Molecular and structural insights into SARS-CoV-2 evolution: from BA.2 to XBB subvariants

Hisano Yajima; Tomo Nomai; Kaho Okumura; Katsumi Maenaka; Genotype to Phenotype Japan (G2P-Japan) Consortium; Jumpei Ito; Takao Hashiguchi; Kei Sato

doi:10.1128/mbio.03220-23

Molecular and structural insights into SARS-CoV-2 evolution: from BA.2 to XBB subvariants

mBio. 2024 Sep 16:e0322023. doi: 10.1128/mbio.03220-23. Online ahead of print.

Authors

Hisano Yajima^#¹, Tomo Nomai^#², Kaho Okumura^{3

4}, Katsumi Maenaka^{2

5

6

7

8}; Genotype to Phenotype Japan (G2P-Japan) Consortium; Jumpei Ito^{3

9}, Takao Hashiguchi^{1

10}, Kei Sato^{3

9

11

12

13

14

15}

Collaborators

Genotype to Phenotype Japan (G2P-Japan) Consortium:
Keita Matsuno, Naganori Nao, Hirofumi Sawa, Keita Mizuma, Jingshu Li, Izumi Kida, Yume Mimura, Yuma Ohari, Shinya Tanaka, Masumi Tsuda, Lei Wang, Yoshikata Oda, Zannatul Ferdous, Kenji Shishido, Hiromi Mohri, Miki Iida, Takasuke Fukuhara, Tomokazu Tamura, Rigel Suzuki, Saori Suzuki, Shuhei Tsujino, Hayato Ito, Yu Kaku, Naoko Misawa, Arnon Plianchaisuk, Ziyi Guo, Alfredo A Hinay Jr, Kaoru Usui, Wilaiporn Saikruang, Spyridon Lytras, Keiya Uriu, Ryo Yoshimura, Shusuke Kawakubo, Luca Nishumura, Yusuke Kosugi, Shigeru Fujita, Jarel Elgin M Tolentino, Luo Chen, Lin Pan, Wenye Li, Maximilian Stanley Yo, Kio Horinaka, Mai Suganami, Mika Chiba, Kyoko Yasuda, Keiko Iida, Adam Patrick Strange, Naomi Ohsumi, Shiho Tanaka, Eiko Ogawa, Tsuki Fukuda, Rina Osujo, Kazuhisa Yoshimura, Kenji Sadamas, Mami Nagashima, Hiroyuki Asakura, Isao Yoshida, So Nakagawa, Kazuo Takayama, Rina Hashimoto, Sayaka Deguchi, Yukio Watanabe, Yoshitaka Nakata, Hiroki Futatsusako, Ayaka Sakamoto, Naoko Yasuhara, Tateki Suzuki, Kanako Kimura, Jiei Sasaki, Yukari Nakajima, Takashi Irie, Ryoko Kawabata, Kaori Sasaki-Tabata, Terumasa Ikeda, Hesham Nasser, Ryo Shimizu, Mst Monira Begum, Michael Jonathan, Yuka Mugita, Sharee Leong, Otowa Takahashi, Takamasa Ueno, Chihiro Motozono, Mako Toyoda, Akatsuki Saito, Anon Kosaka, Miki Kawano, Natsumi Matsubara, Tomoko Nishiuchi, Jiri Zahradnik, Prokopios Andrikopoulos, Miguel Padilla-Blanco, Aditi Konar

Affiliations

¹ Laboratory of Medical Virology, Institute for Life and Medical Sciences, Kyoto University, Kyoto, Japan.
² Laboratory of Biomolecular Science and Center for Research and Education on Drug Discovery, Faculty of Pharmaceutical Sciences, Hokkaido University, Sapporo, Japan.
³ Division of Systems Virology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
⁴ Faculty of Liberal Arts, Sophia University, Tokyo, Japan.
⁵ Institute for Vaccine Research and Development, HU-IVReD, Hokkaido University, Sapporo, Japan.
⁶ Global Station for Biosurfaces and Drug Discovery, Hokkaido University, Sapporo, Japan.
⁷ Division of Pathogen Structure, International Institute for Zoonosis Control, Hokkaido University, Sapporo, Japan.
⁸ Faculty of Pharmaceutical Sciences, Kyushu University, Fukuoka, Japan.
⁹ International Research Center for Infectious Diseases, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
¹⁰ Kyoto University Immunomonitoring Center, Kyoto University, Kyoto, Japan.
¹¹ Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.
¹² Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan.
¹³ International Vaccine Design Center, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
¹⁴ Collaboration Unit for Infection, Joint Research Center for Human Retrovirus Infection, Kumamoto University, Kumamoto, Japan.
¹⁵ MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.

^# Contributed equally.

PMID: 39283095
DOI: 10.1128/mbio.03220-23

Abstract

Due to the incessant emergence of various SARS-CoV-2 variants with enhanced fitness in the human population, controlling the COVID-19 pandemic has been challenging. Understanding how the virus enhances its fitness during a pandemic could offer valuable insights for more effective control of viral epidemics. In this manuscript, we review the evolution of SARS-CoV-2 from early 2022 to the end of 2023-from Omicron BA.2 to XBB descendants. Focusing on viral evolution during this period, we provide concrete examples that SARS-CoV-2 has increased its fitness by enhancing several functions of the spike (S) protein, including its binding affinity to the ACE2 receptor and its ability to evade humoral immunity. Furthermore, we explore how specific mutations modify these functions of the S protein through structural alterations. This review provides evolutionary, molecular, and structural insights into how SARS-CoV-2 has increased its fitness and repeatedly caused epidemic surges during the pandemic.

Keywords: Omicron; SARS-CoV-2; evolution; molecular phylogenetic; spike; structural biology.

Publication types

Review