Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?

Microorganisms are vital in mediating the earth’s biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between microbial community structure and ecosystem processes remains poorly understood. Here, we address a fu...

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Main Authors: Emily B. Graham, Joseph E. Knelman, Andreas eSchindlbacher, Steven eSiciliano, Marc eBreulmann, Anthony eYannarell, J. Michael eBeman, Guy eAbell, Laurent ePhilippot, James eProsser, Arnaud eFoulquier, Jorge Curiel eYuste, Helen C. eGlanville, Davey eJones, Roey eAngel, Janne eSalminen, Ryan J Newton, Helmut eBürgmann, Lachlan J. Ingram, Ute eHamer, Henri MP Siljanen, Krista ePeltoniemi, Karin ePotthast, Lluís eBañeras, Martin eHartmann, Samiran eBanerjee, Ri-Qing eYu, Geraldine eNogaro, Andreas eRichter, Marianne eKoranda, Sarah eCastle, Marta eGoberna, Bongkeun eSong, Amitava eChatterjee, Olga Cristina Nunes, Ana Rita Lopes, Yiping eCao, Aurore eKaisermann, Sara eHallin, Michael S Strickland, Jordi eGarcia-Pausas, Josep eBarba, Hojeong eKang, Kazuo eIsobe, Sokratis ePapaspyrou, Roberta ePastorelli, Alessandra eLagomarsino, Eva eLindström, Nathan eBasiliko, Diana Reid Nemergut
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00214/full
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author Emily B. Graham
Emily B. Graham
Joseph E. Knelman
Joseph E. Knelman
Andreas eSchindlbacher
Steven eSiciliano
Marc eBreulmann
Anthony eYannarell
J. Michael eBeman
Guy eAbell
Laurent ePhilippot
James eProsser
Arnaud eFoulquier
Jorge Curiel eYuste
Helen C. eGlanville
Davey eJones
Roey eAngel
Janne eSalminen
Ryan J Newton
Helmut eBürgmann
Lachlan J. Ingram
Ute eHamer
Henri MP Siljanen
Krista ePeltoniemi
Karin ePotthast
Lluís eBañeras
Martin eHartmann
Samiran eBanerjee
Ri-Qing eYu
Geraldine eNogaro
Andreas eRichter
Marianne eKoranda
Sarah eCastle
Marta eGoberna
Bongkeun eSong
Amitava eChatterjee
Olga Cristina Nunes
Ana Rita Lopes
Yiping eCao
Aurore eKaisermann
Sara eHallin
Michael S Strickland
Jordi eGarcia-Pausas
Josep eBarba
Hojeong eKang
Kazuo eIsobe
Sokratis ePapaspyrou
Roberta ePastorelli
Alessandra eLagomarsino
Eva eLindström
Nathan eBasiliko
Diana Reid Nemergut
Diana Reid Nemergut
author_facet Emily B. Graham
Emily B. Graham
Joseph E. Knelman
Joseph E. Knelman
Andreas eSchindlbacher
Steven eSiciliano
Marc eBreulmann
Anthony eYannarell
J. Michael eBeman
Guy eAbell
Laurent ePhilippot
James eProsser
Arnaud eFoulquier
Jorge Curiel eYuste
Helen C. eGlanville
Davey eJones
Roey eAngel
Janne eSalminen
Ryan J Newton
Helmut eBürgmann
Lachlan J. Ingram
Ute eHamer
Henri MP Siljanen
Krista ePeltoniemi
Karin ePotthast
Lluís eBañeras
Martin eHartmann
Samiran eBanerjee
Ri-Qing eYu
Geraldine eNogaro
Andreas eRichter
Marianne eKoranda
Sarah eCastle
Marta eGoberna
Bongkeun eSong
Amitava eChatterjee
Olga Cristina Nunes
Ana Rita Lopes
Yiping eCao
Aurore eKaisermann
Sara eHallin
Michael S Strickland
Jordi eGarcia-Pausas
Josep eBarba
Hojeong eKang
Kazuo eIsobe
Sokratis ePapaspyrou
Roberta ePastorelli
Alessandra eLagomarsino
Eva eLindström
Nathan eBasiliko
Diana Reid Nemergut
Diana Reid Nemergut
author_sort Emily B. Graham
collection DOAJ
description Microorganisms are vital in mediating the earth’s biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between microbial community structure and ecosystem processes remains poorly understood. Here, we address a fundamental and unanswered question in microbial ecology: ‘When do we need to understand microbial community structure to accurately predict function?’ We present a statistical analysis investigating the value of environmental data and microbial community structure independently and in combination for explaining rates of carbon and nitrogen cycling processes within 82 global datasets. Environmental variables were the strongest predictors of process rates but left 44% of variation unexplained on average, suggesting the potential for microbial data to increase model accuracy. Although only 29% of our datasets were significantly improved by adding information on microbial community structure, we observed improvement in models of processes mediated by narrow phylogenetic guilds via functional gene data, and conversely, improvement in models of facultative microbial processes via community diversity metrics. Our results also suggest that microbial diversity can strengthen predictions of respiration rates beyond microbial biomass parameters, as 53% of models were improved by incorporating both sets of predictors compared to 35% by microbial biomass alone. Our analysis represents the first comprehensive analysis of research examining links between microbial community structure and ecosystem function. Taken together, our results indicate that a greater understanding of microbial communities informed by ecological principles may enhance our ability to predict ecosystem process rates relative to assessments based on environmental variables and microbial physiology.
