Expansion of the genomic and functional diversity of global ocean giant viruses

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  • Aylward, F. O. & Moniruzzaman, M. Viral complexity. Biomolecules 12, 1061 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abrahão, J. et al. Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat. Commun. 9, 749 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • Philippe, N. et al. Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341, 281–286 (2013).

    Article  CAS  PubMed  Google Scholar 

  • Aherfi, S. et al. Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?. ISME J. 16, 695–704 (2022).

    Article  CAS  PubMed  Google Scholar 

  • Ha, A. D., Moniruzzaman, M. & Aylward, F. O. High transcriptional activity and diverse functional repertoires of hundreds of giant viruses in a coastal marine system. mSystems 6, e0029321 (2021).

    Article  PubMed  Google Scholar 

  • Wilson, W. H. et al. Genomic exploration of individual giant ocean viruses. ISME J. 11, 1736–1745 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • Aylward, F. O., Moniruzzaman, M., Ha, A. D. & Koonin, E. V. A phylogenomic framework for charting the diversity and evolution of giant viruses. PLOS Biol. 19, e3001430 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moniruzzaman, M. et al. Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics. Nat. Commun. 8, 16054 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, T.-W. et al. Host range and coding potential of eukaryotic giant viruses. Viruses 12, 1337 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  • Hingamp, P. et al. Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J. 7, 1678–1679 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz, F. et al. Hidden diversity of soil giant viruses. Nat. Commun. 9, 4881 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • Benoiston, A.-S. The evolution of diatoms and their biogeochemical functions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160397 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • Sherr, E. B. & Sherr, B. F. Bacterivory and herbivory: key roles of phagotrophic protists in pelagic food webs. Microb. Ecol. 28, 223–235 (1994).

    Article  CAS  PubMed  Google Scholar 

  • Blanc-Mathieu, R. et al. A persistent giant algal virus, with a unique morphology, encodes an unprecedented number of genes involved in energy metabolism. J. Virol. 95, e02446–20 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ku, C. Giant virus-eukaryote interactions as ecological and evolutionary driving forces. mSystems 6, e0073721 (2021).

    Article  PubMed  Google Scholar 

  • Moniruzzaman, M. et al. Virologs, viral mimicry, and virocell metabolism: the expanding scale of cellular functions encoded in the complex genomes of giant viruses. FEMS Microbiol. Rev. 47, fuad053 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  • Monier, A. et al. Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton. Proc. Natl. Acad. Sci. 114, E7489–E7498 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plugge, B. et al. A potassium channel protein encoded by Chlorella virus PBCV-1. Science 287, 1641–1644 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Kaneko, H. et al. Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean. iScience 24, 102002 (2021).

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea: viruses play critical roles in the structure and function of aquatic food webs. BioScience 49, 781–788 (1999).

    Article  Google Scholar 

  • Meints, R. H., Van Etten, J. L., Kuczmarski, D., Lee, K. & Ang, B. Viral infection of the symbiotic chlorella-like alga present in Hydra viridis. Virology 113, 698–703 (1981).

    Article  CAS  PubMed  Google Scholar 

  • Scola, B. L. et al. A giant virus in amoebae. Science 299, 2033–2033 (2003).

    Article  PubMed  Google Scholar 

  • Raoult, D. et al. The 1.2-megabase genome sequence of mimivirus. Science 306, 1344–1350 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Francis, R., Ominami, Y., Bou Khalil, J. Y. & La Scola, B. High-throughput isolation of giant viruses using high-content screening. Commun. Biol. 2, 216 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  • Khalil, J. Y. B. et al. High-throughput isolation of giant viruses in liquid medium using automated flow cytometry and fluorescence staining. Front. Microbiol. 7, 26 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulz, F., Abergel, C. & Woyke, T. Giant virus biology and diversity in the era of genome-resolved metagenomics. Nat. Rev. Microbiol. 20, 721–736 (2022).

