Yongtao Ye, Marcus H Shum, Isaac Wu, Carlos Chau, Ningqi Zhao, David K Smith, Joseph T Wu, Tommy T Lam
The unprecedentedly large size of the global SARS-CoV-2 phylogeny makes any computation on the tree difficult. Lineage identification (e.g. the PANGO nomenclature for SARS-CoV-2) and assignment are key to track the virus evolution. It requires annotating clade roots of lineages to unlabeled ancestral nodes in a phylogenetic tree. Then the lineage labels of descendant samples under these clade roots can be inferred to be the corresponding lineages. This is the ancestral lineage annotation problem, and matUtils (a package in pUShER) and PastML are commonly used methods. However, their computational tractability is a challenge and their accuracy needs further exploration in huge SARS-CoV-2 phylogenies. We have developed an efficient and accurate method, called ‘F1ALA’, that utilizes the F1-score to evaluate the confidence with which a specific ancestral node can be annotated as the clade root of a lineage, given the lineage labels of a set of taxa in a rooted tree. Compared to these methods, F1ALA achieved roughly an order of magnitude faster yet with ~12% of their memory usage when annotating 2,277 PANGO lineages in a phylogeny of 5.26 million taxa. F1ALA allows real-time lineage tracking be performed on a laptop computer. F1ALA outperformed matUtils (pUShER) with statistical significance, and had comparable accuracy to PastML in tests on empirical and simulated data. F1ALA enables a tree refinement by pruning taxa with inconsistent labels to their closest annotation nodes and re-inserting them back to the pruned tree to improve a SARS-CoV-2 phylogeny with both higher log-likelihood and lower parsimony score. Given the ultrafast speed and high accuracy, we anticipated that F1ALA will also be useful for large phylogenies of other viruses. Codes and benchmark datasets are publicly available at https://github.com/id-bioinfo/F1ALA.
{"title":"F1ALA: ultrafast and memory-efficient ancestral lineage annotation applied to the huge SARS-CoV-2 phylogeny","authors":"Yongtao Ye, Marcus H Shum, Isaac Wu, Carlos Chau, Ningqi Zhao, David K Smith, Joseph T Wu, Tommy T Lam","doi":"10.1093/ve/veae056","DOIUrl":"https://doi.org/10.1093/ve/veae056","url":null,"abstract":"The unprecedentedly large size of the global SARS-CoV-2 phylogeny makes any computation on the tree difficult. Lineage identification (e.g. the PANGO nomenclature for SARS-CoV-2) and assignment are key to track the virus evolution. It requires annotating clade roots of lineages to unlabeled ancestral nodes in a phylogenetic tree. Then the lineage labels of descendant samples under these clade roots can be inferred to be the corresponding lineages. This is the ancestral lineage annotation problem, and matUtils (a package in pUShER) and PastML are commonly used methods. However, their computational tractability is a challenge and their accuracy needs further exploration in huge SARS-CoV-2 phylogenies. We have developed an efficient and accurate method, called ‘F1ALA’, that utilizes the F1-score to evaluate the confidence with which a specific ancestral node can be annotated as the clade root of a lineage, given the lineage labels of a set of taxa in a rooted tree. Compared to these methods, F1ALA achieved roughly an order of magnitude faster yet with ~12% of their memory usage when annotating 2,277 PANGO lineages in a phylogeny of 5.26 million taxa. F1ALA allows real-time lineage tracking be performed on a laptop computer. F1ALA outperformed matUtils (pUShER) with statistical significance, and had comparable accuracy to PastML in tests on empirical and simulated data. F1ALA enables a tree refinement by pruning taxa with inconsistent labels to their closest annotation nodes and re-inserting them back to the pruned tree to improve a SARS-CoV-2 phylogeny with both higher log-likelihood and lower parsimony score. Given the ultrafast speed and high accuracy, we anticipated that F1ALA will also be useful for large phylogenies of other viruses. Codes and benchmark datasets are publicly available at https://github.com/id-bioinfo/F1ALA.","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"34 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2024-07-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141770464","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Negative sense RNA viruses (NSV) include some of the most detrimental human pathogens, including the influenza, Ebola and measles viruses. NSV genomes consist of one or multiple single-stranded RNA molecules that are encapsidated into one or more ribonucleoprotein (RNP) complexes. These RNPs consist of viral RNA, a viral RNA polymerase, and many copies of the viral nucleoprotein (NP). Current evolutionary relationships within the NSV phylum are based on alignment of conserved RNA-directed RNA polymerase (RdRp) domain amino acid sequences. However, the RdRp domain-based phylogeny does not address whether NP, the other core protein in the NSV genome, evolved along the same trajectory or whether several RdRp-NP pairs evolved through convergent evolution in the segmented and non-segmented NSV genomes architectures. Addressing how NP and the RdRp domain evolved may help us better understand NSV diversity. Since NP sequences are too short to infer robust phylogenetic relationships, we here used experimentally-obtained and AlphaFold 2.0-predicted NP structures to probe whether evolutionary relationships can be estimated using NSV NP sequences. Following flexible structure alignments of modeled structures, we find that the structural homology of the NSV NPs reveals phylogenetic clusters that are consistent with RdRp-based clustering. In addition, we were able to assign viruses for which RdRp sequences are currently missing to phylogenetic clusters based on the available NP sequence. Both our RdRp-based and NP-based relationships deviate from the current NSV classification of the segmented Naedrevirales, which cluster with the other segmented NSVs in our analysis. Overall, our results suggest that the NSV RdRp and NP genes largely evolved along similar trajectories and that even short pieces of genetic, protein-coding information can be used to infer evolutionary relationships, potentially making metagenomic analyses more valuable.
