNA (CRESS DNA) viruses are a diverse group of viruses, and their persistence in the environment has been studied for over a decade. However, the persistence of CRESS DNA viruses in herds of domestic animals has, in some cases, serious economic consequence. In this study, we describe the diversity of CRESS DNA viruses identified during the metagenomics analysis of fecal samples collected from a single swine herd with apparently healthy animals. A total of nine genome sequences were assembled and classified into two different groups (CRESSV1 and CRESSV2) of the Cirlivirales order (Cressdnaviricota phylum). The novel CRESS DNA viral sequences shared 85.8–96.8% and 38.1–94.3% amino acid sequence identities for the Rep and putative capsid protein sequences compared to their respective counterparts with extant GenBank record. Data presented here show evidence for simultaneous infection of swine herds with multiple novel CRESS DNA viruses, including po-circo-like viruses and fur seal feces-associated circular DNA viruses. Given that viral genomes with similar sequence and structure have been detected in swine fecal viromes from independent studies, investigation of the association between presence of CRESS DNA viruses and swine health conditions seems to be justified. Full article
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11 pages, 2611 KiB  
Article
Genomic and Micro-Evolutionary Features of Mammalian 2 orthobornavirus (Variegated Squirrel Bornavirus 1, VSBV-1)
by Dániel Cadar, Jonas Schmidt-Chanasit and Dennis Tappe
Microorganisms 2021, 9(6), 1141; https://doi.org/10.3390/microorganisms9061141 - 25 May 2021
Cited by 3 | Viewed by 2159
Abstract
Mammalian 2 orthobornavirus (VSBV-1) is an emerging zoonotic pathogen discovered in several exotic squirrel species and associated with fatal human encephalitis. The dynamics of VSBV-1 spread and evolution in its presumed natural hosts are unknown. Here, we present the phylogeny, micro-evolution, cross-species transmission [...] Read more.
Mammalian 2 orthobornavirus (VSBV-1) is an emerging zoonotic pathogen discovered in several exotic squirrel species and associated with fatal human encephalitis. The dynamics of VSBV-1 spread and evolution in its presumed natural hosts are unknown. Here, we present the phylogeny, micro-evolution, cross-species transmission and spread of VSBV-1 at a temporal and spatial resolution within the limits of animal husbandry. The results showed that VSBV-1 can be classified into six distinct groups and that the most recent common ancestor of the known German strains emerged at least 20 years ago. We here demonstrate that the genetic diversity of the VSBV-1 groups is shaped primarily by in situ evolution and most of the amino acid changes are deleterious polymorphisms removed by purifying selection. Evidence of adaptive evolution has been found in the G and L genes which might have an influence on transmission fitness. Furthermore, there was also evidence for some form of adaptive changes in the glycoprotein which suggests that many sites might be subjected to positive pressure evolving under episodic directional selection, indicating past occurrence of positive selection. Host switching events were detected as dominant evolutionary mechanisms driving the virus-host associations. Virus spread by animal trade followed by subsequent local micro-evolution in zoos and holdings is responsible for diversifying strains. Time-resolved phylogeny indicated that Prevost’s squirrels might be the original squirrel species carrying and seeding the virus in Germany. This study provides the first insight into the ecology and micro-evolutionary dynamics of this novel viral pathogen in the captive exotic squirrel population under artificial ecological conditions (zoos and animal husbandry) and co-housing of different squirrel species. Full article
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23 pages, 5756 KiB  
Article
Comparative Metagenomics of Palearctic and Neotropical Avian Cloacal Viromes Reveal Geographic Bias in Virus Discovery
by Daniel A. Truchado, Alejandro Llanos-Garrido, David A. Oropesa-Olmedo, Belén Cerrada, Pablo Cea, Michaël A. J. Moens, Esperanza Gomez-Lucia, Ana Doménech, Borja Milá, Javier Pérez-Tris, Daniel Cadar and Laura Benítez
Microorganisms 2020, 8(12), 1869; https://doi.org/10.3390/microorganisms8121869 - 26 Nov 2020
Cited by 9 | Viewed by 2810
Abstract
Our understanding about viruses carried by wild animals is still scarce. The viral diversity of wildlife may be best described with discovery-driven approaches to the study of viral diversity that broaden research efforts towards non-canonical hosts and remote geographic regions. Birds have been [...] Read more.
Our understanding about viruses carried by wild animals is still scarce. The viral diversity of wildlife may be best described with discovery-driven approaches to the study of viral diversity that broaden research efforts towards non-canonical hosts and remote geographic regions. Birds have been key organisms in the transmission of viruses causing important diseases, and wild birds are threatened by viral spillovers associated with human activities. However, our knowledge of the avian virome may be biased towards poultry and highly pathogenic diseases. We describe and compare the fecal virome of two passerine-dominated bird assemblages sampled in a remote Neotropical rainforest in French Guiana (Nouragues Natural Reserve) and a Mediterranean forest in central Spain (La Herrería). We used metagenomic data to quantify the degree of functional and genetic novelty of viruses recovered by examining if the similarity of the contigs we obtained to reference sequences differed between both locations. In general, contigs from Nouragues were significantly less similar to viruses in databases than contigs from La Herrería using Blastn but not for Blastx, suggesting that pristine regions harbor a yet unknown viral diversity with genetically more singular viruses than more studied areas. Additionally, we describe putative novel viruses of the families Picornaviridae, Reoviridae and Hepeviridae. These results highlight the importance of wild animals and remote regions as sources of novel viruses that substantially broaden the current knowledge of the global diversity of viruses. Full article
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