Eukaryotic viruses encode the ribosomal protein eL40

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 

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 

Legendre, M. et al. Pandoravirus Celtis illustrates the microevolution processes at work in the giant Pandoraviridae Genomes. Front. Microbiol. 10, 430 (2019).

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 

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. (2021).

Weynberg, K. D., Allen, M. J., Ashelford, K., Scanlan, D. J. & Wilson, W. H. From small hosts come big viruses: the complete genome of a second Ostreococcus tauri virus, OtV-1. Environ. Microbiol. 11, 2821–2839 (2009).

Article 
CAS 
PubMed 

Google Scholar 

Weynberg, K. D., Allen, M. J., Gilg, I. C., Scanlan, D. J. & Wilson, W. H. Genome sequence of Ostreococcus tauri virus OtV-2 throws light on the role of picoeukaryote niche separation in the ocean▿. J. Virol. 85, 4520–4529 (2011).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Moreau, H. et al. Marine prasinovirus genomes show low evolutionary divergence and acquisition of protein metabolism genes by horizontal gene transfer. J. Virol. 84, 12555–12563 (2010).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Yutin, N. & Koonin, E. V. Proteorhodopsin genes in giant viruses. Biol. Direct 7, 34 (2012).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Philosof, A. & Béjà, O. Bacterial, archaeal and viral-like rhodopsins from the Red Sea. Environ. Microbiol. Rep. 5, 475–482 (2013).

Article 
CAS 
PubMed 

Google Scholar 

Bratanov, D. et al. Unique structure and function of viral rhodopsins. Nat. Commun. 10, 4939 (2019).

Article 
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. (2020).

Zabelskii, D. et al. Structure-based insights into evolution of rhodopsins. Commun. Biol. 4, 1–12 (2021).

Article 

Google Scholar 

Monier, A. et al. Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus. Genome Res. 19, 1441–1449 (2009).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Vardi, A. et al. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326, 861–865 (2009).

Article 
CAS 
PubMed 

Google Scholar 

Kijima, S. et al. Discovery of viral myosin genes with complex evolutionary history within plankton. Front. Microbiol. 12, 683294 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar 

Da Cunha, V. et al. Giant viruses encode actin-related proteins. Mol. Biol. Evol. 39, msac022 (2022).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Schvarcz, C. R. & Steward, G. F. A giant virus infecting green algae encodes key fermentation genes. Virology 518, 423–433 (2018).

Article 
CAS 
PubMed 

Google Scholar 

Claverie, J.-M. & Abergel, C. Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genet. 26, 431–437 (2010).

Article 
CAS 
PubMed 

Google Scholar 

Aylward, F. O. et al. Taxonomic update for giant viruses in the order Imitervirales (phylum Nucleocytoviricota). Arch. Virol. 168, 283 (2023).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

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

Article 
CAS 
PubMed 

Google Scholar 

Bajrai, L. H. et al. Isolation of yasminevirus, the first member of Klosneuvirinae Isolated in coculture with vermamoeba vermiformis, demonstrates an extended arsenal of translational apparatus components. J. Virol. 94, e01534-19 (2019).

Article 
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 

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

Article 
CAS 
PubMed 

Google Scholar 

Mizuno, C. M. et al. Numerous cultivated and uncultivated viruses encode ribosomal proteins. Nat. Commun. 10, 752 (2019).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Mourtada-Maarabouni, M., Kirkham, L., Farzaneh, F. & Williams, G. T. Regulation of apoptosis by fau revealed by functional expression cloning and antisense expression. Oncogene 23, 9419–9426 (2004).

Article 
CAS 
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 

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

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Lecompte, O., Ripp, R., Thierry, J., Moras, D. & Poch, O. Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res. 30, 5382–5390 (2002).

Article 
CAS 
PubMed 
PubMed Central 

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 (2021).

Lauersen, K. J. et al. Peroxisomal microbodies are at the crossroads of acetate assimilation in the green microalga Chlamydomonas reinhardtii. Algal Res. 16, 266–274 (2016).

Article 

Google Scholar 

Boyle, N. R., Sengupta, N. & Morgan, J. A. Metabolic flux analysis of heterotrophic growth in Chlamydomonas reinhardtii. PLoS ONE 12, e0177292 (2017).

