The protein structurome of Orthornavirae and its dark matter

Mutz, Pascal; Camargo, Antonio Pedro; Sahakyan, Harutyun; Neri, Uri; Butkovic, Anamarija; Wolf, Yuri I.; Krupovic, Mart; Dolja, Valerian V.; Koonin, Eugene V.

doi:10.1128/mbio.03200-24

The protein structurome of Orthornavirae and its dark matter

Journal Article · Mon Dec 23 00:00:00 UTC 2024 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.03200-24· OSTI ID:2530328

^[1]; Camargo, Antonio Pedro ^[2]; Sahakyan, Harutyun ^[1]; ^[2]; ^[3]; ^[1]; ^[3]; ^[4]; ^[1]

National Institutes of Health (NIH), Bethesda, MD (United States)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Institut Pasteur, Paris (France); Université Paris Cité (France); Centre National de la Recherche Scientifique (CNRS), Paris (France)
Oregon State Univ., Corvallis, OR (United States)

Metatranscriptomics is uncovering more and more diverse families of viruses with RNA genomes comprising the viral kingdom Orthornavirae in the realm Riboviria. Thorough protein annotation and comparison are essential to get insights into the functions of viral proteins and virus evolution. In addition to sequence- and hmm profile-based methods, protein structure comparison adds a powerful tool to uncover protein functions and relationships. We constructed an Orthornavirae “structurome” consisting of already annotated as well as unannotated (“dark matter”) proteins and domains encoded in viral genomes. We used protein structure modeling and similarity searches to illuminate the remaining dark matter in hundreds of thousands of orthornavirus genomes. The vast majority of the dark matter domains showed either “generic” folds, such as single α-helices, or no high confidence structure predictions. Nevertheless, a variety of lineage-specific globular domains that were new either to orthornaviruses in general or to particular virus families were identified within the proteomic dark matter of orthornaviruses, including several predicted nucleic acid-binding domains and nucleases. In addition, we identified a case of exaptation of a cellular nucleoside monophosphate kinase as an RNA-binding protein in several virus families. Notwithstanding the continuing discovery of numerous orthornaviruses, it appears that all the protein domains conserved in large groups of viruses have already been identified. The rest of the viral proteome seems to be dominated by poorly structured domains including intrinsically disordered ones that likely mediate specific virus-host interactions.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: Fondation pour la Recherche Médicale (FRM); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)

Grant/Contract Number:: AC02-05CH11231; SC0014664

Other Award/Contract Number:: SPF202110014092

OSTI ID:: 2530328

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 2 Vol. 16; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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Data for "The protein structurome of Orthornavirae and its dark matter" Mutz, Pascal; Camargo, Antonio; Sahakyan, Harutyun Zenodo https://doi.org/10.5281/zenodo.13770614	dataset	January 2024
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59 BASIC BIOLOGICAL SCIENCES
Orthornaviria
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novel protein domains
protein structure prediction
proteome

The protein structurome of Orthornavirae and its dark matter

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