负感 RNA 病毒(NSV)包括一些对人类危害最大的病原体,如流感病毒、埃博拉病毒和麻疹病毒。NSV 基因组由一个或多个单链 RNA 分子组成,这些分子被封装成一个或多个核糖核蛋白(RNP)复合物。这些 RNP 由病毒 RNA、病毒 RNA 聚合酶和多个病毒核蛋白(NP)拷贝组成。目前,NSV 门内的进化关系是基于保守的 RNA 定向 RNA 聚合酶(RdRp)结构域氨基酸序列的比对。然而,基于 RdRp 结构域的系统发育并没有解决 NSV 基因组中的另一个核心蛋白 NP 是否沿着相同的轨迹进化,或者在分节和非分节的 NSV 基因组结构中,是否有几对 RdRp-NP 通过趋同进化而进化。解决 NP 和 RdRp 结构域如何进化的问题有助于我们更好地理解 NSV 的多样性。由于 NP 序列太短,无法推断出可靠的系统发育关系,因此我们在此使用实验获得的和 AlphaFold 2.0 预测的 NP 结构来探究是否可以使用 NSV NP 序列来估计进化关系。通过对模型结构进行灵活的结构比对,我们发现 NSV NP 的结构同源性揭示了与基于 RdRp 的聚类一致的系统发生群。此外,我们还能根据现有的 NP 序列将目前缺少 RdRp 序列的病毒归入系统发生群。基于 RdRp 和基于 NP 的关系都偏离了目前对分段 Naedrevirales 的 NSV 分类,在我们的分析中,Naedrevirales 与其他分段 NSV 聚类在一起。总之,我们的结果表明,NSV RdRp 和 NP 基因在很大程度上是沿着相似的轨迹进化的,即使是很短的基因、蛋白质编码信息也可以用来推断进化关系,从而可能使元基因组分析更有价值。
{"title":"Using structure prediction of negative sense RNA virus nucleoproteins to assess evolutionary relationships","authors":"Kimberly R Sabsay, te Velthuis Aartjan J.W","doi":"10.1093/ve/veae058","DOIUrl":"https://doi.org/10.1093/ve/veae058","url":null,"abstract":"Negative sense RNA viruses (NSV) include some of the most detrimental human pathogens, including the influenza, Ebola and measles viruses. NSV genomes consist of one or multiple single-stranded RNA molecules that are encapsidated into one or more ribonucleoprotein (RNP) complexes. These RNPs consist of viral RNA, a viral RNA polymerase, and many copies of the viral nucleoprotein (NP). Current evolutionary relationships within the NSV phylum are based on alignment of conserved RNA-directed RNA polymerase (RdRp) domain amino acid sequences. However, the RdRp domain-based phylogeny does not address whether NP, the other core protein in the NSV genome, evolved along the same trajectory or whether several RdRp-NP pairs evolved through convergent evolution in the segmented and non-segmented NSV genomes architectures. Addressing how NP and the RdRp domain evolved may help us better understand NSV diversity. Since NP sequences are too short to infer robust phylogenetic relationships, we here used experimentally-obtained and AlphaFold 2.0-predicted NP structures to probe whether evolutionary relationships can be estimated using NSV NP sequences. Following flexible structure alignments of modeled structures, we find that the structural homology of the NSV NPs reveals phylogenetic clusters that are consistent with RdRp-based clustering. In addition, we were able to assign viruses for which RdRp sequences are currently missing to phylogenetic clusters based on the available NP sequence. Both our RdRp-based and NP-based relationships deviate from the current NSV classification of the segmented Naedrevirales, which cluster with the other segmented NSVs in our analysis. Overall, our results suggest that the NSV RdRp and NP genes largely evolved along similar trajectories and that even short pieces of genetic, protein-coding information can be used to infer evolutionary relationships, potentially making metagenomic analyses more valuable.","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"20 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2024-07-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141770465","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-18eCollection Date: 2024-01-01DOI: 10.1093/ve/veae052
[This corrects the article DOI: 10.1093/ve/vead084.].
