Virus-derived variation in diverse human genomes

Acquisition of genetic material from viruses by their hosts can generate inter-host structural genome variation. We developed computational tools enabling us to study virus-derived structural variants (SVs) in population-scale whole genome sequencing (WGS) datasets and applied them to 3,332 humans....

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Published inPLoS genetics Vol. 17; no. 4; p. e1009324
Main Authors Kojima, Shohei, Kamada, Anselmo Jiro, Parrish, Nicholas F.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 26.04.2021
Public Library of Science (PLoS)
Subjects
Binding sites
Biology and Life Sciences
Blood cells
Chromosomes
Computer and Information Sciences
Datasets
Epstein-Barr virus
Gene expression
Genetic aspects
Genetic research
Genetic variation
Genomes
HIV
Homology
Host-virus relationships
Human genome
Human immunodeficiency virus
Leukocytes (mononuclear)
Medicine and Health Sciences
Peripheral blood mononuclear cells
Reference materials
Research and Analysis Methods
tRNA
Vero cells
Viruses
Japan
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Abstract Acquisition of genetic material from viruses by their hosts can generate inter-host structural genome variation. We developed computational tools enabling us to study virus-derived structural variants (SVs) in population-scale whole genome sequencing (WGS) datasets and applied them to 3,332 humans. Although SVs had already been cataloged in these subjects, we found previously-overlooked virus-derived SVs. We detected non-germline SVs derived from squirrel monkey retrovirus (SMRV), human immunodeficiency virus 1 (HIV-1), and human T lymphotropic virus (HTLV-1); these variants are attributable to infection of the sequenced lymphoblastoid cell lines (LCLs) or their progenitor cells and may impact gene expression results and the biosafety of experiments using these cells. In addition, we detected new heritable SVs derived from human herpesvirus 6 (HHV-6) and human endogenous retrovirus-K (HERV-K). We report the first solo-direct repeat (DR) HHV-6 likely to reflect DR rearrangement of a known full-length endogenous HHV-6. We used linkage disequilibrium between single nucleotide variants (SNVs) and variants in reads that align to HERV-K, which often cannot be mapped uniquely using conventional short-read sequencing analysis methods, to locate previously-unknown polymorphic HERV-K loci. Some of these loci are tightly linked to trait-associated SNVs, some are in complex genome regions inaccessible by prior methods, and some contain novel HERV-K haplotypes likely derived from gene conversion from an unknown source or introgression. These tools and results broaden our perspective on the coevolution between viruses and humans, including ongoing virus-to-human gene transfer contributing to genetic variation between humans.
AbstractList Acquisition of genetic material from viruses by their hosts can generate inter-host structural genome variation. We developed computational tools enabling us to study virus-derived structural variants (SVs) in population-scale whole genome sequencing (WGS) datasets and applied them to 3,332 humans. Although SVs had already been cataloged in these subjects, we found previously-overlooked virus-derived SVs. We detected non-germline SVs derived from squirrel monkey retrovirus (SMRV), human immunodeficiency virus 1 (HIV-1), and human T lymphotropic virus (HTLV-1); these variants are attributable to infection of the sequenced lymphoblastoid cell lines (LCLs) or their progenitor cells and may impact gene expression results and the biosafety of experiments using these cells. In addition, we detected new heritable SVs derived from human herpesvirus 6 (HHV-6) and human endogenous retrovirus-K (HERV-K). We report the first solo-direct repeat (DR) HHV-6 likely to reflect DR rearrangement of a known full-length endogenous HHV-6. We used linkage disequilibrium between single nucleotide variants (SNVs) and variants in reads that align to HERV-K, which often cannot be mapped uniquely using conventional short-read sequencing analysis methods, to locate previously-unknown polymorphic HERV-K loci. Some of these loci are tightly linked to trait-associated SNVs, some are in complex genome regions inaccessible by prior methods, and some contain novel HERV-K haplotypes likely derived from gene conversion from an unknown source or introgression. These tools and results broaden our perspective on the coevolution between viruses and humans, including ongoing virus-to-human gene transfer contributing to genetic variation between humans.
