Numerous cultivated and uncultivated viruses encode ribosomal proteins

Mizuno, Carolina M.; Guyomar, Charlotte; Roux, Simon; Lavigne, Régis; Rodriguez-Valera, Francisco; Sullivan, Matthew B.; Gillet, Reynald; Forterre, Patrick; Krupovic, Mart

doi:10.1038/s41467-019-08672-6

Title: Numerous cultivated and uncultivated viruses encode ribosomal proteins

Journal Article · Wed Feb 13 23:00:00 EST 2019 · Nature Communications

DOI: https://doi.org/10.1038/s41467-019-08672-6 · OSTI ID:1580378

Mizuno, Carolina M. ^[1]; Guyomar, Charlotte ^[2];

^[3]; Lavigne, Régis ^[4];

^[5]; Sullivan, Matthew B. ^[6]; Gillet, Reynald ^[2]; Forterre, Patrick ^[1];

^[1]

Inst. Pasteur, Paris (France)
Univ. Rennes, Rennes (France). Inst. de génétique et développement de Rennes (IGDR)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Univ. Rennes, Rennes (France). Inst. de recherche en santé environnement et travail (Irset)
Univ. Miguel Hernandez, Alicante (Spain)
The Ohio State Univ., Columbus, OH (United States)

Viruses modulate ecosystems by directly altering host metabolisms through auxiliary metabolic genes. However, viral genomes are not known to encode the core components of translation machinery, such as ribosomal proteins (RPs). Here, using reference genomes and global-scale viral metagenomic datasets, we identify 14 different RPs across viral genomes arising from cultivated viral isolates and metagenome-assembled viruses. Viruses tend to encode dynamic RPs, easily exchangeable between ribosomes, suggesting these proteins can replace cellular versions in host ribosomes. Functional assays confirm that the two most common virus-encoded RPs, bS21 and bL12, are incorporated into 70S ribosomes when expressed in Escherichia coli. Ecological distribution of virus-encoded RPs suggests some level of ecosystem adaptations as aquatic viruses and viruses of animal-associated bacteria are enriched for different subsets of RPs. Finally, RP genes are under purifying selection and thus likely retained an important function after being horizontally transferred into virus genomes.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Gordon and Betty Moore Foundation (GBMF); National Science Foundation (NSF); General Directorate of Armaments and Ministry of Higher Education and Research of France; European Commission

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1580378

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 10; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Photosynthesis genes in marine viruses yield proteins during host infection Lindell, Debbie; Jaffe, Jacob D.; Johnson, Zackary I. Nature, Vol. 438, Issue 7064 https://doi.org/10.1038/nature04111	journal	October 2005
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The Dormancy Regulator DosR Controls Ribosome Stability in Hypoxic Mycobacteria Trauner, Andrej; Lougheed, Kathryn E. A.; Bennett, Mark H. Journal of Biological Chemistry, Vol. 287, Issue 28 https://doi.org/10.1074/jbc.M112.364851	journal	April 2012
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Protein L5 is crucial for in vivo assembly of the bacterial 50S ribosomal subunit central protuberance Korepanov, Alexey P.; Korobeinikova, Anna V.; Shestakov, Sergey A. Nucleic Acids Research, Vol. 40, Issue 18 https://doi.org/10.1093/nar/gks676	journal	July 2012
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
Assessment of viral community functional potential from viral metagenomes may be hampered by contamination with cellular sequences Roux, Simon; Krupovic, Mart; Debroas, Didier Open Biology, Vol. 3, Issue 12 https://doi.org/10.1098/rsob.130160	journal	December 2013
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Sulfur Oxidation Genes in Diverse Deep-Sea Viruses Anantharaman, K.; Duhaime, M. B.; Breier, J. A. Science, Vol. 344, Issue 6185 https://doi.org/10.1126/science.1252229	journal	May 2014
Giant viruses with an expanded complement of translation system components Schulz, Frederik; Yutin, Natalya; Ivanova, Natalia N. Science, Vol. 356, Issue 6333 https://doi.org/10.1126/science.aal4657	journal	April 2017
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A Gripping Tale of Ribosomal Frameshifting: Extragenic Suppressors of Frameshift Mutations Spotlight P-Site Realignment Atkins, J. F.; Bjork, G. R. Microbiology and Molecular Biology Reviews, Vol. 73, Issue 1 https://doi.org/10.1128/MMBR.00010-08	journal	March 2009
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Phage-Encoded Anti-CRISPR Defenses Stanley, Sabrina Y.; Maxwell, Karen L. Annual Review of Genetics, Vol. 52, Issue 1 https://doi.org/10.1146/annurev-genet-120417-031321	journal	November 2018
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