Virus diversity, wildlife-domestic animal circulation and potential zoonotic viruses of small mammals, pangolins and zoo animals.

Xinyuan Cui¹ Kewei Fan² Xianghui Liang¹ Wenjie Gong^3,4 Wu Chen⁵ Biao He⁴ Xiaoyuan Chen¹ Hai Wang¹ Xiao Wang¹ Ping Zhang¹ Xingbang Lu¹ Rujian Chen¹ Kaixiong Lin⁶ Jiameng Liu¹ Junqiong Zhai⁵ Ding Xiang Liu^7,8 Fen Shan⁵ Yuqi Li² Rui Ai Chen⁸ Huifang Meng¹ Xiaobing Li^1,2 Shijiang Mi^3,4 Jianfeng Jiang^3,4 Niu Zhou⁵ Zujin Chen⁵ Jie-Jian Zou⁹ Deyan Ge¹⁰ Qisen Yang¹⁰ Kai He¹¹ Tengteng Chen⁶ Ya-Jiang Wu⁵ Haoran Lu¹² David M Irwin^13,14 Xuejuan Shen¹ Yuanjia Hu¹ Xiaoman Lu¹ Chan Ding^15,16 Yi Guan^17,18 Changchun Tu^19,20 Yongyi Shen^21,22

Affiliations 22 institutions

State Key Laboratory for Animal Disease Control and Prevention, Guangdong Laboratory for Lingnan Modern Agriculture, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural University, Guangzhou, 510642, China.
Fujian Provincial Key Laboratory for the Prevention and Control of Animal Infectious Diseases and Biotechnology, College of Life Sciences, Longyan University, Longyan, 364012, China.
State Key Laboratory for Zoonotic Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education, Institute of Zoonosis, College of Veterinary Medicine, Jilin University, Changchun, 130062, China.
Changchun Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Changchun, 130122, China.
Guangzhou Zoo & Guangzhou Wildlife Research Center, Guangzhou, 510070, China.
Fujian Meihuashan Institute of South China Tiger Breeding, Longyan, 364201, China.
Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, Guangdong, 510642, China.
Zhaoqing Branch Center of Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Zhaoqing, 526000, Guangdong, China.
Guangdong Provincial Wildlife Monitoring and Rescue Center, Guangzhou, 510000, China.
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China.
Key Laboratory of Conservation and Application in Biodiversity of South China, School of Life Sciences, Guangzhou University, Guangzhou, Guangdong, 510006, China.
School of Mathematics, Sun Yat-sen University, Guangzhou, 510275, China.
Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, M5S1A8, Canada.
Banting and Best Diabetes Centre, University of Toronto, Toronto, M5S1A8, Canada.
Department of Avian Infectious Diseases, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Science, Shanghai, 201106, China. [email protected].
Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, 225009, China. [email protected].
Joint Influenza Research Centre (SUMC/HKU), Shantou University Medical College (SUMC), Shantou, 515041, China. [email protected].
Centre of Influenza Research, School of Public Health, The University of Hong Kong, Hong Kong, China. [email protected].
Changchun Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Changchun, 130122, China. [email protected].
Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, 225009, China. [email protected].
State Key Laboratory for Animal Disease Control and Prevention, Guangdong Laboratory for Lingnan Modern Agriculture, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural University, Guangzhou, 510642, China. [email protected].
Guangdong Provincial Key Laboratory of Zoonosis Prevention and Control, Guangzhou, 510642, China. [email protected].

PMID37120646 DOI10.1038/s41467-023-38202-4 Year2023 Journal Nature communications Nat Commun Languageeng Statusepublish

Abstract

Wildlife is reservoir of emerging viruses. Here we identified 27 families of mammalian viruses from 1981 wild animals and 194 zoo animals collected from south China between 2015 and 2022, isolated and characterized the pathogenicity of eight viruses. Bats harbor high diversity of coronaviruses, picornaviruses and astroviruses, and a potentially novel genus of Bornaviridae. In addition to the reported SARSr-CoV-2 and HKU4-CoV-like viruses, picornavirus and respiroviruses also likely circulate between bats and pangolins. Pikas harbor a new clade of Embecovirus and a new genus of arenaviruses. Further, the potential cross-species transmission of RNA viruses (paramyxovirus and astrovirus) and DNA viruses (pseudorabies virus, porcine circovirus 2, porcine circovirus 3 and parvovirus) between wildlife and domestic animals was identified, complicating wildlife protection and the prevention and control of these diseases in domestic animals. This study provides a nuanced view of the frequency of host-jumping events, as well as assessments of zoonotic risk.

