Structural and Proteomic Studies of the Aureococcus anophagefferens Virus Demonstrate a Global Distribution of Virus-Encoded Carbohydrate Processing
Abstract
Viruses modulate the function(s) of environmentally relevant microbial populations, yet considerations of the metabolic capabilities of individual virus particles themselves are rare. We used shotgun proteomics to quantitatively identify 43 virus-encoded proteins packaged within purified Aureococcus anophagefferens Virus (AaV) particles, normalizing data to the per-virion level using a 9.5-Å-resolution molecular reconstruction of the 1900-Å (AaV) particle that we generated with cryogenic electron microscopy. This packaged proteome was used to determine similarities and differences between members of different giant virus families. We noted that proteins involved in sugar degradation and binding (e.g., carbohydrate lyases) were unique to AaV among characterized giant viruses. To determine the extent to which this virally encoded metabolic capability was ecologically relevant, we examined the TARA Oceans dataset and identified genes and transcripts of viral origin. Our analyses demonstrated that putative giant virus carbohydrate lyases represented up to 17% of the marine pool for this function. In total, our observations suggest that the AaV particle has potential prepackaged metabolic capabilities and that these may be found in other giant viruses that are widespread and abundant in global oceans.
- Authors:
-
[3];
[3];
- Univ. of Tennessee, Knoxville, TN (United States)
- Univ. of Texas at El Paso, TX (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Institutes of Health (NIH)
- OSTI Identifier:
- 1767873
- Grant/Contract Number:
- AC05-00OR22725; IOS1922958; EMS4971; U24GM116787; U24GM116792; R01GM129525
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; giant viruses; viro-cell metabolism; proteomics; cryo-EM; carbohydrate lyases
Citation Formats
Gann, Eric R., Xian, Yuejiao, Abraham, Paul E., Hettich, Robert L., Reynolds, Todd B., Xiao, Chuan, and Wilhelm, Steven W. Structural and Proteomic Studies of the Aureococcus anophagefferens Virus Demonstrate a Global Distribution of Virus-Encoded Carbohydrate Processing. United States: N. p., 2020.
Web. doi:10.3389/fmicb.2020.02047.
Gann, Eric R., Xian, Yuejiao, Abraham, Paul E., Hettich, Robert L., Reynolds, Todd B., Xiao, Chuan, & Wilhelm, Steven W. Structural and Proteomic Studies of the Aureococcus anophagefferens Virus Demonstrate a Global Distribution of Virus-Encoded Carbohydrate Processing. United States. https://doi.org/10.3389/fmicb.2020.02047
Gann, Eric R., Xian, Yuejiao, Abraham, Paul E., Hettich, Robert L., Reynolds, Todd B., Xiao, Chuan, and Wilhelm, Steven W. Tue .
"Structural and Proteomic Studies of the Aureococcus anophagefferens Virus Demonstrate a Global Distribution of Virus-Encoded Carbohydrate Processing". United States. https://doi.org/10.3389/fmicb.2020.02047. https://www.osti.gov/servlets/purl/1767873.
@article{osti_1767873,
title = {Structural and Proteomic Studies of the Aureococcus anophagefferens Virus Demonstrate a Global Distribution of Virus-Encoded Carbohydrate Processing},
author = {Gann, Eric R. and Xian, Yuejiao and Abraham, Paul E. and Hettich, Robert L. and Reynolds, Todd B. and Xiao, Chuan and Wilhelm, Steven W.},
abstractNote = {Viruses modulate the function(s) of environmentally relevant microbial populations, yet considerations of the metabolic capabilities of individual virus particles themselves are rare. We used shotgun proteomics to quantitatively identify 43 virus-encoded proteins packaged within purified Aureococcus anophagefferens Virus (AaV) particles, normalizing data to the per-virion level using a 9.5-Å-resolution molecular reconstruction of the 1900-Å (AaV) particle that we generated with cryogenic electron microscopy. This packaged proteome was used to determine similarities and differences between members of different giant virus families. We noted that proteins involved in sugar degradation and binding (e.g., carbohydrate lyases) were unique to AaV among characterized giant viruses. To determine the extent to which this virally encoded metabolic capability was ecologically relevant, we examined the TARA Oceans dataset and identified genes and transcripts of viral origin. Our analyses demonstrated that putative giant virus carbohydrate lyases represented up to 17% of the marine pool for this function. In total, our observations suggest that the AaV particle has potential prepackaged metabolic capabilities and that these may be found in other giant viruses that are widespread and abundant in global oceans.},
doi = {10.3389/fmicb.2020.02047},
journal = {Frontiers in Microbiology},
number = 1,
volume = 11,
place = {United States},
year = {Tue Sep 08 00:00:00 EDT 2020},
month = {Tue Sep 08 00:00:00 EDT 2020}
}
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