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

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, ho...

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Vydáno v:The ISME Journal Ročník 9; číslo 6; s. 1352 - 1364
Hlavní autoři: 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
Médium: Journal Article
Jazyk:angličtina
Vydáno: London Nature Publishing Group UK 01.06.2015
Oxford University Press
Nature Publishing Group
Témata:
631/158/2451
631/158/855
631/326/171/1878
704/172
Animals
Bacteria - virology
Biogeochemical cycles
Biomass
Biomedical and Life Sciences
Carbon
Community structure
Cyanobacteria - metabolism
Ecological function
Ecology
Ecosystem
Ecosystem models
Euphotic zone
Evolutionary Biology
Food Chain
Food webs
Life Sciences
Marine ecosystems
Microbial Ecology
Microbial Genetics and Genomics
Microbial Interactions
Microbiology
Microorganisms
Nutrient cycles
Oceans
Oceans and Seas
Organic matter
Original
original-article
Recycling
Trophic levels
Viruses
Water Microbiology
Zooplankton - metabolism
ISSN:1751-7362, 1751-7370, 1751-7370
On-line přístup:Získat plný text
Tagy: Přidat tag
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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.
AbstractList 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.
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.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 Lennon, Jay T
Suttle, Curtis A
Follows, Michael J
Middelboe, Mathias
Stock, Charles A
Frede Thingstad, T
Wilhelm, Steven W
Fuhrman, Jed A
Sonderegger, Derek L
Bourouiba, Lydia
Jover, Luis F
Taylor, Bradford P
Coleman, Maureen L
Buchan, Alison
Weitz, Joshua S
Wilson, William H
Eric Wommack, K
Author_xml – sequence: 1
  givenname: Joshua S
  surname: Weitz
  fullname: Weitz, Joshua S
  email: jsweitz@gatech.edu
  organization: School of Biology, Georgia Institute of Technology, School of Physics, Georgia Institute of Technology
– sequence: 2
  givenname: Charles A
  surname: Stock
  fullname: Stock, Charles A
  organization: Geophysical Fluid Dynamics Laboratory, NOAA
– sequence: 3
  givenname: Steven W
  surname: Wilhelm
  fullname: Wilhelm, Steven W
  organization: Department of Microbiology, University of Tennessee
– sequence: 4
  givenname: Lydia
  surname: Bourouiba
  fullname: Bourouiba, Lydia
  organization: Department of Applied Mathematics, Massachusetts Institute of Technology
– sequence: 5
  givenname: Maureen L
  surname: Coleman
  fullname: Coleman, Maureen L
  organization: Department of Geosciences, University of Chicago
– sequence: 6
  givenname: Alison
  surname: Buchan
  fullname: Buchan, Alison
  organization: Department of Microbiology, University of Tennessee
– sequence: 7
  givenname: Michael J
  surname: Follows
  fullname: Follows, Michael J
  organization: Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology
– sequence: 8
  givenname: Jed A
  surname: Fuhrman
  fullname: Fuhrman, Jed A
  organization: Department of Biological Sciences, University of Southern California
– sequence: 9
  givenname: Luis F
  surname: Jover
  fullname: Jover, Luis F
  organization: School of Physics, Georgia Institute of Technology
– sequence: 10
  givenname: Jay T
  surname: Lennon
  fullname: Lennon, Jay T
  organization: Department of Biology, Indiana University
– sequence: 11
  givenname: Mathias
  surname: Middelboe
  fullname: Middelboe, Mathias
  organization: Marine Biological Section, University of Copenhagen
– sequence: 12
  givenname: Derek L
  surname: Sonderegger
  fullname: Sonderegger, Derek L
  organization: Department of Mathematics, Northern Arizona University
– sequence: 13
  givenname: Curtis A
  surname: Suttle
  fullname: Suttle, Curtis A
  organization: Department of Earth and Ocean Sciences, Department of Botany, and Department of Microbiology and Immunology, University of British Columbia
– sequence: 14
  givenname: Bradford P
  surname: Taylor
  fullname: Taylor, Bradford P
  organization: School of Physics, Georgia Institute of Technology
– sequence: 15
  givenname: T
  surname: Frede Thingstad
  fullname: Frede Thingstad, T
  organization: Department of Biology, University of Bergen
– sequence: 16
  givenname: William H
  surname: Wilson
  fullname: Wilson, William H
  organization: Bigelow Laboratory for Ocean Sciences, 16Current address: Plymouth Marine Laboratory, Plymouth, UK
– sequence: 17
  givenname: K
  surname: Eric Wommack
  fullname: Eric Wommack, K
  organization: Delaware Biotechnology Institute, University of Delaware
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25635642$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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Copyright © 2015 International Society for Microbial Ecology 2015 International Society for Microbial Ecology
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Snippet Viral lysis of microbial hosts releases organic matter that can then be assimilated by nontargeted microorganisms. Quantitative estimates of virus-mediated...
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SubjectTerms 631/158/2451
631/158/855
631/326/171/1878
704/172
Animals
Bacteria - virology
Biogeochemical cycles
Biomass
Biomedical and Life Sciences
Carbon
Community structure
Cyanobacteria - metabolism
Ecological function
Ecology
Ecosystem
Ecosystem models
Euphotic zone
Evolutionary Biology
Food Chain
Food webs
Life Sciences
Marine ecosystems
Microbial Ecology
Microbial Genetics and Genomics
Microbial Interactions
Microbiology
Microorganisms
Nutrient cycles
Oceans
Oceans and Seas
Organic matter
Original
original-article
Recycling
Trophic levels
Viruses
Water Microbiology
Zooplankton - metabolism
Title A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes
URI https://link.springer.com/article/10.1038/ismej.2014.220
https://www.ncbi.nlm.nih.gov/pubmed/25635642
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https://pubmed.ncbi.nlm.nih.gov/PMC4438322
Volume 9
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