Literature DB >> 25635642

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

Joshua S Weitz1, Charles A Stock2, Steven W Wilhelm3, Lydia Bourouiba4, Maureen L Coleman5, Alison Buchan3, Michael J Follows6, Jed A Fuhrman7, Luis F Jover8, Jay T Lennon9, Mathias Middelboe10, Derek L Sonderegger11, Curtis A Suttle12, Bradford P Taylor8, T Frede Thingstad13, William H Wilson14, K Eric Wommack15.   

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.

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Year:  2015        PMID: 25635642      PMCID: PMC4438322          DOI: 10.1038/ismej.2014.220

Source DB:  PubMed          Journal:  ISME J        ISSN: 1751-7362            Impact factor:   10.302


  37 in total

Review 1.  Marine viruses--major players in the global ecosystem.

Authors:  Curtis A Suttle
Journal:  Nat Rev Microbiol       Date:  2007-10       Impact factor: 60.633

2.  Dangerous nutrients: evolution of phytoplankton resource uptake subject to virus attack.

Authors:  Duncan N L Menge; Joshua S Weitz
Journal:  J Theor Biol       Date:  2008-11-14       Impact factor: 2.691

3.  The significance of viruses to mortality in aquatic microbial communities.

Authors:  C A Suttle
Journal:  Microb Ecol       Date:  1994-09       Impact factor: 4.552

4.  Persistence of bacteria and phages in a chemostat.

Authors:  Hal L Smith; Horst R Thieme
Journal:  J Math Biol       Date:  2011-06-09       Impact factor: 2.259

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

Authors:  Luis F Jover; T Chad Effler; Alison Buchan; Steven W Wilhelm; Joshua S Weitz
Journal:  Nat Rev Microbiol       Date:  2014-07       Impact factor: 60.633

6.  Coevolutionary arms races between bacteria and bacteriophage.

Authors:  J S Weitz; H Hartman; S A Levin
Journal:  Proc Natl Acad Sci U S A       Date:  2005-06-23       Impact factor: 11.205

7.  Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution.

Authors:  Debbie Lindell; Jacob D Jaffe; Maureen L Coleman; Matthias E Futschik; Ilka M Axmann; Trent Rector; Gregory Kettler; Matthew B Sullivan; Robert Steen; Wolfgang R Hess; George M Church; Sallie W Chisholm
Journal:  Nature       Date:  2007-09-06       Impact factor: 49.962

8.  Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages.

Authors:  Marianne De Paepe; François Taddei
Journal:  PLoS Biol       Date:  2006-07       Impact factor: 8.029

9.  Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging.

Authors:  Li Deng; Ann Gregory; Suzan Yilmaz; Bonnie T Poulos; Philip Hugenholtz; Matthew B Sullivan
Journal:  MBio       Date:  2012-10-30       Impact factor: 7.867

10.  Universally sloppy parameter sensitivities in systems biology models.

Authors:  Ryan N Gutenkunst; Joshua J Waterfall; Fergal P Casey; Kevin S Brown; Christopher R Myers; James P Sethna
Journal:  PLoS Comput Biol       Date:  2007-08-15       Impact factor: 4.475

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  62 in total

1.  High coverage metabolomics analysis reveals phage-specific alterations to Pseudomonas aeruginosa physiology during infection.

Authors:  Jeroen De Smet; Michael Zimmermann; Maria Kogadeeva; Pieter-Jan Ceyssens; Wesley Vermaelen; Bob Blasdel; Ho Bin Jang; Uwe Sauer; Rob Lavigne
Journal:  ISME J       Date:  2016-02-16       Impact factor: 10.302

Review 2.  Virus-host interactions and their roles in coral reef health and disease.