[此处更正了文章 DOI:10.1093/ve/vead084]。
{"title":"Correction to: Human immunodeficiency virus dynamics in secondary lymphoid tissues and the evolution of cytotoxic T lymphocyte escape mutants.","authors":"","doi":"10.1093/ve/veae052","DOIUrl":"https://doi.org/10.1093/ve/veae052","url":null,"abstract":"<p><p>[This corrects the article DOI: 10.1093/ve/vead084.].</p>","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"10 1","pages":"veae052"},"PeriodicalIF":5.5,"publicationDate":"2024-07-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11259755/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141735787","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Dongbin Park, Kwan Woo Kim, Young-Il Kim, Mark Anthony B Casel, Hyunwoo Jang, Woohyun Kwon, Kanghee Kim, Se-Mi Kim, Monford Paul Abishek N, Eun-Ha Kim, Hobin Jang, Suhee Hwang, Seok-Min Yun, Joo-Yeon Lee, Hye Won Jeong, Su-Jin Park, Young Ki Choi
The Severe Fever with Thrombocytopenia Syndrome Virus (SFTSV) poses a significant public health challenge in East Asia, necessitating a deeper understanding of its evolutionary dynamics to effectively manage its spread and pathogenicity. This study provides a comprehensive analysis of the genetic diversity, recombination patterns, and selection pressures across the SFTSV genome, utilizing an extensive dataset of 2,041 sequences from various hosts and regions up to November 2023. Employing Maximum Likelihood (ML) and Bayesian Evolutionary Analysis (BEAST), we elucidated the phylogenetic relationships among nine distinct SFTSV genotypes (A, B1, B2, B3, B4, C, D, E, and F), revealing intricate patterns of viral evolution and genotype distribution across China, South Korea, and Japan. Further, our analysis identified 34 potential reassortments, underscoring a dynamic genetic interplay among SFTSV strains. Genetic recombination was observed most frequently in the L segment and least in the S segment, with notable recombination hotspots characterized by stem-loop hairpin structures, indicative of a structural propensity for genetic recombination. Additionally, selection pressure analysis on critical viral genes indicated a predominant trend of negative selection, with specific sites within the RdRp and glycoprotein genes showing positive selection. These sites suggest evolutionary adaptations to host immune responses and environmental pressures. This study sheds light on the intricate evolutionary mechanisms shaping SFTSV, offering insights into its adaptive strategies and potential implications for vaccine development and therapeutic interventions.
严重发热伴血小板减少综合征病毒(SFTSV)对东亚地区的公共卫生构成了重大挑战,因此有必要深入了解其进化动态,以有效控制其传播和致病性。本研究利用截至2023年11月来自不同宿主和地区的2041个序列的广泛数据集,对SFTSV基因组的遗传多样性、重组模式和选择压力进行了全面分析。利用最大似然法(ML)和贝叶斯进化分析法(BEAST),我们阐明了九种不同的SFTSV基因型(A、B1、B2、B3、B4、C、D、E和F)之间的系统发育关系,揭示了病毒进化的复杂模式以及基因型在中国、韩国和日本的分布。此外,我们的分析还发现了 34 个潜在的基因重组,突显了 SFTSV 株系间动态的基因相互作用。基因重组在 L 段最常见,在 S 段最少,显著的重组热点以茎环发夹结构为特征,表明了基因重组的结构倾向。此外,对关键病毒基因的选择压力分析表明,主要趋势是负选择,RdRp 和糖蛋白基因中的特定位点显示出正选择。这些位点表明病毒在进化过程中适应了宿主的免疫反应和环境压力。这项研究揭示了形成 SFTSV 的复杂进化机制,有助于深入了解其适应策略以及对疫苗开发和治疗干预的潜在影响。
{"title":"Deciphering the Evolutionary Landscape of Severe Fever with Thrombocytopenia Syndrome Virus Across East Asia","authors":"Dongbin Park, Kwan Woo Kim, Young-Il Kim, Mark Anthony B Casel, Hyunwoo Jang, Woohyun Kwon, Kanghee Kim, Se-Mi Kim, Monford Paul Abishek N, Eun-Ha Kim, Hobin Jang, Suhee Hwang, Seok-Min Yun, Joo-Yeon Lee, Hye Won Jeong, Su-Jin Park, Young Ki Choi","doi":"10.1093/ve/veae054","DOIUrl":"https://doi.org/10.1093/ve/veae054","url":null,"abstract":"The Severe Fever with Thrombocytopenia Syndrome Virus (SFTSV) poses a significant public health challenge in East Asia, necessitating a deeper understanding of its evolutionary dynamics to effectively manage its spread and pathogenicity. This study provides a comprehensive analysis of the genetic diversity, recombination patterns, and selection pressures across the SFTSV genome, utilizing an extensive dataset of 2,041 sequences from various hosts and regions up to November 2023. Employing Maximum Likelihood (ML) and Bayesian Evolutionary Analysis (BEAST), we elucidated the phylogenetic relationships among nine distinct SFTSV genotypes (A, B1, B2, B3, B4, C, D, E, and F), revealing intricate patterns of viral evolution and genotype distribution across China, South Korea, and Japan. Further, our analysis identified 34 potential reassortments, underscoring a dynamic genetic interplay among SFTSV strains. Genetic recombination was observed most frequently in the L segment and least in the S segment, with notable recombination hotspots characterized by stem-loop hairpin structures, indicative of a structural propensity for genetic recombination. Additionally, selection pressure analysis on critical viral genes indicated a predominant trend of negative selection, with specific sites within the RdRp and glycoprotein genes showing positive selection. These sites suggest evolutionary adaptations to host immune responses and environmental pressures. This study sheds light on the intricate evolutionary mechanisms shaping SFTSV, offering insights into its adaptive strategies and potential implications for vaccine development and therapeutic interventions.","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"93 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2024-07-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141745154","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
