Original Article

The ISME Journal (2015) 9, 1352–1364; doi:10.1038/ismej.2014.220; published online 30 January 2015

A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes

Joshua S Weitz1,2, Charles A Stock3, Steven W Wilhelm4, Lydia Bourouiba5, Maureen L Coleman6, Alison Buchan4, Michael J Follows7, Jed A Fuhrman8, Luis F Jover2, Jay T Lennon9, Mathias Middelboe10, Derek L Sonderegger11, Curtis A Suttle12, Bradford P Taylor2, T Frede Thingstad13, William H Wilson14,16 and K Eric Wommack15

  1. 1School of Biology, Georgia Institute of Technology, Atlanta, GA, USA
  2. 2School of Physics, Georgia Institute of Technology, Atlanta, GA, USA
  3. 3Geophysical Fluid Dynamics Laboratory, NOAA, Princeton, NJ, USA
  4. 4Department of Microbiology, University of Tennessee, Knoxville, TN, USA
  5. 5Department of Applied Mathematics, Massachusetts Institute of Technology, Cambridge, MA, USA
  6. 6Department of Geosciences, University of Chicago, Chicago, IL, USA
  7. 7Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA
  8. 8Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA
  9. 9Department of Biology, Indiana University, Bloomington, IN, USA
  10. 10Marine Biological Section, University of Copenhagen, Copenhagen, Denmark
  11. 11Department of Mathematics, Northern Arizona University, Flagstaff, AZ, USA
  12. 12Department of Earth and Ocean Sciences, Department of Botany, and Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia, Canada
  13. 13Department of Biology, University of Bergen, Bergen, Norway
  14. 14Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA
  15. 15Delaware Biotechnology Institute, University of Delaware, Newark, DE, USA

Correspondence: JS Weitz, School of Biology, Georgia Institute of Technology, 310 Ferst Drive, Atlanta, GA 30332-0230, USA. E-mail: jsweitz@gatech.edu

16Current address: Plymouth Marine Laboratory, Plymouth, UK.

Received 22 June 2014; Revised 15 October 2014; Accepted 17 October 2014
Advance online publication 30 January 2015

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Abstract

Viral lysis of microbial hosts releases organic matter that can then be assimilated by nontargeted microorganisms. Quantitative estimates of virus-mediated recycling of carbon in marine waters, first established in the late 1990s, were originally extrapolated from marine host and virus densities, host carbon content and inferred viral lysis rates. Yet, these estimates did not explicitly incorporate the cascade of complex feedbacks associated with virus-mediated lysis. To evaluate the role of viruses in shaping community structure and ecosystem functioning, we extend dynamic multitrophic ecosystem models to include a virus component, specifically parameterized for processes taking place in the ocean euphotic zone. Crucially, we are able to solve this model analytically, facilitating evaluation of model behavior under many alternative parameterizations. Analyses reveal that the addition of a virus component promotes the emergence of complex communities. In addition, biomass partitioning of the emergent multitrophic community is consistent with well-established empirical norms in the surface oceans. At steady state, ecosystem fluxes can be probed to characterize the effects that viruses have when compared with putative marine surface ecosystems without viruses. The model suggests that ecosystems with viruses will have (1) increased organic matter recycling, (2) reduced transfer to higher trophic levels and (3) increased net primary productivity. These model findings support hypotheses that viruses can have significant stimulatory effects across whole-ecosystem scales. We suggest that existing efforts to predict carbon and nutrient cycling without considering virus effects are likely to miss essential features of marine food webs that regulate global biogeochemical cycles.