Authors:  Rebecca Vega Thurber; Jérôme P Payet; Andrew R Thurber; Adrienne M S Correa
Journal:  Nat Rev Microbiol       Date:  2017-01-16       Impact factor: 60.633

3.  Energetic differences between bacterioplankton trophic groups and coral reef resistance.

Authors:  Tracey McDole Somera; Barbara Bailey; Katie Barott; Juris Grasis; Mark Hatay; Brett J Hilton; Nao Hisakawa; Bahador Nosrat; James Nulton; Cynthia B Silveira; Chris Sullivan; Russell E Brainard; Forest Rohwer
Journal:  Proc Biol Sci       Date:  2016-04-27       Impact factor: 5.349

4.  Lytic to temperate switching of viral communities.

Authors:  B Knowles; C B Silveira; B A Bailey; K Barott; V A Cantu; A G Cobián-Güemes; F H Coutinho; E A Dinsdale; B Felts; K A Furby; E E George; K T Green; G B Gregoracci; A F Haas; J M Haggerty; E R Hester; N Hisakawa; L W Kelly; Y W Lim; M Little; A Luque; T McDole-Somera; K McNair; L S de Oliveira; S D Quistad; N L Robinett; E Sala; P Salamon; S E Sanchez; S Sandin; G G Z Silva; J Smith; C Sullivan; C Thompson; M J A Vermeij; M Youle; C Young; B Zgliczynski; R Brainard; R A Edwards; J Nulton; F Thompson; F Rohwer
Journal:  Nature       Date:  2016-03-16       Impact factor: 49.962

5.  Deciphering ocean carbon in a changing world.

Authors:  Mary Ann Moran; Elizabeth B Kujawinski; Aron Stubbins; Rob Fatland; Lihini I Aluwihare; Alison Buchan; Byron C Crump; Pieter C Dorrestein; Sonya T Dyhrman; Nancy J Hess; Bill Howe; Krista Longnecker; Patricia M Medeiros; Jutta Niggemann; Ingrid Obernosterer; Daniel J Repeta; Jacob R Waldbauer
Journal:  Proc Natl Acad Sci U S A       Date:  2016-03-07       Impact factor: 11.205

6.  Re-examination of the relationship between marine virus and microbial cell abundances.

Authors:  Charles H Wigington; Derek Sonderegger; Corina P D Brussaard; Alison Buchan; Jan F Finke; Jed A Fuhrman; Jay T Lennon; Mathias Middelboe; Curtis A Suttle; Charles Stock; William H Wilson; K Eric Wommack; Steven W Wilhelm; Joshua S Weitz
Journal:  Nat Microbiol       Date:  2016-01-25       Impact factor: 17.745

7.  Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses.

Authors:  Simon Roux; Jennifer R Brum; Bas E Dutilh; Shinichi Sunagawa; Melissa B Duhaime; Alexander Loy; Bonnie T Poulos; Natalie Solonenko; Elena Lara; Julie Poulain; Stéphane Pesant; Stefanie Kandels-Lewis; Céline Dimier; Marc Picheral; Sarah Searson; Corinne Cruaud; Adriana Alberti; Carlos M Duarte; Josep M Gasol; Dolors Vaqué; Peer Bork; Silvia G Acinas; Patrick Wincker; Matthew B Sullivan
Journal:  Nature       Date:  2016-09-21       Impact factor: 49.962

8.  Knowles &Rohwer reply.

Authors:  Ben Knowles; Forest Rohwer
Journal:  Nature       Date:  2017-09-20       Impact factor: 49.962

9.  Size-dependent Catalysis of Chlorovirus Population Growth by A Messy Feeding Predator.

Authors:  John P DeLong; Zeina Al-Ameeli; Shelby Lyon; James L Van Etten; David D Dunigan
Journal:  Microb Ecol       Date:  2017-11-08       Impact factor: 4.552

10.  Halobacteriovorax, an underestimated predator on bacteria: potential impact relative to viruses on bacterial mortality.

Authors:  Henry N Williams; Despoina S Lymperopoulou; Rana Athar; Ashvini Chauhan; Tamar L Dickerson; Huan Chen; Edward Laws; Timkhite-Kulu Berhane; Adrienne R Flowers; Nadine Bradley; Shanterial Young; Denene Blackwood; Jacqueline Murray; Oladipupo Mustapha; Cory Blackwell; Yahsuan Tung; Rachel T Noble
Journal:  ISME J       Date:  2015-08-07       Impact factor: 10.302

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