José L Carrasco, Silvia Ambrós, Pablo A Gutiérrez, Santiago F Elena
The outcome of a viral infection depends on a complex interplay between the host physiology and the virus, mediated through numerous protein-protein interactions. In a previous study, we used high-throughput yeast two-hybrid (HT-Y2H) to identify proteins in Arabidopsis thaliana that bind to the proteins encoded by the turnip mosaic virus (TuMV) genome. Furthermore, after experimental evolution of TuMV lineages in plants with mutations in defense-related or proviral genes, most mutations observed in the evolved viruses affected the VPg cistron. Among these mutations, D113G was a convergent mutation selected in many lineages across different plant genotypes, including cpr5-2 with constitutive expression of systemic acquired resistance. In contrast, mutation R118H specifically emerged in the jin1 mutant with affected jasmonate signaling. Using the HT-Y2H system, we analyzed the impact of these two mutations on VPg’s interaction with plant proteins. Interestingly, both mutations severely compromised the interaction of VPg with the translation initiation factor eIF(iso)4E, a crucial interactor for potyvirus infection. Moreover, mutation D113G, but not R118H, adversely affected the interaction with RHD1, a zinc-finger homeodomain transcription factor involved in regulating DNA demethylation. Our results suggest that RHD1 enhances plant tolerance to TuMV infection. We also discuss our findings in a broad virus evolution context.
{"title":"Adaptation of turnip mosaic virus to Arabidopsis thaliana involves rewiring of VPg - host proteome interactions","authors":"José L Carrasco, Silvia Ambrós, Pablo A Gutiérrez, Santiago F Elena","doi":"10.1093/ve/veae055","DOIUrl":"https://doi.org/10.1093/ve/veae055","url":null,"abstract":"The outcome of a viral infection depends on a complex interplay between the host physiology and the virus, mediated through numerous protein-protein interactions. In a previous study, we used high-throughput yeast two-hybrid (HT-Y2H) to identify proteins in Arabidopsis thaliana that bind to the proteins encoded by the turnip mosaic virus (TuMV) genome. Furthermore, after experimental evolution of TuMV lineages in plants with mutations in defense-related or proviral genes, most mutations observed in the evolved viruses affected the VPg cistron. Among these mutations, D113G was a convergent mutation selected in many lineages across different plant genotypes, including cpr5-2 with constitutive expression of systemic acquired resistance. In contrast, mutation R118H specifically emerged in the jin1 mutant with affected jasmonate signaling. Using the HT-Y2H system, we analyzed the impact of these two mutations on VPg’s interaction with plant proteins. Interestingly, both mutations severely compromised the interaction of VPg with the translation initiation factor eIF(iso)4E, a crucial interactor for potyvirus infection. Moreover, mutation D113G, but not R118H, adversely affected the interaction with RHD1, a zinc-finger homeodomain transcription factor involved in regulating DNA demethylation. Our results suggest that RHD1 enhances plant tolerance to TuMV infection. We also discuss our findings in a broad virus evolution context.","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"61 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2024-07-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141718825","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Zachary K Barth, Ian Hicklin, Julien Thézé, Jun Takatsuka, Madoka Nakai, Elisabeth A Herniou, Anne M Brown, Frank O Aylward
Polinton-like viruses (PLVs) are a diverse group of small integrative dsDNA viruses that infect diverse eukaryotic hosts. Many PLVs are hypothesized to parasitize viruses in the phylum Nucleocytoviricota for their own propagation and spread. Here we analyze the genomes of novel PLVs associated with the occlusion bodies of entomopoxvirus (EV) infections of two separate lepidopteran hosts. The presence of these elements within EV occlusion bodies suggests that they are the first known hyperparasites of poxviruses. We find that these PLVs belong to two distinct lineages that are highly diverged from known PLVs. These PLVs possess mosaic genomes, and some essential genes share homology with mobile genes within EVs. Based on this homology and observed PLV mosaicism, we propose a mechanism to explain the turnover of PLV replication and integration genes.
