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      The evolution, pathogenicity and transmissibility of quadruple reassortant H1N2 swine influenza virus in China: A potential threat to public health

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          Abstract

          Swine are regarded as “intermediate hosts” or “mixing vessels” of influenza viruses, capable of generating strains with pandemic potential. From 2020 to 2021, we conducted surveillance on swine H1N2 influenza (swH1N2) viruses in swine farms located in Guangdong, Yunnan, and Guizhou provinces in southern China, as well as Henan and Shandong provinces in northern China. We systematically analyzed the evolution and pathogenicity of swH1N2 isolates, and characterized their replication and transmission abilities. The isolated viruses are quadruple reassortant H1N2 viruses containing genes from pdm/09 H1N1 ( PB2, PB1, PA and NP genes), triple-reassortant swine ( NS gene), Eurasian Avian-like ( HA and M genes), and recent human H3N2 ( NA gene) lineages. The NA, PB2, and NP of SW/188/20 and SW/198/20 show high gene similarities to A/Guangdong/Yue Fang277/2017 (H3N2). The HA gene of swH1N2 exhibits a high evolutionary rate. The five swH1N2 isolates replicate efficiently in human, canine, and swine cells, as well as in the turbinate, trachea, and lungs of mice. A/swine/Shandong/198/2020 strain efficiently replicates in the respiratory tract of pigs and effectively transmitted among them. Collectively, these current swH1N2 viruses possess zoonotic potential, highlighting the need for strengthened surveillance of swH1N2 viruses.

          Highlights

          • Five quadruple reassortant swH1N2 viruses were identified which have close genetic relationship with current human virus.

          • The swH1N2 viruses replicates effectively in human, canine, and swine cells and mice.

          • A/swine/Shandong/198/2020 replicates efficiently in the respiratory tract of pigs and spreads effectively.

          • The swH1N2 viruses pose zoonotic potential, highlighting the need for strengthened surveillance of swH1N2 viruses.

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          Most cited references55

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          IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies

          Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus, there is need for additional approaches that employ different search strategies to find ML trees and that are at the same time as fast as currently available ML programs. We show that a combination of hill-climbing approaches and a stochastic perturbation method can be time-efficiently implemented. If we allow the same CPU time as RAxML and PhyML, then our software IQ-TREE found higher likelihoods between 62.2% and 87.1% of the studied alignments, thus efficiently exploring the tree-space. If we use the IQ-TREE stopping rule, RAxML and PhyML are faster in 75.7% and 47.1% of the DNA alignments and 42.2% and 100% of the protein alignments, respectively. However, the range of obtaining higher likelihoods with IQ-TREE improves to 73.3-97.1%.
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            Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation

            The Interactive Tree Of Life ( https://itol.embl.de ) is an online tool for the display, manipulation and annotation of phylogenetic and other trees. It is freely available and open to everyone. iTOL version 5 introduces a completely new tree display engine, together with numerous new features. For example, a new dataset type has been added (MEME motifs), while annotation options have been expanded for several existing ones. Node metadata display options have been extended and now also support non-numerical categorical values, as well as multiple values per node. Direct manual annotation is now available, providing a set of basic drawing and labeling tools, allowing users to draw shapes, labels and other features by hand directly onto the trees. Support for tree and dataset scales has been extended, providing fine control over line and label styles. Unrooted tree displays can now use the equal-daylight algorithm, proving a much greater display clarity. The user account system has been streamlined and expanded with new navigation options and currently handles >1 million trees from >70 000 individual users. Graphical Abstract iTOL: an online tool for the tree display and annotation.
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              Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7

              Abstract Bayesian inference of phylogeny using Markov chain Monte Carlo (MCMC) plays a central role in understanding evolutionary history from molecular sequence data. Visualizing and analyzing the MCMC-generated samples from the posterior distribution is a key step in any non-trivial Bayesian inference. We present the software package Tracer (version 1.7) for visualizing and analyzing the MCMC trace files generated through Bayesian phylogenetic inference. Tracer provides kernel density estimation, multivariate visualization, demographic trajectory reconstruction, conditional posterior distribution summary, and more. Tracer is open-source and available at http://beast.community/tracer.
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                Author and article information

                Contributors
                Journal
                Virol Sin
                Virol Sin
                Virologica Sinica
                Wuhan Institute of Virology, Chinese Academy of Sciences
                1674-0769
                1995-820X
                10 February 2024
                April 2024
                10 February 2024
                : 39
                : 2
                : 205-217
                Affiliations
                [a ]College of Veterinary Medicine, South China Agricultural University, Guangzhou, 510642, China
                [b ]Key Laboratory of Zoonosis Control and Prevention of Guangdong Province, South China Agricultural University, Guangzhou, 510642, China
                [c ]National and Regional Joint Engineering Laboratory for Medicament of Zoonosis Prevention and Control, South China Agricultural University, Guangzhou, 510642, China
                [d ]Shandong Vocational Animal Science and Veterinary College, Weifang, 261061, China
                [e ]Institute of Animal Health, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China
                Author notes
                [1]

                Xinxin Cui, Jinhuan Ma and Zifeng Pang contribute equally to this work.

                Article
                S1995-820X(24)00022-1
                10.1016/j.virs.2024.02.002
                11074646
                38346538
                fc556135-4b19-4517-91b8-7f5473d6a3df
                © 2024 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 3 October 2023
                : 6 February 2024
                Categories
                Research Article

                swine influenza virus (siv),h1n2,evolution,replication,pathogenicity,zoonotic potential

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