Outbreaks of H5N1 high pathogenicity avian influenza in South Africa in 2023 were caused by two distinct sub-genotypes of clade 2.3.4.4b viruses

Abstract

In 2023, South Africa continued to experience sporadic cases of clade 2.3.4.4b H5N1 high-pathogenicity avian influenza (HPAI) in coastal seabirds and poultry. Active environmental surveillance determined that H5Nx, H7Nx, H9Nx, H11Nx, H6N2, and H12N2, amongst other unidentified subtypes, circulated in wild birds and ostriches in 2023, but that H5Nx was predominant. Genome sequencing and phylogenetic analysis of confirmed H5N1 HPAI cases determined that only two of the fifteen sub-genotypes that circulated in South Africa in 2021-2022 still persisted in 2023. Sub-genotype SA13 remained restricted to coastal seabirds, with accelerated mutations observed in the neuraminidase protein. SA15 caused the chicken outbreaks, but outbreaks in the Paardeberg and George areas, in the Western Cape province, and the Camperdown region of the KwaZulu-Natal province were unrelated to each other, implicating wild birds as the source. All SA15 viruses contained a truncation in the PB1-F2 gene, but in the Western Cape SA15 chicken viruses, PA-X was putatively expressed as a novel isoform with eight additional amino acids. South African clade 2.3.4.4b H5N1 viruses had comparatively fewer markers of virulence and pathogenicity compared to European strains, a possible reason why no spillover to mammals has occurred here yet.

Description

DATA AVAILABILITY STATEMENT : All data are presented within the manuscript or as Supplementary Materials. Sequences generated in this study are deposited in the GISAID EpiFlu database under accession numbers: EPI_ISL_18799506 to EPI_ISL18809555. (https://gisaid.org/, accessed 8 May 2024).
SUPPLEMENTARY MATERIAL FIGURE S1: Time-scaled maximum clade credibility tree of the concatenated genomes of southern African clade 2.3.4.4b H5N1 HPAI viruses. Blue node bars represent the common ancestor 95% height posterior density and the numerical value denotes the posterior probability; FIGURE S2 (a–h): Maximum likelihood phylogenetic trees of the eight genome segments of South African clade 2.3.4.4B H5N1 HPAI viruses and the closest relatives. Viruses sequenced in this study are in boldface. PB2—polymerase B2; PB1—polymerase 1; PA—polymerase A; HA—hemagglutinin (H5 subtype);NP—nucleocapsid protein; NA—neuraminidase; M—matrix protein, NS—non-structural protein; FIGURE S3: Maximum likelihood phylogenetic tree of the concatenated HA, M, NA, NS, NP and PB2 genes of SA15 viruses (8766 nt); (721,913 lacks a PB1 and 719,311 lacks PB1 and PA). Additional sequences are in boldface; TABLE S1: Monthly number of environmental fecal swab pools (n = 130 a) from wild ducks tested for the presence of avian influenza (AIV) and H5Nx/H7Nx subtype- specific viral RNA in 2023; TABLE S2: BLAST sequence homology results for avian influenza viruses detected in commercial ostriches in 2023; TABLE S3: Unique markers in the translated protein sequences that emerged in coastal seabird H5N1 HPAI sub-lineage SA13 viruses; TABLE S4: Distance matrix for the HA protein expressed as number of differences; TABLE S5: Distance matrix for the neuraminidase protein expressed as number of differences.

Keywords

High-pathogenicity avian influenza (HPAI), Clade 2.3.4.4b, H5N1, Seabirds, Poultry, Phylogenetic analysis, PA-X isoform, PB1-F2 truncation, Wild bird disease surveillance

Sustainable Development Goals

SDG-03: Good health and well-being
SDG-15: Life on land

Citation

Abolnik, C.; Roberts, L.C.; Strydom, C.; Snyman, A.; Roberts, D.G. Outbreaks of H5N1 High Pathogenicity Avian Influenza in South Africa in 2023 Were Caused by Two Distinct Sub-Genotypes of Clade 2.3.4.4b Viruses. Viruses 2024, 16, 896. https://doi.org/10.3390/v16060896.