Cross-species transmission and PB2 mammalian adaptations of highly pathogenic avian influenza A/H5N1 viruses in Chile.

Catalina Pardo-Roa^1,2 Martha I Nelson³ Naomi Ariyama⁴ Carolina Aguayo⁵ Leonardo I Almonacid^6,7 Gabriela Munoz⁵ Carlos Navarro⁸ Claudia Avila⁵ Mauricio Ulloa^8,9 Rodolfo Reyes⁹ Eugenia Fuentes Luppichini² Christian Mathieu⁵ Ricardo Vergara⁵ Álvaro González⁵ Carmen Gloria González⁵ Hugo Araya⁵ Jorge Fernández¹⁰ Rodrigo Fasce¹⁰ Magdalena Johow⁵ Rafael A Medina^2,11,12 Victor Neira⁴

Affiliations 12 institutions

Department of Child and Adolescent Health, School of Nursing, Pontificia Universidad Católica de Chile, Santiago, Chile.
Department of Pediatric Infectious Diseases and Immunology, School of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile.
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20892, USA.
Departamento de Medicina Preventiva Animal, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile. 11735 Santa Rosa, La Pintana, Santiago, Chile.
Servicio Agrícola y Ganadero, SAG, Chile.
Molecular Bioinformatics Laboratory, Department of Molecular Genetics and Microbiology, Faculty of Biological Sciences, Pontificia Universidad Católica de Chile, Santiago, Chile.
Institute for Biological and Medical Engineering, Schools of Engineering, Medicine and Biological Sciences, Pontificia Universidad Católica de Chile, Santiago, Chile.
Servicio Nacional de Pesca y Acuicultura, SERNAPESCA, Chile.
Veterinary Histology and Pathology, Institute of Animal Health and Food Safety, Veterinary School, University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain.
Instituto de Salud Pública, ISP, Ministerio de Salud, Santiago, Chile.
Department of Pathology and Laboratory Medicine, School of Medicine, Emory Vaccine Center, Emory University, Atlanta, USA.
Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, USA.

PMID37786724 DOI10.1101/2023.06.30.547205 Year2023 Journal bioRxiv : the preprint server for biology bioRxiv Languageeng Statusepublish

Abstract

H5N1 highly pathogenic avian influenza viruses (HPAIV) emerged in wild birds in Chile in December 2022 and spilled over into poultry, marine mammals, and one human. Between December 9, 2022 - March 14, 2023, a coordinated government/academic response detected HPAIV by real-time RT-PCR in 8.5% (412/4735) of samples from 23 avian and 3 mammal orders. Whole-genome sequences obtained from 77 birds and 8 marine mammals revealed that all Chilean H5N1 viruses belong to lineage 2.3.4.4b and cluster monophyletically with viruses from Peru, indicating a single introduction from North America into Peru/Chile. Mammalian adaptations were identified in the PB2 segment: D701N in two sea lions, one human, and one shorebird, and Q591K in the human and one sea lion. Minor variant analysis revealed that D701N was present in 52.9 - 70.9% of sequence reads, indicating the presence of both genotypes within hosts. Further surveillance of spillover events is warranted to assess the emergence and potential onward transmission of mammalian adapted H5N1 HPAIV in South America.

Supporting text Virus Host Location

Chile 9 Genomic Surveillance 10 H5N1 82 HPAIV 6 Interspecies transmission 51 Marine Mammals 2 Panzootic 2 Zoonotic 23

Evidence records

6 total

Zoonotic Surveillance

1 records · 1 evidence types

Evidence type Viral Detection

1 records

OVE7410 Viral Detection

Key finding

H5N1 highly pathogenic avian influenza virus was detected by real-time RT-PCR in samples from multiple avian and mammalian species in Chile.

Virus

Host

Location

Supporting text

Method: real-time RT-PCR
Sample type: samples
Geographic raw: Chile
Country inferred: CHL

Transmission Evidence

3 records · 2 evidence types

Evidence type Spillover Event

1 records

OVE7413 Spillover Event

Key finding

H5N1 highly pathogenic avian influenza virus spilled over from animals into one human in Chile during the 2022–2023 outbreak.

Virus

Host

human Homo sapiens Natural host

birds Aves Natural host

mammals Mammalia Natural host

Location

Supporting text

H5N1 highly pathogenic avian influenza viruses (HPAIV) emerged in wild birds in Chile in December 2022 and spilled over into poultry, marine mammals, and one human.

Method: real-time RT-PCR detection | whole-genome sequencing
Study design: outbreak investigation with genomic and surveillance data
Transmission direction: animal-to-human
Geographic raw: Chile
Country inferred: CHL

Evidence type Cross-species Transmission

2 records

OVE7411 Cross-species Transmission

Key finding

H5N1 highly pathogenic avian influenza viruses transmitted from wild birds to poultry in Chile.

Virus

Host

Location

Supporting text

H5N1 highly pathogenic avian influenza viruses (HPAIV) emerged in wild birds in Chile in December 2022 and spilled over into poultry, marine mammals, and one human.

Method: real-time RT-PCR | whole-genome sequencing
Study design: field surveillance and genomic analysis
Transmission direction: animal-to-animal
Geographic raw: Chile
Country inferred: CHL

OVE7412 Cross-species Transmission

Key finding

H5N1 highly pathogenic avian influenza viruses transmitted from wild birds to marine mammals in Chile.

Virus

Host

Location

Supporting text

H5N1 highly pathogenic avian influenza viruses (HPAIV) emerged in wild birds in Chile in December 2022 and spilled over into poultry, marine mammals, and one human.

Method: real-time RT-PCR | whole-genome sequencing
Study design: field surveillance and genomic analysis
Transmission direction: animal-to-animal
Geographic raw: Chile
Country inferred: CHL

Functional Mechanism

1 records · 1 evidence types

Evidence type Molecular Adaptation

1 records

OVE7415 Molecular Adaptation

Key finding

H5N1 viruses from sea lions, a human, and a shorebird in Chile carried PB2 mammalian adaptation mutations D701N and Q591K associated with enhanced replication or host-range in mammals.

Virus

Host

Location

Supporting text

Mammalian adaptations were identified in the PB2 segment: D701N in two sea lions, one human, and one shorebird, and Q591K in the human and one sea lion.

Genes or proteins: PB2
Mutations: D701N | Q591K
Mechanism types: replication adaptation | host-range expansion

Genomic Evolution

1 records · 1 evidence types

Evidence type Phylogenetic Evolution

1 records

OVE7414 Phylogenetic Evolution

Key finding

Phylogenetic analysis showed that Chilean H5N1 viruses belong to lineage 2.3.4.4b and form a monophyletic cluster with Peruvian viruses, indicating a single introduction from North America into Peru and Chile.

Virus

Host

Location

Supporting text

Whole-genome sequences obtained from 77 birds and 8 marine mammals revealed that all Chilean H5N1 viruses belong to lineage 2.3.4.4b and cluster monophyletically with viruses from Peru, indicating a single introduction from North America into Peru/Chile.

Genes or proteins: whole genome
Analysis methods: phylogenetic analysis | whole-genome sequencing

References

53 references

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