Article 
PubMed 
PubMed Central 

Google Scholar 

Delmont, T. O. et al. Functional repertoire convergence of distantly related eukaryotic plankton lineages abundant in the sunlit ocean. Cell Genomics 2, 100123 (2022).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Strauss, J. et al. Plastid-localized xanthorhodopsin increases diatom biomass and ecosystem productivity in iron-limited surface oceans. Nat. Microbiol. (2023).

Olson, D. K., Yoshizawa, S., Boeuf, D., Iwasaki, W. & DeLong, E. F. Proteorhodopsin variability and distribution in the North Pacific Subtropical Gyre. ISME J. 12, 1047–1060 (2018).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Brown, L. S. & Ernst, O. P. Recent advances in biophysical studies of rhodopsins – oligomerization, folding, and structure. Biochim. Biophys. Acta Proteins Proteom. 1865, 1512–1521 (2017).

Article 
CAS 
PubMed 

Google Scholar 

Man, D. et al. Diversification and spectral tuning in marine proteorhodopsins. EMBO J. 22, 1725–1731 (2003).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Martiny, J. B. H., Riemann, L., Marston, M. F. & Middelboe, M. Antagonistic coevolution of marine planktonic viruses and their hosts. Ann. Rev. Mar. Sci. 6, 393–414 (2014).

Article 
PubMed 

Google Scholar 

Frickel, J., Sieber, M. & Becks, L. Eco-evolutionary dynamics in a coevolving host–virus system. Ecol. Lett. 19, 450–459 (2016).

Article 
PubMed 

Google Scholar 

Friman, V.-P. & Buckling, A. Effects of predation on real-time host–parasite coevolutionary dynamics. Ecol. Lett. 16, 39–46 (2013).

Article 
PubMed 

Google Scholar 

Miller, C. M., Selvam, S. & Fuchs, G. Fatal attraction: the roles of ribosomal proteins in the viral life cycle. Wiley Interdiscip. Rev. RNA 12, e1613 (2021).

Article 
CAS 
PubMed 

Google Scholar 

Wang, X., Zhu, J., Zhang, D. & Liu, G. Ribosomal control in RNA virus-infected cells. Front. Microbiol. 13, 1026887 (2022).

Article 
PubMed 
PubMed Central 

Google Scholar 

Chen, L.-X. et al. Phage-encoded ribosomal protein S21 expression is linked to late-stage phage replication. ISME Commun. 2, 1–10 (2022).

Article 

Google Scholar 

Al-Shayeb, B. et al. Clades of huge phages from across Earth’s ecosystems. Nature 578, 425–431 (2020).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Liu, Y. et al. Diversity, taxonomy, and evolution of archaeal viruses of the class Caudoviricetes. PLoS Biol. 19, e3001442 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar 

Michiels, L., Van der Rauwelaert, E., Van Hasselt, F., Kas, K. & Merregaert, J. fau cDNA encodes a ubiquitin-like-S30 fusion protein and is expressed as an antisense sequence in the Finkel-Biskis-Reilly murine sarcoma virus. Oncogene 8, 2537–2546 (1993).

CAS 
PubMed 

Google Scholar 

Martín-Villanueva, S., Gutiérrez, G., Kressler, D. & de la Cruz, J. Ubiquitin and ubiquitin-like proteins and domains in ribosome production and function: chance or necessity? Int J. Mol. Sci. 22, 4359 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar 

Fernández-Pevida, A., Rodríguez-Galán, O., Díaz-Quintana, A., Kressler, D. & de la Cruz, J. Yeast ribosomal protein L40 assembles late into precursor 60 S ribosomes and is required for their cytoplasmic maturation. J. Biol. Chem. 287, 38390–38407 (2012).

Article 
PubMed 
PubMed Central 

Google Scholar 

Zhao, J. et al. Ribosomal protein L40e fused with a ubiquitin moiety is essential for the vegetative growth, morphological homeostasis, cell cycle progression, and pathogenicity of Cryptococcus neoformans. Front. Microbiol. 11, 570269 (2020).

Article 
PubMed 
PubMed Central 

Google Scholar 

Lee, A. S.-Y., Burdeinick-Kerr, R. & Whelan, S. P. J. A ribosome-specialized translation initiation pathway is required for cap-dependent translation of vesicular stomatitis virus mRNAs. Proc. Natl Acad. Sci. USA 110, 324–329 (2013).