    Article  CAS  PubMed  Google Scholar 

  • Cook, R. et al. INfrastructure for a PHAge REference database: identification of large-scale biases in the current collection of cultured phage genomes. PHAGE 2, 214–223 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  • Blackwell, G. A. et al. Exploring bacterial diversity via a curated and searchable snapshot of archived DNA sequences. PLOS Biol. 19, e3001421 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andreani, J., Verneau, J., Raoult, D., Levasseur, A. & La Scola, B. Deciphering viral presences: two novel partial giant viruses detected in marine metagenome and in a mine drainage metagenome. Virol. J. 15, 66 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • Colson, P., Scola, B. L. & Raoult, D. Giant viruses of amoebae as potential human pathogens. Intervirology 56, 376–385 (2013).

    Article  PubMed  Google Scholar 

  • Ghedin, E. & Claverie, J.-M. Mimivirus relatives in the Sargasso sea. Virol. J. 2, 62 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  • Kristensen, D. M., Mushegian, A. R., Dolja, V. V. & Koonin, E. V. New dimensions of the virus world discovered through metagenomics. Trends Microbiol. 18, 11–19 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Loh, J. et al. Detection of novel sequences related to African Swine Fever virus in human serum and sewage. J. Virol. 83, 13019–13025 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monier, A., Claverie, J.-M. & Ogata, H. Taxonomic distribution of large DNA viruses in the sea. Genome Biol. 9, R106 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  • Mihara, T. et al. Taxon richness of ‘megaviridae’ exceeds those of bacteria and archaea in the ocean. Microbes Environ. 33, 162–171 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • Yau, S. et al. Virophage control of Antarctic algal host–virus dynamics. Proc. Natl. Acad. Sci. 108, 6163–6168 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, W. et al. Four novel algal virus genomes discovered from Yellowstone Lake metagenomes. Sci. Rep. 5, 15131 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bäckström, D. et al. Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism. mBio 10, e02497–18 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, H. et al. The genome of a prasinoviruses-related freshwater virus reveals unusual diversity of phycodnaviruses. BMC Genomics 19, 49 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulz, F. et al. Giant viruses with an expanded complement of translation system components. Science 356, 82–85 (2017).

    Article  CAS  PubMed  Google Scholar 

  • Schulz, F. et al. Giant virus diversity and host interactions through global metagenomics. Nature 578, 432–436 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moniruzzaman, M., Martinez-Gutierrez, C. A., Weinheimer, A. R. & Aylward, F. O. Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses. Nat. Commun. 11, 1710 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaïa M. et al., “Mirusviruses link herpesviruses to giant viruses,” Nature. 1–7 https://doi.org/10.1038/s41586-023-05962-4 (2023).

  • Minch, B. and Moniruzzaman, M., BEREN: A bioinformatic tool for recovering Giant viruses, Polinton-like Viruses, and Virophages in metagenomic data. bioRxiv, pp.2024-10. (2024).

  • Farzad, R., Ha, A. D. & Aylward, F. O. Diversity and genomics of giant viruses in the North Pacific Subtropical Gyre. Front. Microbiol. 13, 1021923 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  • Acquisti, C., Kumar, S. & Elser, J. J. Signatures of nitrogen limitation in the elemental composition of the proteins involved in the metabolic apparatus. Proc. R. Soc. B Biol. Sci. 276, 2605–2610 (2009).

    Article  CAS  Google Scholar 

  • Valero-Mora, P. M. ggplot2: elegant graphics for data analysis. J. Stat. Softw. 35, 1–3 (2010).

    Article  Google Scholar 

  • Koonin, E. V. & Yutin, N. Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses. Intervirology 53, 284–292 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  • Legendre, M. et al. mRNA deep sequencing reveals 75 new genes and a complex transcriptional landscape in Mimivirus. Genome Res. 20, 664–674 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chelikani, V., Ranjan, T. & Kondabagil, K. Revisiting the genome packaging in viruses with lessons from the ‘Giants. Virology 466–467, 15–26 (2014).

    Article  PubMed  Google Scholar 

  • Ha, A. D., Moniruzzaman, M. & Aylward, F. O. Assessing the biogeography of marine giant viruses in four oceanic transects. ISME Commun. 3, 43 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  • Chase, E. E., Truchon, A. R., Creasey, B. A. & Wilhelm, S. W. Time of day of infection shapes development of a eukaryotic algal-Nucleocytoviricota virocell. FEMS Microb. Ecol. 100, https://doi.org/10.1093/femsec/fiae123 (2024).