Acquisition of genetic material from viruses by their hosts can generate inter-host structural genome variation. We developed computational tools enabling us to study virus-derived structural variants (SVs) in population-scale whole genome sequencing (WGS) datasets and applied them to 3,332 humans. Although SVs had already been cataloged in these subjects, we found previously-overlooked virus-derived SVs. We detected non-germline SVs derived from squirrel monkey retrovirus (SMRV), human immunodeficiency virus 1 (HIV-1), and human T lymphotropic virus (HTLV-1); these variants are attributable to infection of the sequenced lymphoblastoid cell lines (LCLs) or their progenitor cells and may impact gene expression results and the biosafety of experiments using these cells. In addition, we detected new heritable SVs derived from human herpesvirus 6 (HHV-6) and human endogenous retrovirus-K (HERV-K). We report the first solo-direct repeat (DR) HHV-6 likely to reflect DR rearrangement of a known full-length endogenous HHV-6. We used linkage disequilibrium between single nucleotide variants (SNVs) and variants in reads that align to HERV-K, which often cannot be mapped uniquely using conventional short-read sequencing analysis methods, to locate previously-unknown polymorphic HERV-K loci. Some of these loci are tightly linked to trait-associated SNVs, some are in complex genome regions inaccessible by prior methods, and some contain novel HERV-K haplotypes likely derived from gene conversion from an unknown source or introgression. These tools and results broaden our perspective on the coevolution between viruses and humans, including ongoing virus-to-human gene transfer contributing to genetic variation between humans. The sequences that make up each person’s genome have diverse origin stories. For example, some people’s genomes include fragments of chromosomes originating from Neanderthals. Variation in the genes in these chromosomal fragments may be associated with observable differences between people. Human genomes also include sequences originating from viruses, but the extent to which these sequences vary in different humans is unknown. We studied virus-derived variation in thousands of human genomes using new tools made for this purpose. In the process, we uncovered virus infection in cell lines used as reference materials for human genome variation. We also found rare germline variants originating from acquisition of human herpesvirus 6, as well as more extensive variation in human endogenous retroviruses than has previously been described. This work expands the toolbox for studying the intriguing class of virus-derived genetic variants in human genomes.
Acquisition of genetic material from viruses by their hosts can generate inter-host structural genome variation. We developed computational tools enabling us to study virus-derived structural variants (SVs) in population-scale whole genome sequencing (WGS) datasets and applied them to 3,332 humans. Although SVs had already been cataloged in these subjects, we found previously-overlooked virus-derived SVs. We detected non-germline SVs derived from squirrel monkey retrovirus (SMRV), human immunodeficiency virus 1 (HIV-1), and human T lymphotropic virus (HTLV-1); these variants are attributable to infection of the sequenced lymphoblastoid cell lines (LCLs) or their progenitor cells and may impact gene expression results and the biosafety of experiments using these cells. In addition, we detected new heritable SVs derived from human herpesvirus 6 (HHV-6) and human endogenous retrovirus-K (HERV-K). We report the first solo-direct repeat (DR) HHV-6 likely to reflect DR rearrangement of a known full-length endogenous HHV-6. We used linkage disequilibrium between single nucleotide variants (SNVs) and variants in reads that align to HERV-K, which often cannot be mapped uniquely using conventional short-read sequencing analysis methods, to locate previously-unknown polymorphic HERV-K loci. Some of these loci are tightly linked to trait-associated SNVs, some are in complex genome regions inaccessible by prior methods, and some contain novel HERV-K haplotypes likely derived from gene conversion from an unknown source or introgression. These tools and results broaden our perspective on the coevolution between viruses and humans, including ongoing virus-to-human gene transfer contributing to genetic variation between humans.Acquisition of genetic material from viruses by their hosts can generate inter-host structural genome variation. We developed computational tools enabling us to study virus-derived structural variants (SVs) in population-scale whole genome sequencing (WGS) datasets and applied them to 3,332 humans. Although SVs had already been cataloged in these subjects, we found previously-overlooked virus-derived SVs. We detected non-germline SVs derived from squirrel monkey retrovirus (SMRV), human immunodeficiency virus 1 (HIV-1), and human T lymphotropic virus (HTLV-1); these variants are attributable to infection of the sequenced lymphoblastoid cell lines (LCLs) or their progenitor cells and may impact gene expression results and the biosafety of experiments using these cells. In addition, we detected new heritable SVs derived from human herpesvirus 6 (HHV-6) and human endogenous retrovirus-K (HERV-K). We report the first solo-direct repeat (DR) HHV-6 likely to reflect DR rearrangement of a known full-length endogenous HHV-6. We used linkage disequilibrium between single nucleotide variants (SNVs) and variants in reads that align to HERV-K, which often cannot be mapped uniquely using conventional short-read sequencing analysis methods, to locate previously-unknown polymorphic HERV-K loci. Some of these loci are tightly linked to trait-associated SNVs, some are in complex genome regions inaccessible by prior methods, and some contain novel HERV-K haplotypes likely derived from gene conversion from an unknown source or introgression. These tools and results broaden our perspective on the coevolution between viruses and humans, including ongoing virus-to-human gene transfer contributing to genetic variation between humans.
