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

Joshua S. Weitz, Charles A. Stock, Steven W. Wilhelm, Lydia Bourouiba, Maureen L. Coleman, Alison Buchan, Michael J. Follows, Jed A. Fuhrman, Luis F. Jover, Jay T. Lennon, Mathias Middelboe, Derek L Sonderegger, Curtis A. Suttle, Bradford P. Taylor, T. Frede Thingstad, William H. Wilson, K. Eric Wommack

Research output: Contribution to journalArticle

74 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)1352-1364
Number of pages13
JournalISME Journal
Volume9
Issue number6
DOIs
StatePublished - Jun 23 2015

Fingerprint

Food Chain
food webs
Ecosystem
food web
virus
Viruses
viruses
ecosystems
ecosystem
Viral Structures
lysis
Carbon
Oceans and Seas
Satellite Viruses
recycling
biogeochemical cycles
carbon
effect
oceans
Recycling

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Microbiology

Cite this

Weitz, J. S., Stock, C. A., Wilhelm, S. W., Bourouiba, L., Coleman, M. L., Buchan, A., ... Eric Wommack, K. (2015). A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME Journal, 9(6), 1352-1364. https://doi.org/10.1038/ismej.2014.220

A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. / Weitz, Joshua S.; Stock, Charles A.; Wilhelm, Steven W.; Bourouiba, Lydia; Coleman, Maureen L.; Buchan, Alison; Follows, Michael J.; Fuhrman, Jed A.; Jover, Luis F.; Lennon, Jay T.; Middelboe, Mathias; Sonderegger, Derek L; Suttle, Curtis A.; Taylor, Bradford P.; Frede Thingstad, T.; Wilson, William H.; Eric Wommack, K.

In: ISME Journal, Vol. 9, No. 6, 23.06.2015, p. 1352-1364.

Research output: Contribution to journalArticle

Weitz, JS, Stock, CA, Wilhelm, SW, Bourouiba, L, Coleman, ML, Buchan, A, Follows, MJ, Fuhrman, JA, Jover, LF, Lennon, JT, Middelboe, M, Sonderegger, DL, Suttle, CA, Taylor, BP, Frede Thingstad, T, Wilson, WH & Eric Wommack, K 2015, 'A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes', ISME Journal, vol. 9, no. 6, pp. 1352-1364. https://doi.org/10.1038/ismej.2014.220
Weitz, Joshua S. ; Stock, Charles A. ; Wilhelm, Steven W. ; Bourouiba, Lydia ; Coleman, Maureen L. ; Buchan, Alison ; Follows, Michael J. ; Fuhrman, Jed A. ; Jover, Luis F. ; Lennon, Jay T. ; Middelboe, Mathias ; Sonderegger, Derek L ; Suttle, Curtis A. ; Taylor, Bradford P. ; Frede Thingstad, T. ; Wilson, William H. ; Eric Wommack, K. / A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. In: ISME Journal. 2015 ; Vol. 9, No. 6. pp. 1352-1364.
@article{067fe4c3d363465e98bd2cef1ec50bdc,
title = "A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes",
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.",
author = "Weitz, {Joshua S.} and Stock, {Charles A.} and Wilhelm, {Steven W.} and Lydia Bourouiba and Coleman, {Maureen L.} and Alison Buchan and Follows, {Michael J.} and Fuhrman, {Jed A.} and Jover, {Luis F.} and Lennon, {Jay T.} and Mathias Middelboe and Sonderegger, {Derek L} and Suttle, {Curtis A.} and Taylor, {Bradford P.} and {Frede Thingstad}, T. and Wilson, {William H.} and {Eric Wommack}, K.",
year = "2015",
month = "6",
day = "23",
doi = "10.1038/ismej.2014.220",
language = "English (US)",
volume = "9",
pages = "1352--1364",
journal = "ISME Journal",
issn = "1751-7362",
publisher = "Nature Publishing Group",
number = "6",

}

TY - JOUR

T1 - A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes

AU - Weitz, Joshua S.

AU - Stock, Charles A.

AU - Wilhelm, Steven W.

AU - Bourouiba, Lydia

AU - Coleman, Maureen L.

AU - Buchan, Alison

AU - Follows, Michael J.

AU - Fuhrman, Jed A.

AU - Jover, Luis F.

AU - Lennon, Jay T.

AU - Middelboe, Mathias

AU - Sonderegger, Derek L

AU - Suttle, Curtis A.

AU - Taylor, Bradford P.

AU - Frede Thingstad, T.

AU - Wilson, William H.

AU - Eric Wommack, K.

PY - 2015/6/23

Y1 - 2015/6/23

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84929653204&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84929653204&partnerID=8YFLogxK

U2 - 10.1038/ismej.2014.220

DO - 10.1038/ismej.2014.220

M3 - Article

VL - 9

SP - 1352

EP - 1364

JO - ISME Journal

JF - ISME Journal

SN - 1751-7362

IS - 6

ER -