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Significant Differences in Planktonic Virus Communities Between “Cellular Fraction” (0.22 ~ 3.0 µm) and “Viral Fraction” (< 0.22 μm) in the Ocean

  • Microbiology of Aquatic Systems
  • Published:
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Abstract

Compared to free-living viruses (< 0.22 m) in the ocean, planktonic viruses in the “cellular fraction” (0.22 ~ 3.0 μm) are now far less well understood, and the differences between them remain largely unexplored. Here, we revealed that even in the same seawater samples, the “cellular fraction” comprised significantly distinct virus communities from the free virioplankton, with only 13.87% overlap in viral contigs at the species level. Compared to the viral genomes deposited in NCBI RefSeq database, 99% of the assembled viral genomes in the “cellular fraction” represented novel genera. Notably, the assembled (near-) complete viral genomes within the “cellular fraction” were significantly larger than that in the “viral fraction,” and the “cellular fraction” contained three times more species of giant viruses or jumbo phages with genomes > 200 kb than the “viral fraction.” The longest complete genomes of jumbo phage (~ 252 kb) and giant virus (~ 716 kb) were both detected only in the “cellular fraction.” Moreover, a relatively higher proportion of proviruses were predicted within the “cellular fraction” than “viral fraction.” Besides the substantial divergence in viral community structure, the different fractions also contained their unique viral auxiliary metabolic genes; e.g., those potentially participating in inorganic carbon fixation in deep sea were detected only in the “cellular-fraction” viromes. In addition, there was a considerable divergence in the community structure of both “cellular fraction” and “viral fraction” viromes between the surface and deep-sea habitats, suggesting that they might have similar environmental adaptation properties. The findings deepen our understanding of the complexity of viral community structure and function in the ocean.

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Data Availability

The CVC and VVC datasets reported in this study have been deposited in the Genome Warehouse in the National Genomics Data Center [104], Beijing Institute of Genomics (China National Center for Bioinformation), Chinese Academy of Sciences, under BioProject accession number PRJCA002898 and BioSample accession number SAMC231958 and SAMC231959, respectively. The CVG and VVG datasets have been deposited under BioSample accession number SAMC195331 and SAMC195332, respectively. The C-vMAGs and V-vMAGs datasets have been deposited under BioSample accession number SAMC1000078 and SAMC1000079, respectively. They are publicly accessible at https://bigd.big.ac.cn/gwh. Raw data files and R codes for statistical analyses have been deposited in the Figshare: https://doi.org/10.6084/m9.figshare.c.5984017.v4.

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Funding

This work was funded by the National Natural Science Foundation of China (No. 41876174, 42206124, 42106107, 42006093); the Senior User Project of RV KEXUE (KEXUE2019GZ03) supported by the Center for Ocean Mega-Science, Chinese Academy of Sciences; and the open research cruise NORC2017-05 supported by an NSFC Ship-time Sharing Project.

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Author notes

  1. Jiulong Zhao and Zengmeng Wang contributed equally to this work.

Authors and Affiliations

  1. Shandong Provincial Key Laboratory of Energy Genetics, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, 266101, China

    Jiulong Zhao, Zengmeng Wang, Chengcheng Li, Tongmei Shi, Yantao Liang & Yongyu Zhang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Jiulong Zhao, Zengmeng Wang, Tongmei Shi & Yongyu Zhang

  3. State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, 361005, China

    Nianzhi Jiao

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  1. Jiulong Zhao
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Contributions

Y.Z. and N.J. designed the experiment. J.Z. and Z.W. conducted the experiments and performed the metagenomic analysis. C.L., T.S., and Y.L. collected the samples. J.Z., Z.W., and Y.Z. wrote the manuscript.

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Correspondence to Yongyu Zhang.

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The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

248_2022_2167_MOESM1_ESM.pdf

Supplementary file1 Fig. S1: Workflow of metagenomic sampling, sequencing, assembly, and creation of the South China Sea viral genome datasets. Fig. S2: Abundance profiles of free virus-like particles and prokaryotes in the seawater. (a) The abundance of virus-like particles and prokaryotes in all the samples. The virus-to-prokaryote ratio (VPR) of each sample was calculated by dividing the abundance of free virus-like particles by the abundance of prokaryotes. The error bars represent the standard deviation of three measurements. (b) The correlation between prokaryotic abundance and viral-like particle (VLP) abundance in all the samples. Fig. S3: Distribution of size and GC content (%) of CVCs/VVCs (a) and CVGs/ VVGs (b). Fig. S4: Phylogenetic analysis of the CVGs obtained from the ‘cellular-fraction’ metagenomes and reference viral genomes. Branches in red indicate the viral genomes from this study, whereas those in black indicate reference viral genomes retrieved from the NCBI RefSeq Virus database. The rings outside the tree represent (from inside to outside) the CVGs, the virus family, and the host group. Fig. S5: Phylogenetic analysis of the VVGs obtained from the ‘viral-fraction’ metagenomesand reference viral genomes. Branches in red indicate the viral genomes from this study, whereas those in black indicate the reference viral genomes retrieved from the NCBI RefSeq Virus database. The rings outside the tree represent (from inside to outside) the VVGs, the virus family, and the host group. Fig. S6: Genome map of CVG_41. The rings (from inside to outside) represent GC Skew (Ring 1), GC content (Ring 2), the direction of transcription (Ring 3), and gene features (i.e., functional genes, hypothetical protein, and unknown function) (Ring 4). Fig. S7: Annotation of the genes encoded by viruses in the CVC (a) and VVC (b) datasets against the eggNOG 5.0 database. Colors in pie charts represent the number of genes; red as the annotated genes, and blue as unknown. Fig. S8: Percentage of viral contigs having predicted hosts in the ‘cellular fraction’ and ‘viral fraction’ (pie charts), and predicted host composition grouped by phylum (class for Proteobacteria) in the two fractions (bar plots). Fig. S9: Proteomic tree representing the proteome-wide similarity relationships between the longest viral MAGs (C-S3C4721) and 112 reference eukaryotic viral genomes. The inner ring represents the virus family, and the outer ring represents the host group. (PDF 13361 KB)

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Zhao, J., Wang, Z., Li, C. et al. Significant Differences in Planktonic Virus Communities Between “Cellular Fraction” (0.22 ~ 3.0 µm) and “Viral Fraction” (< 0.22 μm) in the Ocean. Microb Ecol 86, 825–842 (2023). https://doi.org/10.1007/s00248-022-02167-6

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