Prevalence of Reversed Genome Organizations for Viruses in the Family Iflaviridae, Order Picornavirales

ABSTRACT Viruses in the order Picornavirales possess a positive-strand RNA genome that encodes structural proteins (SPs) and nonstructural proteins (NSPs). According to the recent report of the International Committee on Taxonomy of Viruses (ICTV), there are 8 families in Picornavirales, and monopar...

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Main Authors: Yan Zhang, Zhuang-Xin Ye, Xiao-Xiao Feng, Zhong-Tian Xu, Jian-Ping Chen, Chuan-Xi Zhang, Jun-Min Li
Format: Article
Language:English
Published: American Society for Microbiology 2023-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.04738-22
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author Yan Zhang
Zhuang-Xin Ye
Xiao-Xiao Feng
Zhong-Tian Xu
Jian-Ping Chen
Chuan-Xi Zhang
Jun-Min Li
author_facet Yan Zhang
Zhuang-Xin Ye
Xiao-Xiao Feng
Zhong-Tian Xu
Jian-Ping Chen
Chuan-Xi Zhang
Jun-Min Li
author_sort Yan Zhang
collection DOAJ
description ABSTRACT Viruses in the order Picornavirales possess a positive-strand RNA genome that encodes structural proteins (SPs) and nonstructural proteins (NSPs). According to the recent report of the International Committee on Taxonomy of Viruses (ICTV), there are 8 families in Picornavirales, and monopartite picornaviruses in each family exhibit distinct types of genome organizations with rearranged genes coding for SPs and NSPs, namely, TypeI (5′-SPs-NSPs-3′) and TypeII (5′-NSPs-SPs-3′). In the present study, 2 iflaviruses with the 2 genome types were unexpectedly identified in a damselfly host species, suggesting that these 2 genome types coexisted in the same host species, and the families of order Picornavirales might be more complex than previously thought. The consequent systematic homologous screening with all the publicly available picornaviruses successfully revealed a considerable number of candidates rearranged genome types of picornaviruses in various families of Picornavirales. Subsequently, phylogenetic trees were reconstructed based on RNA dependent RNA polymerase and coat protein, which evidently confirmed the prevalence of the 10 typeII iflaviruses in the Iflaviridae family. This suggests that genome types may not be relevant to viral taxonomy in this family. However, candidate picornaviruses with reversed genome types in the Secoviridae and Dicistroviridae families require further investigation. All in all, as the number of newly discovered viruses increases, more viruses with non-canonical genome arrangements will be uncovered, which can expand our current knowledge on the genome complexity and evolution of picornaviruses. IMPORTANCE Monopartite viruses in the order Picornavirales exhibit distinct genome arrangement of nonstructural proteins and structural proteins for each of the 8 families. Recent studies indicated that at least 4 ifla-like viruses possessed reversed genome organization in the family Iflaviridae, raising the possibility that this phenomenon may commonly present in different families of picornaviruses. Since we discovered 2 iflaviruses with exchanged structural and nonstructural proteins simultaneously in the damselfly, a systematic screening was subsequently performed for all of the current available picornaviruses (1,543 candidates). The results revealed 10 picornaviruses with reversed genome organization in the family Iflaviridae, implying that this phenomenon might prevalence in the order Picornavirales. These results will contribute to a better understanding for the future study on the genome complexity and taxonomy of picornaviruses.
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spelling doaj.art-ab55d20ae372444f8347bc25422f08c12023-06-15T13:18:33ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.04738-22Prevalence of Reversed Genome Organizations for Viruses in the Family Iflaviridae, Order PicornaviralesYan Zhang0Zhuang-Xin Ye1Xiao-Xiao Feng2Zhong-Tian Xu3Jian-Ping Chen4Chuan-Xi Zhang5Jun-Min Li6State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, ChinaAgricultural Experiment Station, Zhejiang University, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, ChinaABSTRACT Viruses in the order Picornavirales possess a positive-strand RNA genome that encodes structural proteins (SPs) and nonstructural proteins (NSPs). According to the recent report of the International Committee on Taxonomy of Viruses (ICTV), there are 8 families in Picornavirales, and monopartite picornaviruses in each family exhibit distinct types of genome organizations with rearranged genes coding for SPs and NSPs, namely, TypeI (5′-SPs-NSPs-3′) and TypeII (5′-NSPs-SPs-3′). In the present study, 2 iflaviruses with the 2 genome types were unexpectedly identified in a damselfly host species, suggesting that these 2 genome types coexisted in the same host species, and the families of order Picornavirales might be more complex than previously thought. The consequent systematic homologous screening with all the publicly available picornaviruses successfully revealed a considerable number of candidates rearranged genome types of picornaviruses in various families of Picornavirales. Subsequently, phylogenetic trees were reconstructed based on RNA dependent RNA polymerase and coat protein, which evidently confirmed the prevalence of the 10 typeII iflaviruses in the Iflaviridae family. This suggests that genome types may not be relevant to viral taxonomy in this family. However, candidate picornaviruses with reversed genome types in the Secoviridae and Dicistroviridae families require further investigation. All in all, as the number of newly discovered viruses increases, more viruses with non-canonical genome arrangements will be uncovered, which can expand our current knowledge on the genome complexity and evolution of picornaviruses. IMPORTANCE Monopartite viruses in the order Picornavirales exhibit distinct genome arrangement of nonstructural proteins and structural proteins for each of the 8 families. Recent studies indicated that at least 4 ifla-like viruses possessed reversed genome organization in the family Iflaviridae, raising the possibility that this phenomenon may commonly present in different families of picornaviruses. Since we discovered 2 iflaviruses with exchanged structural and nonstructural proteins simultaneously in the damselfly, a systematic screening was subsequently performed for all of the current available picornaviruses (1,543 candidates). The results revealed 10 picornaviruses with reversed genome organization in the family Iflaviridae, implying that this phenomenon might prevalence in the order Picornavirales. These results will contribute to a better understanding for the future study on the genome complexity and taxonomy of picornaviruses.https://journals.asm.org/doi/10.1128/spectrum.04738-22picornavirusiflavirusvirus taxonomyreversed genome organization
spellingShingle Yan Zhang
Zhuang-Xin Ye
Xiao-Xiao Feng
Zhong-Tian Xu
Jian-Ping Chen
Chuan-Xi Zhang
Jun-Min Li
Prevalence of Reversed Genome Organizations for Viruses in the Family Iflaviridae, Order Picornavirales
Microbiology Spectrum
picornavirus
iflavirus
virus taxonomy
reversed genome organization
title Prevalence of Reversed Genome Organizations for Viruses in the Family Iflaviridae, Order Picornavirales
title_full Prevalence of Reversed Genome Organizations for Viruses in the Family Iflaviridae, Order Picornavirales
title_fullStr Prevalence of Reversed Genome Organizations for Viruses in the Family Iflaviridae, Order Picornavirales
title_full_unstemmed Prevalence of Reversed Genome Organizations for Viruses in the Family Iflaviridae, Order Picornavirales
title_short Prevalence of Reversed Genome Organizations for Viruses in the Family Iflaviridae, Order Picornavirales
title_sort prevalence of reversed genome organizations for viruses in the family iflaviridae order picornavirales
topic picornavirus
iflavirus
virus taxonomy
reversed genome organization
url https://journals.asm.org/doi/10.1128/spectrum.04738-22
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