{"title":"Genomic analysis of hyperparasitic viruses associated with entomopoxviruses","authors":"Zachary K Barth, Ian Hicklin, Julien Thézé, Jun Takatsuka, Madoka Nakai, Elisabeth A Herniou, Anne M Brown, Frank O Aylward","doi":"10.1093/ve/veae051","DOIUrl":"https://doi.org/10.1093/ve/veae051","url":null,"abstract":"Polinton-like viruses (PLVs) are a diverse group of small integrative dsDNA viruses that infect diverse eukaryotic hosts. Many PLVs are hypothesized to parasitize viruses in the phylum Nucleocytoviricota for their own propagation and spread. Here we analyze the genomes of novel PLVs associated with the occlusion bodies of entomopoxvirus (EV) infections of two separate lepidopteran hosts. The presence of these elements within EV occlusion bodies suggests that they are the first known hyperparasites of poxviruses. We find that these PLVs belong to two distinct lineages that are highly diverged from known PLVs. These PLVs possess mosaic genomes, and some essential genes share homology with mobile genes within EVs. Based on this homology and observed PLV mosaicism, we propose a mechanism to explain the turnover of PLV replication and integration genes.","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"18 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2024-07-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141609612","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ana R Lopes, Matthew Low, Raquel Martín-Hernández, M Alice Pinto, Joachim R de Miranda
Deformed wing virus (DWV) is a honey bee virus, whose emergence from relative obscurity is driven by the recent host-switch, adaptation and global dispersal of the ectoparasitic mite Varroa destructor (a highly efficient vector of DWV) to reproduction on honey bees (Apis mellifera). Our study examines how varroa affects the continuing evolution of DWV, using the Azores archipelago, where varroa is only present on only three out of the eight islands, as a natural experimental system for comparing different evolutionary conditions and trajectories. We combined qPCR of 494 honey bee colonies sampled across the archipelago with amplicon deep sequencing to reveal how the DWV genetic landscape is altered by varroa. Two of the varroa-free islands were also free of DWV, while a further two islands were intriguingly dominated by the rare DWV-C major variant. The other four islands, including the three varroa-infested islands, were dominated by the common DWV-A and DWV-B variants. The varroa-infested islands had, as expected, an elevated DWV prevalence relative to the uninfested islands, but not elevated DWV loads, due the relatively high prevalence and loads of DWV-C on the varroa-free islands. This establishes the Azores as a stable refuge for DWV-C and provides the most convincing evidence to date that at least some major strains of DWV may be capable of not just surviving, but actually thriving in honey bees in the absence of varroa-mediated transmission. We did not detect any change in DWV genetic diversity associated with island varroa status but did find a positive association of DWV diversity with virus load, irrespective of island varroa status.