  • Gilbert, N. E. et al. Giant virus infection signatures are modulated by Euphotic Zone Depth Strata and iron regimes of the Subantarctic Southern Ocean. mSystems 8, e01260–22 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  • Meng, L. et al. Genomic adaptation of giant viruses in polar oceans. Nat. Commun. 14, 6233 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Needham, D. M. et al. A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. Proc. Natl. Acad. Sci. USA 116, 20574–20583 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rozenberg, A. et al. Lateral gene transfer of anion-conducting channelrhodopsins between green algae and giant viruses. Curr. Biol. CB 30, 4910–4920.e5 (2020).

    Article  CAS  PubMed  Google Scholar 

  • Zabelskii, D. et al. Viral rhodopsins 1 are an unique family of light-gated cation channels. Nat. Commun. 11, 5707 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gann, E. R., Gainer, P. J., Reynolds, T. B. & Wilhelm, S. W. Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a ‘giant virus. PLOS ONE 15, e0226758 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thamatrakoln, K. et al. Light regulation of coccolithophore host–virus interactions. N. Phytol. 221, 1289–1302 (2019).

    Article  CAS  Google Scholar 

  • Juneau, P., Lawrence, J., Suttle, C. & Harrison, P. Effects of viral infection on photosynthetic processes in the bloom-forming alga Heterosigma akashiwo. Aquat. Microb. Ecol. 31, 9–17 (2003).

    Article  Google Scholar 

  • Seaton, G. G. R., Lee, K. & Rohozinski, J. Photosynthetic shutdown in Chlorella NC64A associated with the infection cycle of Paramecium bursaria Chlorella Virus-1. Plant Physiol. 108, 1431–1438 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philosof, A., Battchikova, N., Aro, E. M. & Béja, O. Marine cyanophages: tinkering with the electron transport chain. ISME J. 5, 1568–1570 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharon, I. et al. Photosystem I gene cassettes are present in marine virus genomes. Nature 461, 258–262 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finke, J. F., Hunt, B. P. V., Winter, C., Carmack, E. C. & Suttle, C. A. Nutrients and other environmental factors influence virus abundances across oxic and hypoxic marine environments. Viruses 9, 152 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin M., “Cutadapt removes adapter sequences from high-throughput sequencing reads,” EMBnet.journal, 17, 1, https://doi.org/10.14806/ej.17.1.200 2011.

  • Li, D., Liu, C.-M., Luo, R., Sadakane, K. & Lam, T.-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).

    Article  CAS  PubMed  Google Scholar 

  • Kang, D. D. et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 7, e7359 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  • Aylward, F. O. & Moniruzzaman, M. ViralRecall—a flexible command-line tool for the detection of giant virus signatures in ‘omic data. Viruses 13, 150 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864–2868 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen, W., Le, S., Li, Y. & Hu, F. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLOS ONE 11, e0163962 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  • Grzymski, J. J. & Dussaq, A. M. The significance of nitrogen cost minimization in proteomes of marine microorganisms. ISME J. 6, 71–80 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Ha, A. D. & Aylward, F. O. Automated classification of giant virus genomes using a random forest model built on trademark protein families. Npj Viruses 2, 1–9 (2024).

    Article  Google Scholar 

  • Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).

    Article  CAS  PubMed  Google Scholar 

  • Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camargo, A. P. et al. Identification of mobile genetic elements with geNomad. Nat. Biotechnol. 42, 1303–1312 (2024).

    Article  CAS  PubMed  Google Scholar 

  • Mistry, J. et al. Pfam: The protein families database in 2021. Nucleic Acids Res. 49, D412–D419 (2021).

    Article  CAS  PubMed  Google Scholar 

  • Grazziotin, A. L., Koonin, E. V. & Kristensen, D. M. Prokaryotic Virus Orthologous Groups (pVOGs): a resource for comparative genomics and protein family annotation. Nucleic Acids Res. 45, D491–D498 (2017).

    Article  CAS  PubMed  Google Scholar 

  • Tatusov, R. L., Galperin, M. Y., Natale, D. A. & Koonin, E. V. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33–36 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinegger, M. & Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026–1028 (2017).

    Article  CAS  PubMed  Google Scholar 

  • Eren, A. M. et al. Community-led, integrated, reproducible multi-omics with anvi’o. Nat. Microbiol. 6, 3–6 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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