2019-2022年中国H6N1亚型禽流感病毒的生物学特性分析

doi:10.3864/j.issn.0578-1752.2024.09.015

Abstract

Abstract:

【Background】H6 avian influenza virus (AIV) is widely prevalent in southern China, which is one of the most common subtypes of AIVs circulating in poultry in China. H6N1 AIVs frequently undergo gene reassortment events with other wild bird-origin virus, which can be a donor to provide internal gene segments to highly pathogenic AIVs, which may lead to the emergence of novel virus and threaten human health.【Objective】The aim of this study was to investigate the evolution and biological characteristics of H6N1 AIVs in China, so as to provide valuable data for the prevention and control of avian influenza in China.【Method】From 2019 to 2022, cloacal and throat swabs were collected from live poultry markets and breeding farms across 25 provinces or autonomous regions in China. 7 H6N1 viruses were isolated by inoculating into chicken embryos. The complete genome sequences were determined, followed by analyzing their phylogenetic relationships, receptor binding properties, as well as replication in SPF chickens and BALB/c mice.【Result】The phylogenetic analysis revealed that the genes of the 7 H6N1 AIVs were highly homologous to those of wild bird-origin viruses from North America and Southeast Asia, indicating a complex genetic origin with significant genetic diversity. According to the Bayesian evolution analysis, the HA gene of H6 subtype AIVs had many times of intercontinental transmission in the history, and the Eurasian lineage strains also had a long time of circulation in North America. The HA gene of one strain of the virus was highly homologous to that of the North American strain. Based on the results of Bayesian evolutionary analysis, it was hypothesized that the virus was introduced to China via wild birds after undergoing complex genetic reassortment in wild birds. Analysis of specific amino acid sites revealed that the cleavage site of HA protein was PQIETR↓GLF, which was the signature of low pathogenic AIVs. In addition, one other virus had a Y52H mutation in the NP protein, which was critical in BTN3A3 evasion. Receptor binding analysis demonstrated that some of the H6N1 AIVs bound to both avian-type receptor and human-type receptor, however, their affinity towards human receptors was weaker compared with avian receptors. Infectivity experiments on SPF chickens indicated that flocks was still able to shed virus up through oropharyngeal and cloacal routes after infection with A/chicken/Jiangxi/S40445/2019(H6N1) and that the virus could be transmitted via contact within flocks. Only a few chickens infected with A/duck/Jiangxi/S10941/2019(H6N1) shed virus through their oropharyngeal tract, and the virus could not be transmitted via contact among chickens. The infectivity experiments conducted on mice showed that H6N1 subtype AIVs could replicate in the respiratory organs of infected mice without prior adaptation, but display low pathogenicity levels in mice.【Conclusion】Most of the genes of H6N1 subtype AIV isolated in China from 2019 to 2022 were derived from wild bird-origin viruses, and those migratory birds could introduce the viruses into China via the East Asia-Australasian migratory flyway. Some of the H6 AIVs bound to human-type receptors and replicate in the respiratory organs of mice suggested that H6N1 viruses posed a potential threat to human health.

Key words: H6N1, avian influenza virus, intercontinental transmission, reassortment, infectivity

CHEN Yuan, CUI PengFei, SHI JianZhong, ZHANG YuanCheng, YU QingQing, YAN Cheng, ZHANG YaPing, WANG CongCong, ZHANG Jie, WANG Yan, DENG GuoHua, CHEN HuaLan. Biological Characteristics of H6N1 Subtype Avian Influenza Virus from 2019 to 2022 in China[J].Scientia Agricultura Sinica, 2024, 57(9): 1820-1832.