{"title":"Origins, diversity, and adaptive evolution of DWV in the honey bees of the Azores: the impact of the invasive mite Varroa destructor","authors":"Ana R Lopes, Matthew Low, Raquel Martín-Hernández, M Alice Pinto, Joachim R de Miranda","doi":"10.1093/ve/veae053","DOIUrl":"https://doi.org/10.1093/ve/veae053","url":null,"abstract":"Deformed wing virus (DWV) is a honey bee virus, whose emergence from relative obscurity is driven by the recent host-switch, adaptation and global dispersal of the ectoparasitic mite Varroa destructor (a highly efficient vector of DWV) to reproduction on honey bees (Apis mellifera). Our study examines how varroa affects the continuing evolution of DWV, using the Azores archipelago, where varroa is only present on only three out of the eight islands, as a natural experimental system for comparing different evolutionary conditions and trajectories. We combined qPCR of 494 honey bee colonies sampled across the archipelago with amplicon deep sequencing to reveal how the DWV genetic landscape is altered by varroa. Two of the varroa-free islands were also free of DWV, while a further two islands were intriguingly dominated by the rare DWV-C major variant. The other four islands, including the three varroa-infested islands, were dominated by the common DWV-A and DWV-B variants. The varroa-infested islands had, as expected, an elevated DWV prevalence relative to the uninfested islands, but not elevated DWV loads, due the relatively high prevalence and loads of DWV-C on the varroa-free islands. This establishes the Azores as a stable refuge for DWV-C and provides the most convincing evidence to date that at least some major strains of DWV may be capable of not just surviving, but actually thriving in honey bees in the absence of varroa-mediated transmission. We did not detect any change in DWV genetic diversity associated with island varroa status but did find a positive association of DWV diversity with virus load, irrespective of island varroa status.","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"28 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2024-07-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141718826","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Krista R Gerbino, Joshua M Borin, Sarah M Ardell, Justin J Lee, Kevin D Corbett, Justin R Meyer
How viruses evolve to expand their host range is a major question with implications for predicting the next pandemic. Gain-of-function experiments have revealed that host-range expansions can occur through relatively few mutations in viral receptor-binding proteins, and the search for molecular mechanisms that explain such expansions are underway. Previous research on expansions of receptor use in bacteriophage λ has shown that mutations that destabilize λ’s receptor-binding protein cause it to fold into new conformations that can utilize novel receptors but have weakened thermostability. These observations led us to hypothesize that other viruses may take similar paths to expand their host range. Here, we find support for our hypothesis by studying another virus, bacteriophage 21 (Φ21), which evolves to use two new host receptors within two weeks of laboratory evolution. By measuring the thermodynamic stability of Φ21 and its descendants, we show that as Φ21 evolves to use new receptors and expands its host range, it becomes less stable and produces viral particles that are genetically identical but vary in their thermostabilities. Next, we show that this non-genetic heterogeneity between particles is directly associated with receptor use innovation, as phage particles with more derived receptor-use capabilities are more unstable and decay faster. Lastly, by manipulating the expression of protein chaperones during Φ21 infection, we demonstrate that heterogeneity in receptor use of phage particles arises during protein folding. Altogether, our results provide support for the hypothesis that viruses can evolve new receptor-use tropisms through mutations that destabilize the receptor-binding protein and produce multiple protein conformers.
{"title":"Bacteriophage Φ21’s receptor-binding protein evolves new functions through destabilizing mutations that generate non-genetic phenotypic heterogeneity","authors":"Krista R Gerbino, Joshua M Borin, Sarah M Ardell, Justin J Lee, Kevin D Corbett, Justin R Meyer","doi":"10.1093/ve/veae049","DOIUrl":"https://doi.org/10.1093/ve/veae049","url":null,"abstract":"How viruses evolve to expand their host range is a major question with implications for predicting the next pandemic. Gain-of-function experiments have revealed that host-range expansions can occur through relatively few mutations in viral receptor-binding proteins, and the search for molecular mechanisms that explain such expansions are underway. Previous research on expansions of receptor use in bacteriophage λ has shown that mutations that destabilize λ’s receptor-binding protein cause it to fold into new conformations that can utilize novel receptors but have weakened thermostability. These observations led us to hypothesize that other viruses may take similar paths to expand their host range. Here, we find support for our hypothesis by studying another virus, bacteriophage 21 (Φ21), which evolves to use two new host receptors within two weeks of laboratory evolution. By measuring the thermodynamic stability of Φ21 and its descendants, we show that as Φ21 evolves to use new receptors and expands its host range, it becomes less stable and produces viral particles that are