Article 
CAS 
PubMed 

Google Scholar 

Iyer, L. M., Balaji, S., Koonin, E. V. & Aravind, L. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res. 117, 156–184 (2006).

Article 
CAS 
PubMed 

Google Scholar 

Lant, S. & Maluquer de Motes, C. Poxvirus interactions with the host ubiquitin system. Pathogens 10, 1034 (2021).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Chen, S. S. & Williamson, J. R. Characterization of the ribosome biogenesis landscape in E. coli using quantitative mass spectrometry. J. Mol. Biol. 425, 767–779 (2013).

Article 
CAS 
PubMed 

Google Scholar 

Watson, Z. L. et al. Structure of the bacterial ribosome at 2 Å resolution. eLife 9, e60482 (2020).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Andreani, J. et al. Orpheovirus IHUMI-LCC2: a new virus among the giant viruses. Front. Microbiol. 8, 2643 (2018).

Schvarcz, C. R. Cultivation And Characterization Of Viruses Infecting Eukaryotic Phytoplankton From The Tropical North Pacific Ocean (2018).

Karl, D. M. & Lukas, R. The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep Sea Res. Part II: Top. Stud. Oceanogr. 43, 129–156 (1996).

Article 
CAS 

Google Scholar 

Keller, M. D., Selvin, R. C., Claus, W. & Guillard, R. R. L. Media for the culture of oceanic ultraphytoplankton1,2. J. Phycol. 23, 633–638 (1987).

Article 

Google Scholar 

Moon-van der Staay, S. Y., De Wachter, R. & Vaulot, D. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409, 607–610 (2001).

Article 
CAS 
PubMed 

Google Scholar 

Worden, A. Picoeukaryote diversity in coastal waters of the Pacific Ocean. Aquat. Microb. Ecol. 43, 165–175 (2006).

Article 

Google Scholar 

Lawrence, J. E. & Steward, G. F. Manual of Aquatic Viral Ecology (eds. Wilhelm, S., Weinbauer, M. & Suttle, C.) 166–181 (American Society of Limnology and Oceanography, 2010).

Patel, A. et al. Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I. Nat. Protoc. 2, 269–276 (2007).

Article 
CAS 
PubMed 

Google Scholar 

Koren, S. et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722–736 (2017).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Chin, C.-S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569 (2013).

Article 
CAS 
PubMed 

Google Scholar 

Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).

Article 
CAS 
PubMed 

Google Scholar 

Schattner, P., Brooks, A. N. & Lowe, T. M. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33, W686–689 (2005).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Chan, P. P. & Lowe, T. M. tRNAscan-SE: searching for tRNA genes in genomic sequences. Methods Mol. Biol. 1962, 1–14 (2019).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).

Article 
CAS 
PubMed 

Google Scholar 

Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Kans, J. Entrez Direct: E-Utilities on the Unix Command Line. Entrez Programming Utilities Help [Internet] (National Center for Biotechnology Information (US), 2021).

Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).

Article 
CAS 
PubMed 

Google Scholar 

Schulz, F. et al. Giant virus diversity and host interactions through global metagenomics. Nature (2020).

Gaïa, M. et al. Mirusviruses link herpesviruses to giant viruses. Nature 616, 783–789 (2023).

Article 
PubMed 
PubMed Central 

Google Scholar 

Zhang, Z. KaKs_Calculator 3.0: calculating selective pressure on coding and non-coding sequences. Genom. Proteom. Bioinform. 20, 536–540 (2022).

Article 
CAS 

Google Scholar 

Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567–580 (2001).

Article 
CAS 
PubMed 

Google Scholar 

Omasits, U., Ahrens, C. H., Müller, S. & Wollscheid, B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30, 884–886 (2014).

Article 
CAS 
PubMed 

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 

Katoh, K. & Standley, D. M. MAFFT Multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Lemoine, F. & Gascuel, O. Gotree/Goalign: toolkit and Go API to facilitate the development of phylogenetic workflows. NAR Genom. Bioinform. 3, lqab075 (2021).

Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).

Article 
CAS 
PubMed 

Google Scholar 

Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).

Article 
CAS 
PubMed 

Google Scholar 

Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128 (2007).

Article 
CAS 
PubMed 

Google Scholar