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Giant virus diversity and host interactions through global metagenomics

Author

Listed:
  • Frederik Schulz

    (Lawrence Berkeley National Laboratory)

  • Simon Roux

    (Lawrence Berkeley National Laboratory)

  • David Paez-Espino

    (Lawrence Berkeley National Laboratory)

  • Sean Jungbluth

    (Lawrence Berkeley National Laboratory)

  • David A. Walsh

    (Concordia University)

  • Vincent J. Denef

    (University of Michigan)

  • Katherine D. McMahon

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Konstantinos T. Konstantinidis

    (Georgia Institute of Technology)

  • Emiley A. Eloe-Fadrosh

    (Lawrence Berkeley National Laboratory)

  • Nikos C. Kyrpides

    (Lawrence Berkeley National Laboratory)

  • Tanja Woyke

    (Lawrence Berkeley National Laboratory)

Abstract

Our current knowledge about nucleocytoplasmic large DNA viruses (NCLDVs) is largely derived from viral isolates that are co-cultivated with protists and algae. Here we reconstructed 2,074 NCLDV genomes from sampling sites across the globe by building on the rapidly increasing amount of publicly available metagenome data. This led to an 11-fold increase in phylogenetic diversity and a parallel 10-fold expansion in functional diversity. Analysis of 58,023 major capsid proteins from large and giant viruses using metagenomic data revealed the global distribution patterns and cosmopolitan nature of these viruses. The discovered viral genomes encoded a wide range of proteins with putative roles in photosynthesis and diverse substrate transport processes, indicating that host reprogramming is probably a common strategy in the NCLDVs. Furthermore, inferences of horizontal gene transfer connected viral lineages to diverse eukaryotic hosts. We anticipate that the global diversity of NCLDVs that we describe here will establish giant viruses—which are associated with most major eukaryotic lineages—as important players in ecosystems across Earth’s biomes.

Suggested Citation

  • Frederik Schulz & Simon Roux & David Paez-Espino & Sean Jungbluth & David A. Walsh & Vincent J. Denef & Katherine D. McMahon & Konstantinos T. Konstantinidis & Emiley A. Eloe-Fadrosh & Nikos C. Kyrpid, 2020. "Giant virus diversity and host interactions through global metagenomics," Nature, Nature, vol. 578(7795), pages 432-436, February.
  • Handle: RePEc:nat:nature:v:578:y:2020:i:7795:d:10.1038_s41586-020-1957-x
    DOI: 10.1038/s41586-020-1957-x
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    Cited by:

    1. Hanpeng Liao & Chen Liu & Shungui Zhou & Chunqin Liu & David J. Eldridge & Chaofan Ai & Steven W. Wilhelm & Brajesh K. Singh & Xiaolong Liang & Mark Radosevich & Qiu-e Yang & Xiang Tang & Zhong Wei & , 2024. "Prophage-encoded antibiotic resistance genes are enriched in human-impacted environments," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Sofia Rigou & Sébastien Santini & Chantal Abergel & Jean-Michel Claverie & Matthieu Legendre, 2022. "Past and present giant viruses diversity explored through permafrost metagenomics," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Xinzhu Yi & Jie-Liang Liang & Ping Wen & Pu Jia & Shi-wei Feng & Shen-yan Liu & Yuan-yue Zhuang & Yu-qian Guo & Jing-li Lu & Sheng-ji Zhong & Bin Liao & Zhang Wang & Wen-sheng Shu & Jin-tian Li, 2024. "Giant viruses as reservoirs of antibiotic resistance genes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Gonçalo J. Piedade & Max E. Schön & Cédric Lood & Mikhail V. Fofanov & Ella M. Wesdorp & Tristan E. G. Biggs & Lingyi Wu & Henk Bolhuis & Matthias G. Fischer & Natalya Yutin & Bas E. Dutilh & Corina P, 2024. "Seasonal dynamics and diversity of Antarctic marine viruses reveal a novel viral seascape," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Lulu Li & Hehong Zhang & Zihang Yang & Chen Wang & Shanshan Li & Chen Cao & Tongsong Yao & Zhongyan Wei & Yanjun Li & Jianping Chen & Zongtao Sun, 2022. "Independently evolved viral effectors convergently suppress DELLA protein SLR1-mediated broad-spectrum antiviral immunity in rice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Jianhua Wang & Guan-Zhu Han, 2023. "Genome mining shows that retroviruses are pervasively invading vertebrate genomes," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    7. Lingjie Meng & Tom O. Delmont & Morgan Gaïa & Eric Pelletier & Antonio Fernàndez-Guerra & Samuel Chaffron & Russell Y. Neches & Junyi Wu & Hiroto Kaneko & Hisashi Endo & Hiroyuki Ogata, 2023. "Genomic adaptation of giant viruses in polar oceans," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Patrick Arthofer & Florian Panhölzl & Vincent Delafont & Alban Hay & Siegfried Reipert & Norbert Cyran & Stefanie Wienkoop & Anouk Willemsen & Ines Sifaoui & Iñigo Arberas-Jiménez & Frederik Schulz & , 2024. "A giant virus infecting the amoeboflagellate Naegleria," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Alexandra Bessenay & Hugo Bisio & Lucid Belmudes & Yohann Couté & Lionel Bertaux & Jean-Michel Claverie & Chantal Abergel & Sandra Jeudy & Matthieu Legendre, 2024. "Complex transcriptional regulations of a hyperparasitic quadripartite system in giant viruses infecting protists," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Zongzhi Wu & Tang Liu & Qian Chen & Tianyi Chen & Jinyun Hu & Liyu Sun & Bingxue Wang & Wenpeng Li & Jinren Ni, 2024. "Unveiling the unknown viral world in groundwater," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    11. Shaojun Pan & Chengkai Zhu & Xing-Ming Zhao & Luis Pedro Coelho, 2022. "A deep siamese neural network improves metagenome-assembled genomes in microbiome datasets across different environments," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

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