Insights into phage-bacteria interaction in cold seep Gigantidas platifrons through metagenomics and transcriptome analyses.

Yan Zhang, Hao Chen, Chao Lian, Lei Cao, Yang Guo, Minxiao Wang, Zhaoshan Zhong, Mengna Li, Huan Zhang, Chaolun Li
Author Information
  1. Yan Zhang: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
  2. Hao Chen: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
  3. Chao Lian: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
  4. Lei Cao: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
  5. Yang Guo: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
  6. Minxiao Wang: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China. wangminxiao@qdio.ac.cn.
  7. Zhaoshan Zhong: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
  8. Mengna Li: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
  9. Huan Zhang: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
  10. Chaolun Li: Center of Deep Sea Research, and CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China. lcl@qdio.ac.cn.

Abstract

Viruses are crucial for regulating deep-sea microbial communities and biogeochemical cycles. However, their roles are still less characterized in deep-sea holobionts. Bathymodioline mussels are endemic species inhabiting cold seeps and harboring endosymbionts in gill epithelial cells for nutrition. This study unveiled a diverse array of viruses in the gill tissues of Gigantidas platifrons mussels and analyzed the viral metagenome and transcriptome from the gill tissues of Gigantidas platifrons mussels collected from a cold seep in the South Sea. The mussel gills contained various viruses including Baculoviridae, Rountreeviridae, Myoviridae and Siphovirdae, but the active viromes were Myoviridae, Siphoviridae, and Podoviridae belonging to the order Caudovirales. The overall viral community structure showed significant variation among environments with different methane concentrations. Transcriptome analysis indicated high expression of viral structural genes, integrase, and restriction endonuclease genes in a high methane concentration environment, suggesting frequent virus infection and replication. Furthermore, two viruses (GP-phage-contig14 and GP-phage-contig72) interacted with Gigantidas platifrons methanotrophic gill symbionts (bathymodiolin mussels host intracellular methanotrophic Gammaproteobacteria in their gills), showing high expression levels, and have huge different expression in different methane concentrations. Additionally, single-stranded DNA viruses may play a potential auxiliary role in the virus-host interaction using indirect bioinformatics methods. Moreover, the Cro and DNA methylase genes had phylogenetic similarity between the virus and Gigantidas platifrons methanotrophic gill symbionts. This study also explored a variety of viruses in the gill tissues of Gigantidas platifrons and revealed that bacteria interacted with the viruses during the symbiosis with Gigantidas platifrons. This study provides fundamental insights into the interplay of microorganisms within Gigantidas platifrons mussels in deep sea.

Keywords

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Grants

  1. 42030407/National Natural Science Foundation of China
  2. 2022QNLM030004/Laoshan Laboratory
  3. ZDBS-LY-DQC032/the Key Research Program of Frontier Sciences
  4. XDA22050303/the Strategic Priority Research Program of the Chinese Academy of Sciences

MeSH Term

Animals
Metagenomics
Bacteriophages
Gills
Bivalvia
Gene Expression Profiling
Transcriptome
Virome
Bacteria
Symbiosis
Metagenome

Word Cloud

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