A novel long-tailed myovirus represents a new T4-like cyanophage cluster

Yuanfang Liu; Xue Meng; Hongrui Zheng; Lanlan Cai; Shuzhen Wei; Minglu He; Jiale He; Yue Hao; Chang Ge; Jihua Liu; Feng Chen; Yongle Xu

doi:10.3389/fmicb.2023.1293846

A novel long-tailed myovirus represents a new T4-like cyanophage cluster

Front Microbiol. 2023 Nov 9:14:1293846. doi: 10.3389/fmicb.2023.1293846. eCollection 2023.

Authors

Yuanfang Liu^#¹, Xue Meng^#¹, Hongrui Zheng^#¹, Lanlan Cai², Shuzhen Wei³, Minglu He⁴, Jiale He⁵, Yue Hao⁵, Chang Ge⁵, Jihua Liu¹, Feng Chen⁶, Yongle Xu¹

Affiliations

¹ Institute of Marine Science and Technology, Shandong University, Qingdao, China.
² Department of Ocean Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong SAR, China.
³ State Key Laboratory of Marine Environmental Science, Fujian Key Laboratory of Marine Carbon Sequestration, College of Ocean and Earth Sciences, Xiamen University, Xiamen, China.
⁴ School of Information Science and Engineering, Shandong University, Qingdao, China.
⁵ School of Life Science, Shandong University, Qingdao, China.
⁶ Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, Baltimore, MD, United States.

^# Contributed equally.

Abstract

Cyanophages affect the abundance, diversity, metabolism, and evolution of picocyanobacteria in marine ecosystems. Here we report an estuarine Synechococcus phage, S-CREM2, which represents a novel viral genus and leads to the establishment of a new T4-like cyanophage clade named cluster C. S-CREM2 possesses the longest tail (~418 nm) among isolated cyanomyoviruses and encodes six tail-related proteins that are exclusively homologous to those predicted in the cluster C cyanophages. Furthermore, S-CREM2 may carry three regulatory proteins in the virion, which may play a crucial role in optimizing the host intracellular environment for viral replication at the initial stage of infection. The cluster C cyanophages lack auxiliary metabolic genes (AMGs) that are commonly found in cyanophages of the T4-like clusters A and B and encode unique AMGs like an S-type phycobilin lyase gene. A variation in the composition of tRNA and cis-regulatory RNA genes was observed between the marine and freshwater phage strains in cluster C, reflecting their different modes of coping with hosts and habitats. The cluster C cyanophages are widespread in estuarine and coastal regions and exhibit equivalent or even higher relative abundance compared to those of clusters A and B cyanophages in certain estuarine regions. The isolation of cyanophage S-CREM2 provides new insights into the phage-host interactions mediated by both newly discovered AMGs and virion-associated proteins and emphasizes the ecological significance of cluster C cyanophages in estuarine environments.

Keywords: T4-like cyanophages; auxiliary metabolic gene; cluster C; ecological distribution; longest tail; virion-associated protein.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by Joint Funds of the National Natural Science Foundation of China (U1906216), the National Key Research and Development Program of China (2018YFA0605800), and the National Natural Science Foundation of China (41706161).