genetically identical but vary in their thermostabilities. Next, we show that this non-genetic heterogeneity between particles is directly associated with receptor use innovation, as phage particles with more derived receptor-use capabilities are more unstable and decay faster. Lastly, by manipulating the expression of protein chaperones during Φ21 infection, we demonstrate that heterogeneity in receptor use of phage particles arises during protein folding. Altogether, our results provide support for the hypothesis that viruses can evolve new receptor-use tropisms through mutations that destabilize the receptor-binding protein and produce multiple protein conformers.","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"51 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2024-07-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141609691","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Rebecca M Grimwood, Stephanie J Waller, Janelle R Wierenga, Lauren Lim, Jeremy Dubrulle, Edward C Holmes, Jemma L Geoghegan
Antarctica harbours some of the most isolated and extreme environments on Earth, concealing a largely unexplored and unique component of the global animal virosphere. To understand the diversity and evolutionary histories of viruses in these polar species we determined the viromes of gill metatranscriptomes from 11 Antarctic fish species with 248 samples collected from the Ross Sea region spanning the Perciformes, Gadiformes, and Scorpaeniformes orders. The continent’s shift southward and cooling temperatures over 20 million years ago led to a reduction in biodiversity and subsequent radiation of some marine fauna, such as the notothenioid fishes. Despite decreased host species richness in polar regions, we revealed a surprisingly complex virome diversity in Ross Sea fish, with the types and numbers of viruses per host species and individuals sampled comparable to that of fish in warmer marine environments with higher host community diversity. We also observed a higher number of closely related viruses likely representing instances of recent and historic host-switching events among the Perciformes (all notothenioids) than in the Gadiformes, suggesting that rapid speciation events within this order generated closely related host species with few genetic barriers to cross-species transmission. Additionally, we identified novel genomic variation in an arenavirus with a split nucleoprotein sequence containing a stable helical structure, indicating potential adaptation of viral proteins to extreme temperatures. These findings enhance our understanding of virus evolution and virus-host interactions in response to environmental shifts, especially in less diverse ecosystems more vulnerable to the impacts of anthropogenic and climate changes. Keywords: Antarctica; Ross Sea; fish, viromes; evolution; genomes
{"title":"Viromes of Antarctic fish resembles the diversity found at lower latitudes","authors":"Rebecca M Grimwood, Stephanie J Waller, Janelle R Wierenga, Lauren Lim, Jeremy Dubrulle, Edward C Holmes, Jemma L Geoghegan","doi":"10.1093/ve/veae050","DOIUrl":"https://doi.org/10.1093/ve/veae050","url":null,"abstract":"Antarctica harbours some of the most isolated and extreme environments on Earth, concealing a largely unexplored and unique component of the global animal virosphere. To understand the diversity and evolutionary histories of viruses in these polar species we determined the viromes of gill metatranscriptomes from 11 Antarctic fish species with 248 samples collected from the Ross Sea region spanning the Perciformes, Gadiformes, and Scorpaeniformes orders. The continent’s shift southward and cooling temperatures over 20 million years ago led to a reduction in biodiversity and subsequent radiation of some marine fauna, such as the notothenioid fishes. Despite decreased host species richness in polar regions, we revealed a surprisingly complex virome diversity in Ross Sea fish, with the types and numbers of viruses per host species and individuals sampled comparable to that of fish in warmer marine environments with higher host community diversity. We also observed a higher number of closely related viruses likely representing instances of recent and historic host-switching events among the Perciformes (all notothenioids) than in the Gadiformes, suggesting that rapid speciation events within this order generated closely related host species with few genetic barriers to cross-species transmission. Additionally, we identified novel genomic variation in an arenavirus with a split nucleoprotein sequence containing a stable helical structure, indicating potential adaptation of viral proteins to extreme temperatures. These findings enhance our understanding of virus evolution and virus-host interactions in response to environmental shifts, especially in less diverse ecosystems more vulnerable to the impacts of anthropogenic and climate changes. Keywords: Antarctica; Ross Sea; fish, viromes; evolution; genomes","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"57 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2024-07-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141609755","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-06-22eCollection Date: 2024-01-01DOI: 10.1093/ve/veae045
Thi Nguyen Hoa-Tran, Toyoko Nakagomi, Hung Manh Vu, Trang Thu Thi Nguyen, Anh Thi Hai Dao, Anh The Nguyen, Julie E Bines, Sarah Thomas, Varja Grabovac, Chikako Kataoka-Nakamura, Takemura Taichiro, Futoshi Hasebe, Toshio Kodama, Miho Kaneko, Huyen Thi Thanh Dang, Hong Thi Duong, Dang Duc Anh, Osamu Nakagomi