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Figures/Tables 9

Table 1

Table 2

Homology analysis of each gene segment of 7 H6N1 AIVs"

病毒 Virus	基因 Gene	核苷酸相似性最高的病毒 Virus with highest identity	相似性 Identity	片段编号 Segment ID
DK/HuB/186/19	HA	A/mallard/Anhui/2-549/2019 (H6N1)	99%	EPI1743652
	NA	A/Anser brachyrhynchus/South Korea/42/2019 (H6N1)	99%	EPI2395430
	PB2	A/mallard/Anhui/2-549/2019 (H6N1)	99%	EPI1743649
	PB1	A/wild bird/Hunan/01.18 DTHBDF33/2019(H9N2)	99%	EPI1626428
	PA	A/mallard/Korea/H37-1/2019 (H10N3)	98%	EPI1752410
	NP	A/wild bird /Shandong/11452/2019 (H9N2)	99%	EPI1896647
	M	A/White-fronted Goose/South Korea/KNU2021-18/2021 (H6N2)	99%	EPI2153859
	NS	A/common teal/Shanghai/JDS110203/2019 (H12N8)	99%	EPI1767944
DK/JX/941/19	HA	A/northern pintail/Alaska/UGAI17-4733/2017 (H6N5)	99%	EPI1774620
	NA	A/White-fronted goose/South Korea/KNU2019-37/2019 (H1N1)	99%	EPI1902856
	PB2	A/Anser fabalis/South Korea/50/2019 (H6N2)	99%	EPI2395451
	PB1	A/spot-billed duck/South Korea/JB32-105/2019 (H4N2)	99%	EPI1903725
	PA	A/duck/Mongolia/543/2015 (H4N6)	99%	EPI704413
	NP	A/pink-footed goose/Korea/H3473/2015 (H5N3)	99%	EPI1513819
	M	A/mallard/Omsk region/45/2020 (H5N2)	99%	EPI1847610
	NS	A/duck/Mongolia/MN18-14/2018 (H3N8)	100%	EPI1903627
CK/JX/445/19	HA	A/mallard/Anhui/2-549/2019 (H6N1)	99%	EPI1743652
	NA	A/Anser brachyrhynchus/South Korea/42/2019 (H6N1)	99%	EPI2395430
	PB2	A/duck/Mongolia/826/2019 (H4N6)	99%	EPI1777578
	PB1	A/duck/Mongolia/820/2019 (H4N2)	99%	EPI1777571
	PA	A/environment/Korea/W437/2012 (H7N7)	98%	EPI837838
	NP	A/mallard/Anhui/3-617/2019 (H6N1)	98%	EPI1743661
	M	A/wild bird/Korea/H2542/2015 (H10N7)	99%	EPI1752361
	NS	A/duck/Mongolia/518/2015 (H10N3)	99%	EPI704566
DK/FJ/48/20	HA	A/mallard/Anhui/2-549/2019 (H6N1)	99%	EPI1743652
	NA	A/Anser brachyrhynchus/South Korea/42/2019 (H6N1)	99%	EPI2395430
	PB2	A/mallard/Anhui/2-549/2019 (H6N1)	99%	EPI1743649
	PB1	A/duck/Mongolia/217/2018 (H3N8)	98%	EPI1818050
	PA	A/little curlew/Liaoning/dandong142/2019 (H7N4)	98%	EPI1738381
	NP	A/wild bird /Shandong/11452/2019 (H9N2)	99%	EPI1896647
	M	A/environment/Kagoshima/KU-G3/2019 (H3N8)	99%	EPI2073561
	NS	A/common teal/Shanghai/JDS110203/2019 (H12N8)	99%	EPI1767944
DK/HuN/268/20	HA	A/mallard/Anhui/2-549/2019 (H6N1)	99%	EPI1743652
	NA	A/Anser brachyrhynchus/South Korea/42/2019 (H6N1)	99%	EPI2395430
	PB2	A/mallard/Anhui/2-549/2019 (H6N1)	99%	EPI1743649
	PB1	A/wild duck/Shandong/W11397/2019 (H3N8)	99%	EPI2245882
	PA	A/Gadwall/Buryatia/2206/2019 (H12N5)	99%	EPI1638480
	NP	A/mallard/Anhui/2-549/2019 (H6N1)	99%	EPI1743645
	M	A/environment/Japan/KU-C10/2020 (H3N8)	99%	EPI2596493
	NS	A/common teal/Shanghai/JDS110203/2019 (H12N8)	99%	EPI1767944
DK/GZ/674/21	HA	A/Anser albifrons/South Korea/50/2022 (H6N2)	99%	EPI2395103
	NA	A/Anser albifrons/South Korea/64/2022 (H6N1)	99%	EPI2395393
	PB2	A/Mallard/South Korea/KNU2021-49/2021 (H7N7)	99%	EPI2153561
	PB1	A/wild duck/Shandong/W11397/2019 (H3N8)	99%	EPI2245882
	PA	A/enviroment/Shanghai/CM20659/2020(H4N2)	99%	EPI2600926
	NP	A/Common Teal/South Korea/KNU2021-22/2021 (H8N4)	99%	EPI2153541
	M	A/mallard/South Korea/20X-20/2021 (H7N9)	99%	EPI1930790
	NS	A/environment/Kagoshima/KU-3c/2019 (H11N2)	99%	EPI2075052
DK/HuN/963/21	HA	A/Common_Teal/Buryatia/73i/2019 (H6N1)	98%	EPI1657043
	NA	A/Mallard/South Korea/KNU2021-9/2021 (H1N1)	98%	EPI2153457
	PB2	A/Mallard/South Korea/KNU2021-49/2021 (H7N7)	99%	EPI2153561
	PB1	A/duck/Mongolia/543/2015 (H4N6)	98%	EPI704412
	PA	A/Wild Duck/South Korea/KNU2020-101/2020 (H9N2)	99%	EPI1931705
	NP	A/wild duck/Shandong/W6271/2019 (H3N8)	99%	EPI2245829
	M	A/environment/Japan/KU-C10/2020 (H3N8)	99%	EPI2596493
	NS	A/environment/Kagoshima/KU-3c/2019 (H11N2)	99%	EPI2075052