Supporting text Virus Host Location

Chiroptera 371 COVID-19 425 Viruses 49 Animals 1948 Animals, Domestic 35 Animals, Wild 187 Animals, Zoo 18 Mammals 92 Pangolins 29 Phylogeny 805 Zoonoses 397

Evidence records

13 total

Zoonotic Surveillance

10 records · 3 evidence types

Evidence type Virus Isolation

1 records

OVE6943 Virus Isolation

Key finding

Eight infectious viruses were isolated from samples of wild and zoo animals collected in south China.

Virus

Host

Location

Supporting text

We isolated and characterized the pathogenicity of eight viruses from 1981 wild animals and 194 zoo animals collected from south China between 2015 and 2022.

Evidence type Viral Detection

7 records

OVE6942 Viral Detection

Key finding

Twenty-seven families of mammalian viruses were detected from 1981 wild animals and 194 zoo animals collected in south China between 2015 and 2022.

Virus

Host

Location

Supporting text

Here we identified 27 families of mammalian viruses from 1981 wild animals and 194 zoo animals collected from south China between 2015 and 2022.

Method: virus identification | metagenomic sequencing | molecular detection
Sample type: animal samples
Geographic raw: south China
Country inferred: CHN

OVE6948 Viral Detection

Key finding

Paramyxovirus was observed in both wildlife and domestic animals, supporting potential cross-species transmission.

Virus

Host

Location

Supporting text

Further, the potential cross-species transmission of RNA viruses (paramyxovirus and astrovirus) and DNA viruses (pseudorabies virus, porcine circovirus 2, porcine circovirus 3 and parvovirus) between wildlife and domestic animals was identified.

Method: virus detection | phylogenetic analysis | genomic comparison

OVE6949 Viral Detection

Key finding

Astrovirus was found to cross between wildlife and domestic animals, indicating cross-species viral exchange.

Virus

Host

Location

Supporting text

Method: virus detection | phylogenetic analysis | genomic comparison

OVE6950 Viral Detection

Key finding

Pseudorabies virus exhibited potential transmission between wildlife and domestic animals.

Virus

Host

Location

Supporting text

Method: virus detection | phylogenetic analysis | genomic comparison

OVE6951 Viral Detection

Key finding

Porcine circovirus 2 was identified in both wildlife and domestic animals, suggesting potential interspecies transmission.

Virus

Host

Location

Supporting text

Method: virus detection | phylogenetic analysis | genomic comparison

OVE6952 Viral Detection

Key finding

Porcine circovirus 3 was identified in both wildlife and domestic animals, consistent with cross-species transmission.

Virus

Host

Location

Supporting text

Method: virus detection | phylogenetic analysis | genomic comparison

OVE6953 Viral Detection

Key finding

Parvovirus was found in both wildlife and domestic animals, indicating potential cross-species viral exchange.

Virus

Host

Location

Supporting text

Method: virus detection | phylogenetic analysis | genomic comparison

Evidence type Reservoir Ecology

2 records

OVE6944 Reservoir Ecology

Key finding

Bats in south China harbor a high diversity of coronaviruses, picornaviruses, astroviruses, and a potentially novel genus of Bornaviridae, indicating ecological maintenance of diverse viruses in bat populations.

Virus

Host

Location

Supporting text

Here we identified 27 families of mammalian viruses from 1981 wild animals and 194 zoo animals collected from south China between 2015 and 2022. Bats harbor high diversity of coronaviruses, picornaviruses and astroviruses, and a potentially novel genus of Bornaviridae.

Method: metagenomic sequencing | ecological diversity analysis
Geographic raw: south China
Country inferred: CHN

OVE6945 Reservoir Ecology

Key finding

Pikas from south China harbor a new clade of Embecovirus and a new genus of arenaviruses, supporting a reservoir role of pikas for novel viral taxa.

Virus

Host

Location

Supporting text

Here we identified 27 families of mammalian viruses from 1981 wild animals and 194 zoo animals collected from south China between 2015 and 2022. Pikas harbor a new clade of Embecovirus and a new genus of arenaviruses.

Method: metagenomic sequencing
Geographic raw: south China
Country inferred: CHN

Experimental Infection

1 records · 1 evidence types

Evidence type Pathogenicity Experiment

1 records

OVE6954 Pathogenicity Experiment

Key finding

The study isolated and characterized the pathogenicity of eight viruses from wild and zoo animals collected from south China.

Virus

Host

Location

Supporting text

Here we identified 27 families of mammalian viruses from 1981 wild animals and 194 zoo animals collected from south China between 2015 and 2022, isolated and characterized the pathogenicity of eight viruses.