Animal rotaviruses A (RVAs) are considered the source of emerging, novel RVA strains that have the potential to cause global spread in humans. A case in point was the emergence of G8 bovine RVA consisting of the P[8] VP4 gene and the DS-1-like backbone genes that appeared to have jumped into humans recently. However, it was not well documented what evolutionary changes occurred on the animal RVA-derived genes during circulation in humans. Rotavirus surveillance in Vietnam found that DS-1-like G8P[8] strains emerged in 2014, circulated in two prevalent waves, and disappeared in 2021. This surveillance provided us with a unique opportunity to investigate the whole process of evolutionary changes, which occurred in an animal RVA that had jumped the host species barrier. Of the 843 G8P[8] samples collected from children with acute diarrhoea in Vietnam between 2014 and 2021, fifty-eight strains were selected based on their distinctive electropherotypes of the genomic RNA identified using polyacrylamide gel electrophoresis. Whole-genome sequence analysis of those fifty-eight strains showed that the strains dominant during the first wave of prevalence (2014-17) carried animal RVA-derived VP1, NSP2, and NSP4 genes. However, the strains from the second wave of prevalence (2018-21) lost these genes, which were replaced with cognate human RVA-derived genes, thus creating strain with G8P[8] on a fully DS-1-like human RVA gene backbone. The G8 VP7 and P[8] VP4 genes underwent some point mutations but the phylogenetic lineages to which they belonged remained unchanged. We, therefore, propose a hypothesis regarding the tendency for the animal RVA-derived genes to be expelled from the backbone genes of the progeny strains after crossing the host species barrier. This study underlines the importance of long-term surveillance of circulating wild-type strains in order to better understand the adaptation process and the fate of newly emerging, animal-derived RVA among the human population. Further studies are warranted to disclose the molecular mechanisms by which spillover animal RVAs become readily transmissible among humans, and the roles played by the expulsion of animal-derived genes and herd immunity formed in the local population.
{"title":"Evolution of DS-1-like G8P[8] rotavirus A strains from Vietnamese children with acute gastroenteritis (2014-21): Adaptation and loss of animal rotavirus-derived <i>genes</i> during human-to-human spread.","authors":"Thi Nguyen Hoa-Tran, Toyoko Nakagomi, Hung Manh Vu, Trang Thu Thi Nguyen, Anh Thi Hai Dao, Anh The Nguyen, Julie E Bines, Sarah Thomas, Varja Grabovac, Chikako Kataoka-Nakamura, Takemura Taichiro, Futoshi Hasebe, Toshio Kodama, Miho Kaneko, Huyen Thi Thanh Dang, Hong Thi Duong, Dang Duc Anh, Osamu Nakagomi","doi":"10.1093/ve/veae045","DOIUrl":"10.1093/ve/veae045","url":null,"abstract":"<p><p>Animal rotaviruses A (RVAs) are considered the source of emerging, novel RVA strains that have the potential to cause global spread in humans. A case in point was the emergence of G8 bovine RVA consisting of the P[8] VP4 <i>gene</i> and the DS-1-like backbone <i>genes</i> that appeared to have jumped into humans recently. However, it was not well documented what evolutionary changes occurred on the animal RVA-derived <i>genes</i> during circulation in humans. Rotavirus surveillance in Vietnam found that DS-1-like G8P[8] strains emerged in 2014, circulated in two prevalent waves, and disappeared in 2021. This surveillance provided us with a unique opportunity to investigate the whole process of evolutionary changes, which occurred in an animal RVA that had jumped the host species barrier. Of the 843 G8P[8] samples collected from children with acute diarrhoea in Vietnam between 2014 and 2021, fifty-eight strains were selected based on their distinctive electropherotypes of the genomic RNA identified using polyacrylamide gel electrophoresis. Whole-genome sequence analysis of those fifty-eight strains showed that the strains dominant during the first wave of prevalence (2014-17) carried animal RVA-derived VP1, NSP2, and NSP4 <i>genes</i>. However, the strains from the second wave of prevalence (2018-21) lost these <i>genes</i>, which were replaced with cognate human RVA-derived <i>genes</i>, thus creating strain with G8P[8] on a fully DS-1-like human RVA <i>gene</i> backbone. The G8 VP7 and P[8] VP4 <i>gene</i>s underwent some point mutations but the phylogenetic lineages to which they belonged remained unchanged. We, therefore, propose a hypothesis regarding the tendency for the animal RVA-derived <i>genes</i> to be expelled from the backbone <i>genes</i> of the progeny strains after crossing the host species barrier. This study underlines the importance of long-term surveillance of circulating wild-type strains in order to better understand the adaptation process and the fate of newly emerging, animal-derived RVA among the human population. Further studies are warranted to disclose the molecular mechanisms by which spillover animal RVAs become readily transmissible among humans, and the roles played by the expulsion of animal-derived <i>genes</i> and herd immunity formed in the local population.</p>","PeriodicalId":56026,"journal":{"name":"Virus Evolution","volume":"10 1","pages":"veae045"},"PeriodicalIF":5.5,"publicationDate":"2024-06-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11215986/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141478033","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}