Table 2

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Table 3

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毒株名称 Virus name	宿主 Host	分离地点 Location	省份 Province	分离年份 Year
A/duck/Hubei/S4186/2019 (H6N1) ( DK/HuB/186/19)	鸭Duck	养殖场Farm	湖北Hubei	2019
A/duck/Jiangxi/S10941/2019 (H6N1) ( DK/JX/941/19)	鸭Duck	养殖场Farm	江西Jiangxi	2019
A/chicken/Jiangxi/S40445/2019 (H6N1) ( CK/JX/445/19)	鸡Chicken	养殖场Farm	江西Jiangxi	2019
A/duck/Fujian/S1048/2020 (H6N1) ( DK/FJ/48/20)	鸭Duck	市场Market	福建Fujian	2020
A/duck/Hunan/S10268/2020 (H6N1) ( DK/HuN/268/20)	鸭Duck	养殖场Farm	湖南Hunan	2020
A/duck/Guizhou/S4674/2021 (H6N1) ( DK/GZ/674/21)	鸭Duck	市场Market	贵州Guizhou	2021
A/duck/Hunan/S40963/2021 (H6N1) ( DK/HuN/963/21)	鸭Duck	养殖场Farm	湖南Hunan	2021

基因 Gene	最近亲缘关系毒株 Most closely related strain	最近共同祖先时间（95%置信区间） tMRCA (95% HPD interval)	后验概率 Posterior probability
PB2	Waterfowl strains (South Korea and China)	2018.3 (2017.3—2018.10)	0.9976
PB1	Waterfowl H4N2 (South Korea)	2017.6 (2016.6—2018.6)	0.9993
PA	Waterfowl H4N6 (South Korea)	2018.4 (2017.1—2019.1)	0.2914
HA	Waterfowl, wild bird strains (South Korea and China)	2017.11 (2017.7—2018.4)	0.9752
NP	Duck H3N2 (Vietnam)	2016.5 (2013.3—2018.7)	0.9167
NA	Waterfowl H1N1 (South Korea)	2018.12 (2018.6—2019.2)	0.9981
M	Waterfowl strains (Siberia of Russia)	2017.11 (2016.11—2018.7)	0.2385
NS	Duck H4N6 (Mongolia)	2019.1 (2018.9—2019.2)	0.6487

Biological Characteristics of H6N1 Subtype Avian Influenza Virus from 2019 to 2022 in China

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