Method: virus isolation | pathogenicity characterization assays
Experimental system: animal infection experiments using viruses isolated from wild and zoo animals

Genomic Evolution

2 records · 1 evidence types

Evidence type Phylogenetic Evolution

2 records

OVE6946 Phylogenetic Evolution

Key finding

Picornavirus likely circulates between bats and pangolins, indicating cross-species viral transmission.

Virus

Host

Location

Supporting text

In addition to the reported SARSr-CoV-2 and HKU4-CoV-like viruses, picornavirus and respiroviruses also likely circulate between bats and pangolins.

Analysis methods: virus detection | genomic sequencing | phylogenetic analysis

OVE6947 Phylogenetic Evolution

Key finding

Respiroviruses likely circulate between bats and pangolins, suggesting cross-species transmission.

Virus

Host

Location

Supporting text

In addition to the reported SARSr-CoV-2 and HKU4-CoV-like viruses, picornavirus and respiroviruses also likely circulate between bats and pangolins.

Analysis methods: virus detection | genomic sequencing | phylogenetic analysis

References

71 references

Reference network

Force-directed citation graph. OmniVira-indexed references are prioritized and recursively expanded up to three steps.

260 nodes · 299 links · capped

Drag nodes to explore citation neighborhoods


PMID 18288193	Global trends in emerging infectious diseases	Jones	2008
PMID 29066781	Global hotspots and correlates of emerging zoonotic diseases	Allen	2017
PMID 32759999	Zoonotic host diversity increases in human-dominated ecosystems	Gibb	2020
PMID 16847084	Bats: important reservoir hosts of emerging viruses	Calisher	2006
PMID 27578437	Bats as viral reservoirs	Hayman	2016
PMID 34954661	Zoonotic disease and virome diversity in bats	Van Brussel	2022
PMID 35945197 In OmniVira	A strategy to assess spillover risk of bat SARS-related coronaviruses in Southeast Asia.	Sánchez	2022
PMID 32164206	Rodents as hosts of pathogens and related zoonotic disease risk	Dahmana	2020
PMID 30285857	Comparative analysis of rodent and small mammal viromes to better understand the wildlife origin of emerging infectious diseases	Wu	2018
PMID 32380510 In OmniVira	Isolation of SARS-CoV-2-related coronavirus from Malayan pangolins.	Xiao	2020
PMID 33563978 In OmniVira	Evidence for SARS-CoV-2 related coronaviruses circulating in bats and pangolins in Southeast Asia.	Wacharapluesadee	2021
PMID 32218527 In OmniVira	Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins.	Lam	2020
PMID 36803605 In OmniVira	A bat MERS-like coronavirus circulates in pangolins and utilizes human DPP4 and host proteases for cell entry.	Chen	2023
PMID 33843572	Pathogenicity and transmissibility of a novel respirovirus isolated from a Malayan pangolin	Yang	2021
PMID 35413253	Natural infection of pangolins with human respiratory syncytial viruses	Ye	2022
PMID 35678141	Human parainfluenza 3 and respiratory syncytial viruses detected in pangolins	Que	2022
PMID 35236404	Molecular detection of a novel Ancylostoma sp. by whole mtDNA sequence from pangolin Manis javanica	Tuli	2022
PMID 33598400	Identification of Amblyomma javanense and detection of tick-borne Ehrlichia spp. in confiscated Malayan Pangolins. Int	Zhai	2021
PMID 17507975	Origins of major human infectious diseases	Wolfe	2007
PMID 35062324 In OmniVira	SARS-CoV-2 Reverse Zoonoses to Pumas and Lions, South Africa.	Koeppel	2022
PMID 35318922	SARS-CoV-2 outbreak among Malayan tigers and humans, Tennessee, USA, 2020	Grome	2022
PMID 33051368 In OmniVira	From People to <i>Panthera</i>: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo.	McAloose	2020
PMID 26262818	Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases	Wu	2016
PMID 35298912 In OmniVira	Virome characterization of game animals in China reveals a spectrum of emerging pathogens.	He	2022
PMID 32846157	Emerging pandemic diseases: how we got to COVID-19	Morens	2020
PMID 34799704	Ecology, evolution and spillover of coronaviruses from bats	Ruiz-Aravena	2022
PMID 29669833	Discovery of novel bat coronaviruses in south China that use the same receptor as MERS coronavirus	Luo	2018
PMID 29618817 In OmniVira	Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin.	Zhou	2018
PMID 31207129	The re-emerging of SADS-CoV infection in pig herds in Southern China	Zhou	2019
