Energetic cost of building a virus

Proc Natl Acad Sci U S A. 2017 May 30;114(22):E4324-E4333. doi: 10.1073/pnas.1701670114. Epub 2017 May 16.

Abstract

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.

Keywords: T4; cellular energetics; influenza; viral energetics; viral evolution.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alphainfluenzavirus / growth & development
  • Alphainfluenzavirus / metabolism
  • Animals
  • Bacteriophage T4 / growth & development
  • Bacteriophage T4 / metabolism
  • Energy Metabolism
  • Host-Pathogen Interactions / physiology*
  • Humans
  • Kinetics
  • Models, Biological
  • Viruses / growth & development*
  • Viruses / metabolism*