Energetic cost of building a virus
Viruses are incapable of autonomous energy production. Although many experimental studies make it clear that viruses are parasitic entities that hijack the molecular resources of the host, a detailed estimate for the energetic cost of viral synthesis is largely lacking. To quantify the energetic cost of viruses to their hosts, we enumerated the costs associated with two very distinct but representative DNA and RNA viruses, namely, T4 and influenza. We found that, for these viruses, translation of viral proteins is the most energetically expensive process. Interestingly, the costs of building a T4 phage and a single influenza virus are nearly the same. Due to influenza's higher burst size, however, the overall cost of a T4 phage infection is only 2–3% of the cost of an influenza infection. The costs of these infections relative to their host's estimated energy budget during the infection reveal that a T4 infection consumes about a third of its host's energy budget, whereas an influenza infection consumes only ≈ 1%. Building on our estimates for T4, we show how the energetic costs of double-stranded DNA phages scale with the capsid size, revealing that the dominant cost of building a virus can switch from translation to genome replication above a critical size. Last, using our predictions for the energetic cost of viruses, we provide estimates for the strengths of selection and genetic drift acting on newly incorporated genetic elements in viral genomes, under conditions of energy limitation.
© 2017 National Academy of Sciences. Freely available online through the PNAS open access option. Edited by Ned S. Wingreen, Princeton University, Princeton, NJ, and accepted by Editorial Board Member Curtis G. Callan Jr. April 19, 2017 (received for review January 30, 2017). Published ahead of print May 16, 2017. We are grateful to David Baltimore, Markus Covert, Michael Lynch, Bill Gelbart, Joshua Weitz, Forest Rohwer, Thierry Mora, Aleksandra Walczak, Ry Young, David Van Valen, Georgi Marinov, Elsa Birch, Yinon Bar-On, Ty Roach, Franz Weinert, as well as members of the R.P. Laboratory and the Boundaries of Life Initiative for their many insightful recommendations. This study was supported by the National Science Foundation Graduate Research Fellowship (Grant DGE‐1144469), The John Templeton Foundation (Boundaries of Life Initiative; Grant 51250), the National Institute of Health's Maximizing Investigator's Research Award (Grant RFA-GM-17-002), the National Institute of Health's Exceptional Unconventional Research Enabling Knowledge Acceleration (Grant R01- GM098465), and the National Science Foundation (Grant NSF PHY11-25915) through the 2015 Cellular Evolution course at the Kavli Institute for Theoretical Physics. Author contributions: G.M., R.M., and R.P. designed research, performed research, analyzed data, and wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. N.S.W. is a guest editor invited by the Editorial Board. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1701670114/-/DCSupplemental.
Published - PNAS-2017-Mahmoudabadi-E4324-33.pdf
Submitted - 1701.02565.pdf
Supplemental Material - pnas.1701670114.sd01.xlsx
Supplemental Material - pnas.1701670114.sd02.xlsx
Supplemental Material - pnas.1701670114.sd03.xlsx
Supplemental Material - pnas.201701670SI.pdf
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