[...]about 8% of human genetic material is derived from human endogenous retroviruses (HERV) that entered the human genetic lineage via retroviral infection of the germline, and subsequently developed transposon-like intracellular replication cycles; some HERVs integrated recently enough that they can be classified based on homology to extant exogenous retroviruses. Results Detection of virus-mapped reads from diverse human populations To discover human structural variation derived from viral sequences, we analyzed WGS reads that failed to map to the reference human genome (GRCh38DH). All reads lack a guanosine in the tRNA primer binding site (PBS) relative to SMRV-H, which was isolated from macaque cells used to derive preparations of Epstein Barr virus (EBV) [22]; the tRNA PBS of the SMRV detected here is identical to SMRV sequences recently obtained from Vero cells [23], a cell line used for biologicals production (Fig 2A) [24]. [...]to assess whether these presumed SMRV integrations occurred before or after the peripheral blood mononuclear cells (PBMCs) used to produce LCLs were removed from these subjects, we analyzed sequencing results obtained directly from these subject’s nucleated blood cells [25,26].
[...]about 8% of human genetic material is derived from human endogenous retroviruses (HERV) that entered the human genetic lineage via retroviral infection of the germline, and subsequently developed transposon-like intracellular replication cycles; some HERVs integrated recently enough that they can be classified based on homology to extant exogenous retroviruses. Results Detection of virus-mapped reads from diverse human populations To discover human structural variation derived from viral sequences, we analyzed WGS reads that failed to map to the reference human genome (GRCh38DH). All reads lack a guanosine in the tRNA primer binding site (PBS) relative to SMRV-H, which was isolated from macaque cells used to derive preparations of Epstein Barr virus (EBV) [22]; the tRNA PBS of the SMRV detected here is identical to SMRV sequences recently obtained from Vero cells [23], a cell line used for biologicals production (Fig 2A) [24]. [...]to assess whether these presumed SMRV integrations occurred before or after the peripheral blood mononuclear cells (PBMCs) used to produce LCLs were removed from these subjects, we analyzed sequencing results obtained directly from these subject’s nucleated blood cells [25,26].
Audience Academic
Author Kamada, Anselmo Jiro
Kojima, Shohei
Parrish, Nicholas F.
AuthorAffiliation Cornell University, UNITED STATES
Genome Immunobiology RIKEN Hakubi Research Team, RIKEN Center for Integrative Medical Sciences and RIKEN Cluster for Pioneering Research, Yokohama, Japan
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33901175$$D View this record in MEDLINE/PubMed
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CitedBy_id crossref_primary_10_17803_lexgen_2022_1_1_20_33
crossref_primary_10_1038_s41598_024_65386_6
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Snippet Acquisition of genetic material from viruses by their hosts can generate inter-host structural genome variation. We developed computational tools enabling us...
[...]about 8% of human genetic material is derived from human endogenous retroviruses (HERV) that entered the human genetic lineage via retroviral infection of...
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StartPage e1009324
SubjectTerms Binding sites
Biology and Life Sciences
Blood cells
Chromosomes
Computer and Information Sciences
Datasets
Epstein-Barr virus
Gene expression
Genetic aspects
Genetic research
Genetic variation
Genomes
HIV
Homology
Host-virus relationships
Human genome
Human immunodeficiency virus
Leukocytes (mononuclear)
Medicine and Health Sciences
Peripheral blood mononuclear cells
Reference materials
Research and Analysis Methods
tRNA
Vero cells
Viruses
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Title Virus-derived variation in diverse human genomes
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http://dx.doi.org/10.1371/journal.pgen.1009324
Volume 17
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