PMID 36002051	Re-emergence of severe acute diarrhea syndrome coronavirus (SADS-CoV) in Guangxi, China, 2021	Xing	2022
PMID 28786787	Proposed revision to the taxonomy of the genus Pestivirus, family Flaviviridae	Smith	2017
PMID 26111586	The molecular biology of pestiviruses	Tautz	2015
PMID 25384138	Pestiviruses	Schweizer	2014
PMID 25316698	Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. mBio. 2014;5:e01933–01914	Firth	2014
PMID 30405596	Discovery of diverse rodent and bat pestiviruses with distinct genomic and phylogenetic characteristics in several Chinese provinces	Wu	2018
PMID 22855479	Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces	Wu	2012
PMID 31526243	An evolutionary divergent pestivirus lacking the N(pro) gene systemically infects a whale species	Jo	2019
PMID 33492978	Similarities and dissimilarities of COVID-19 and other coronavirus diseases	Fung	2021
PMID 16575523	Structure, function and evolution of the hemagglutinin-esterase proteins of corona- and toroviruses	de Groot	2006
PMID 22094080	Chapter 4 - Coronavirus pathogenesis in Advances in Virus Research	Weiss	2011
PMID 22291594	The murine coronavirus hemagglutinin-esterase receptor-binding site: a major shift in ligand specificity through modest changes in architecture	Langereis	2012
PMID 28279346 In OmniVira	Betacoronavirus Adaptation to Humans Involved Progressive Loss of Hemagglutinin-Esterase Lectin Activity.	Bakkers	2017
PMID 34691006	Discovery and evolution of a divergent coronavirus in the plateau pika from China that extends the host range of alphacoronaviruses	Zhu	2021
-	Arenaviridae: the Viruses and Their Replication (Lippincott-Raven, 2007)	Buchmeier	2007
PMID 14644972	Lassa fever: epidemiology, clinical features, and social consequences	Richmond	2003
-	Plateau pika Ochotona curzoniae poisoning campaign reduces carnivore abundance in southern Qinghai	Andrew	2016
-	The plateau pika (Ochotona curzoniae) is a keystone species for biodiversity on the Tibetan plateau	Smith	1999
PMID 11561960	The infrequency of transmission of herpesviruses between humans and animals; postulation of an unrecognised protective host mechanism	Skinner	2001
PMID 2881053	Pseudorabies in man	Mravak	1987
PMID 29774834	Human endophthalmitis caused by pseudorabies virus infection, China, 2017	Ai	2018
PMID 32667972	A novel human acute encephalitis caused by Pseudorabies virus variant strain	Liu	2020
PMID 25965793	Genomic characterization of emergent pseudorabies virus in China reveals marked sequence divergence: evidence for the existence of two major genotypes	Ye	2015
PMID 31616677	Reservoirs of porcine circoviruses: a mini review	Zhai	2019
PMID 30423086	fastp: an ultra-fast all-in-one FASTQ preprocessor	Chen	2018
PMID 19451168	Fast and accurate short read alignment with Burrows-Wheeler transform	Li	2009
PMID 25609793	MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph	Li	2015
PMID 33828273	Sensitive protein alignments at tree-of-life scale using DIAMOND	Buchfink	2021
PMID 22388286	Fast gapped-read alignment with Bowtie 2	Langmead	2012
PMID 34001434	TaxonKit: A practical and efficient NCBI taxonomy toolkit	Shen	2021
PMID 34406356	coronaSPAdes: from biosynthetic gene clusters to RNA viral assemblies	Meleshko	2021
PMID 22543367	Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data	Kearse	2012
PMID 19505943	The Sequence Alignment/Map format and SAMtools	Li	2009
PMID 23193283	The SILVA ribosomal RNA gene database project: improved data processing and web-based tools	Quast	2013
PMID 29506019	Parallelization of MAFFT for large-scale multiple sequence alignments	Nakamura	2018
PMID 27004904	MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets	Kumar	2016
PMID 19505945	trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses	Capella-Gutiérrez	2009
PMID 32011700	IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era	Minh	2020
PMID 9847317	Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination	Lole	1999
PMID 27774277	RDP4: detection and analysis of recombination patterns in virus genomes	Martin	2015
PMID 25293398	Pathogenicity and genomic characterization of a pseudorabies virus variant isolated from Bartha-K61-vaccinated swine population in China	Luo	2014
PMID 32511839	Molecular and serological investigation of cat viral infectious diseases in China from 2016 to 2019	Liu	2020