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Title: Illuminating structural proteins in viral "dark matter" with metaproteomics

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [1];  [4];  [1];  [5];  [1];  [1]
  1. Univ. of Arizona, Tucson, AZ (United States); The Ohio State Univ., Columbus, OH (United States)
  2. Univ. of Arizona, Tucson, AZ (United States); Univ. of Southern California, Los Angeles, CA (United States)
  3. Univ. of Arizona, Tucson, AZ (United States); Roche Tissue Diagnostics, Oro Valley, AZ (United States)
  4. Univ. of Arizona, Tucson, AZ (United States); Cold Regions Research and Engineering Lab., Hanover, NH (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Texas, El Paso, TX (United States)

Viruses are ecologically important, yet environmental virology is limited by dominance of unannotated genomic sequences representing taxonomic and functional "viral dark matter." Although recent analytical advances are rapidly improving taxonomic annotations, identifying functional darkmatter remains problematic. Here, we apply paired metaproteomics and dsDNA-targeted metagenomics to identify 1,875 virion-associated proteins from the ocean. Over one-half of these proteins were newly functionally annotated and represent abundant and widespread viral metagenome-derived protein clusters (PCs). One primarily unannotated PC dominated the dataset, but structural modeling and genomic context identified this PC as a previously unidentified capsid protein from multiple uncultivated tailed virus families. Furthermore, four of the five most abundant PCs in the metaproteome represent capsid proteins containing the HK97-like protein fold previously found in many viruses that infect all three domains of life. The dominance of these proteins within our dataset, as well as their global distribution throughout the world's oceans and seas, supports prior hypotheses that this HK97-like protein fold is the most abundant biological structure on Earth. Altogether, these culture-independent analyses improve virion-associated protein annotations, facilitate the investigation of proteins within natural viral communities, and offer a high-throughput means of illuminating functional viral dark matter.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE; Work for Others (WFO)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1287026
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, Issue 9; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 47 works
Citation information provided by
Web of Science

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Intriguing Interaction of Bacteriophage-Host Association: An Understanding in the Era of Omics journal April 2017
Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale journal October 2017
Metaproteome analysis reveals that syntrophy, competition, and phage-host interaction shape microbial communities in biogas plants journal April 2019
Single-cell genomics uncover Pelagibacter as the putative host of the extremely abundant uncultured 37-F6 viral population in the ocean journal September 2018
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Diel cycling of the cosmopolitan abundant Pelagibacter virus 37‐F6: one of the most abundant viruses on earth journal February 2020
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