The elemental composition of virus particles: implications for marine biogeochemical cycles

Journal name:
Nature Reviews Microbiology
Volume:
12,
Pages:
519–528
Year published:
DOI:
doi:10.1038/nrmicro3289
Published online

Abstract

In marine environments, virus-mediated lysis of host cells leads to the release of cellular carbon and nutrients and is hypothesized to be a major driver of carbon recycling on a global scale. However, efforts to characterize the effects of viruses on nutrient cycles have overlooked the geochemical potential of the virus particles themselves, particularly with respect to their phosphorus content. In this Analysis article, we use a biophysical scaling model of intact virus particles that has been validated using sequence and structural information to quantify differences in the elemental stoichiometry of marine viruses compared with their microbial hosts. By extrapolating particle-scale estimates to the ecosystem scale, we propose that, under certain circumstances, marine virus populations could make an important contribution to the reservoir and cycling of oceanic phosphorus.

At a glance

Figures

  1. Schematic of the viral shunt.
    Figure 1: Schematic of the viral shunt.

    Virus-mediated lysis of microbial cells releases dissolved organic matter (DOM) and particulate organic matter (POM) back into the microbial loop, rather than these cells being targeted by grazers (for example, nanozooplankton and microzooplankton), which can then be consumed by larger organisms in the aquatic food web. Figure adapted, with permission, from Ref. 22, Faculty of 1000 Ltd.

  2. Model of the elemental stoichiometry of virus particles.
    Figure 2: Model of the elemental stoichiometry of virus particles.

    a | The viral head is approximated as a spherical shell of proteins with an internal core of nucleic acids. The number of proteins scales with the radius of the capsid squared (r2) and the number of base pairs scales with the radius of the capsid cubed (r3). b | The relative carbon, nitrogen and phosphorus content within proteins and nucleic acids. c | The carbon, nitrogen and phosphorus content of the viral head as a function of its external radius (solid lines). The data correspond to experimentally obtained carbon, nitrogen and phosphorus contents for different viral heads. The protein compositions of the capsids were obtained from the following references: T4 (Ref. 84), N4 (Ref. 79), Syn5 (Ref. 80), λ and T7 (Ref. 21), HK97 (Ref. 81), Φ29 (Ref. 83). The model predictions are: Chead = 41(rc − 2.5)3 + 130(7.5rc2 − 18.75rc + 15.63), Nhead = 16(rc − 2.5)3 + 36(7.5rc2 − 18.75rc + 15.63) and Phead = 4.2(rc − 2.5)3, where rc is in units of nm. The basis for model error estimates (dashed lines) is detailed in Supplementary information S1 (box). The estimate of the scaling between genome length and virus capsid radius (Supplementary information S1 (box)) is key.

  3. Theoretical prediction of elemental stoichiometry for viruses.
    Figure 3: Theoretical prediction of elemental stoichiometry for viruses.

    We compare the predicted C/N and N/P ratios for viruses (solid black line) with the ratios that are expected for DNA, marine phytoplankton (as per the Redfield ratio) and heterotrophic microorganisms. The theoretical curve (solid black line) denotes the predicted stoichiometry for viruses that have capsid diameters in the range of 20 nm to 300 nm. The stoichiometry of three representative viruses that have capsid diameters of 20 nm, 30 nm and 100 nm is shown.

  4. Virus-induced transformation of elemental content in cellular debris following lysis.
    Figure 4: Virus-induced transformation of elemental content in cellular debris following lysis.

    a | After lysis, the contents of a host are released as virus particles and other cellular debris (that is, the lysate). The relative carbon, nitrogen and phosphorus levels in the virus particles and the lysate are shown in bars; the bar height is normalized in each case by the total amount of the element in the host. Bar heights are based on the hypothetical infection of Prochlorococcus sp. MED4 host under phosphorus-replete conditions by a podovirus with 70 nm diameter head. Note that, in fact, the total carbon, nitrogen and phosphorus content differs between the host and the virus (Fig. 3). b | Predictions of the model of elemental transformation as applied to a viral infection of three marine cyanobacteria. The fraction of the host element in the lysate in each panel is normalized by the elemental content of the respective host. The x axis denotes culture conditions from phosphorus-limited (0) to phosphorus-replete (1) (Ref. 12).

  5. Predicted DOP concentration in viral populations as a function of viral density and virus size.
    Figure 5: Predicted DOP concentration in viral populations as a function of viral density and virus size.

    a | Virus size is quantified in terms of mean capsid diameter, which varies from 30 nm to 100 nm. b | Virus size is quantified in terms of genome length, which ranges from 4.1 kb to 220 kb. In both cases, viral density varies from 108 virus particles per litre to 1011 virus particles per litre on a logarithmically spaced axis. The contour lines denote combinations of viral density and capsid diameter, which correspond to the same predicted concentration of dissolved organic phosphorus (DOP) that is partitioned in viruses. The colour bar indicates the predicted DOP in units of nmol per litre.

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Author information

Affiliations

  1. School of Physics, Georgia Institute of Technology, Atlanta, Georgia 30332, USA.

    • Luis F. Jover &
    • Joshua S. Weitz
  2. Department of Microbiology, University of Tennessee, Knoxville, Tennessee 37996, USA.

    • T. Chad Effler,
    • Alison Buchan &
    • Steven W. Wilhelm
  3. School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332, USA.

    • Joshua S. Weitz

Competing interests statement

The authors declare no competing interests.

Corresponding author

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Author details

  • Luis F. Jover

    Luis F. Jover is a Ph.D. candidate in physics at the Georgia Institute of Technology, Atlanta, USA. His research interests are in theoretical ecology, with a focus on modelling interactions between marine viruses and their microbial hosts.

  • T. Chad Effler

    T. Chad Effler is an undergraduate majoring in electrical engineering and computer science at the University of Tennessee, Knoxville, USA. His research interests include theoretical computing and bioinformatics.

  • Alison Buchan

    Alison Buchan is Associate Professor of Microbiology at the University of Tennessee, Knoxville, USA. In 2001, she received a Ph.D. in marine sciences from the University of Georgia, Atlanta, USA. Her research interests are broadly in the area of marine microbial ecology, with an emphasis on bacterial transformations of lignin-derived compounds and phage–host interactions.

  • Steven W. Wilhelm

    Steven W. Wilhelm is Professor of Microbiology at the University of Tennessee, Knoxville, USA. In 1994, he received his Ph.D. in plant sciences from the University of Western Ontario, Canada. His research interests broadly centre around aquatic biogeochemical cycles and the viruses and microbial community members that constrain them.

  • Joshua S. Weitz

    Joshua S. Weitz is Associate Professor of Biology at the Georgia Institute of Technology, Atlanta, USA. In 2003, he received his Ph.D. in physics from the Massachusetts Institute of Technology, Cambridge, USA. His research focuses on the application of mathematical and physical models to the life sciences, with an emphasis on virus–host interactions.

Supplementary information

PDF files

  1. Supplementary information S1 (box) (1,734 KB)

    Parameters and ranges used in the theory of viral elemental stoichoimetry

Excel files

  1. Supplementary information S2 (table) (13 KB)

    Phage capsid size and genome length calibration data set

  2. Supplementary information S3 (table) (50 KB)

    Phage genome length data set

  3. Supplementary information S4 (table) (661 KB)

    Viral protein data set

Additional data