Cryo-EM structures of Thogoto virus polymerase reveal unique RNA transcription and replication mechanisms among orthomyxoviruses

Lu Xue, Tiancai Chang, Zimu Li, Chenchen Wang, Heyu Zhao, Mei Li, Peng Tang, Xin Wen, Mengmeng Yu, Jiqin Wu, Xichen Bao, Xiaojun Wang, Peng Gong, Jun He, Xinwen Chen () and Xiaoli Xiong ()
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Lu Xue: Chinese Academy of Sciences
Tiancai Chang: Chinese Academy of Sciences
Zimu Li: Chinese Academy of Sciences
Chenchen Wang: Southern University of Science and Technology
Heyu Zhao: Chinese Academy of Sciences
Mei Li: Guangzhou National Laboratory
Peng Tang: Chinese Academy of Sciences
Xin Wen: Chinese Academy of Sciences
Mengmeng Yu: Chinese Academy of Agricultural Sciences
Jiqin Wu: Chinese Academy of Sciences
Xichen Bao: Chinese Academy of Sciences
Xiaojun Wang: Chinese Academy of Agricultural Sciences
Peng Gong: Chinese Academy of Sciences
Jun He: Chinese Academy of Sciences
Xinwen Chen: Guangzhou National Laboratory
Xiaoli Xiong: Chinese Academy of Sciences

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Influenza viruses and thogotoviruses account for most recognized orthomyxoviruses. Thogotoviruses, exemplified by Thogoto virus (THOV), are capable of infecting humans using ticks as vectors. THOV transcribes mRNA without the extraneous 5′ end sequences derived from cap-snatching in influenza virus mRNA. Here, we report cryo-EM structures to characterize THOV polymerase RNA synthesis initiation and elongation. The structures demonstrate that THOV RNA transcription and replication are able to start with short dinucleotide primers and that the polymerase cap-snatching machinery is likely non-functional. Triggered by RNA synthesis, asymmetric THOV polymerase dimers can form without the involvement of host factors. We confirm that, distinctive from influenza viruses, THOV-polymerase RNA synthesis is weakly dependent of the host factors ANP32A/B/E in human cells. This study demonstrates varied mechanisms in RNA synthesis and host factor utilization among orthomyxoviruses, providing insights into the mechanisms behind thogotoviruses’ broad-infectivity range.

Date: 2024
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DOI: 10.1038/s41467-024-48848-3

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