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Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses

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  • Mohammad Moniruzzaman

    (Department of Biological Sciences, Virginia Tech)

  • Carolina A. Martinez-Gutierrez

    (Department of Biological Sciences, Virginia Tech)

  • Alaina R. Weinheimer

    (Department of Biological Sciences, Virginia Tech)

  • Frank O. Aylward

    (Department of Biological Sciences, Virginia Tech)

Abstract

The discovery of eukaryotic giant viruses has transformed our understanding of the limits of viral complexity, but the extent of their encoded metabolic diversity remains unclear. Here we generate 501 metagenome-assembled genomes of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) from environments around the globe, and analyze their encoded functional capacity. We report a remarkable diversity of metabolic genes in widespread giant viruses, including many involved in nutrient uptake, light harvesting, and nitrogen metabolism. Surprisingly, numerous NCLDV encode the components of glycolysis and the TCA cycle, suggesting that they can re-program fundamental aspects of their host’s central carbon metabolism. Our phylogenetic analysis of NCLDV metabolic genes and their cellular homologs reveals distinct clustering of viral sequences into divergent clades, indicating that these genes are virus-specific and were acquired in the distant past. Overall our findings reveal that giant viruses encode complex metabolic capabilities with evolutionary histories largely independent of cellular life, strongly implicating them as important drivers of global biogeochemical cycles.

Suggested Citation

  • Mohammad Moniruzzaman & Carolina A. Martinez-Gutierrez & Alaina R. Weinheimer & Frank O. Aylward, 2020. "Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-15507-2
    DOI: 10.1038/s41467-020-15507-2
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    Cited by:

    1. Hugo Bisio & Matthieu Legendre & Claire Giry & Nadege Philippe & Jean-Marie Alempic & Sandra Jeudy & Chantal Abergel, 2023. "Evolution of giant pandoravirus revealed by CRISPR/Cas9," Nature Communications, Nature, vol. 14(1), pages 1-15, 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. 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.
    4. Qianqian Shao & Irina V. Agarkova & Eric A. Noel & David D. Dunigan & Yunshu Liu & Aohan Wang & Mingcheng Guo & Linlin Xie & Xinyue Zhao & Michael G. Rossmann & James L. Etten & Thomas Klose & Qiangli, 2022. "Near-atomic, non-icosahedrally averaged structure of giant virus Paramecium bursaria chlorella virus 1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. 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.
    6. Ana-Sofia Eria-Oliveira & Mathilde Folacci & Anne Amandine Chassot & Sandrine Fedou & Nadine Thézé & Dmitrii Zabelskii & Alexey Alekseev & Ernst Bamberg & Valentin Gordeliy & Guillaume Sandoz & Michel, 2024. "Hijacking of internal calcium dynamics by intracellularly residing viral rhodopsins," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    7. 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.

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