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spelling doaj.art-8ccc1905281545e19b1994be059ab4d12022-12-22T01:28:55ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2016-02-01710.3389/fmicb.2016.00214181167Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?Emily B. Graham0Emily B. Graham1Joseph E. Knelman2Joseph E. Knelman3Andreas eSchindlbacher4Steven eSiciliano5Marc eBreulmann6Anthony eYannarell7J. Michael eBeman8Guy eAbell9Laurent ePhilippot10James eProsser11Arnaud eFoulquier12Jorge Curiel eYuste13Helen C. eGlanville14Davey eJones15Roey eAngel16Janne eSalminen17Ryan J Newton18Helmut eBürgmann19Lachlan J. Ingram20Ute eHamer21Henri MP Siljanen22Krista ePeltoniemi23Karin ePotthast24Lluís eBañeras25Martin eHartmann26Samiran eBanerjee27Ri-Qing eYu28Geraldine eNogaro29Andreas eRichter30Marianne eKoranda31Sarah eCastle32Marta eGoberna33Bongkeun eSong34Amitava eChatterjee35Olga Cristina Nunes36Ana Rita Lopes37Yiping eCao38Aurore eKaisermann39Sara eHallin40Michael S Strickland41Jordi eGarcia-Pausas42Josep eBarba43Hojeong eKang44Kazuo eIsobe45Sokratis ePapaspyrou46Roberta ePastorelli47Alessandra eLagomarsino48Eva eLindström49Nathan eBasiliko50Diana Reid Nemergut51Diana Reid Nemergut52University of ColoradoPacific Northwest National LaboratoryUniversity of ColoradoUS Department of EnergyBFWUniv. of SaskatchewanUBZUniv. of Illinois at Urbana-ChampaignUniv. of California - MercedFlinders Univ.INRAUniv. of AberdeenUR MALYCSICBangor Univ.Bangor Univ.Univ. of ViennaHäme Univ. of Applied Sci.Univ. of Wisconsin-MilwaukeeEawag: Swiss Federal Inst. of Aquatic Sci. & TechnologyThe Univ. of SydneyUniv. of MünsterUniv. of Eastern FinlandNat. Resources Inst. Finland (Luke)Technische Univ.Univ. of GironaAgroscopeCSIRO Agriculture FlagshipUniv. of Texas at TylerLNHEUniv. of ViennaUniv. of ViennaUniv. of MontanaCIDE-CSICVirginia Institute of Marine ScienceNorth Dakota State Univ.Univ. of PortoUniv. of PortoSouthern California Coastal Water Res. Project AuthorityINRA BordeauxSwedish Univ. of Agricultural Sci.Virginia Polytechnic Inst. & State Univ.Centre Tecnològic Forestal de CatalunyaCREAFYonsei Univ.The Univ. of TokyoUniv. of CadizRes. Centre for Agrobiology & PedologyRes. Centre for Agrobiology & PedologyUppsala Univ.Laurentian Univ.University of ColoradoDuke UniversityMicroorganisms are vital in mediating the earth’s biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between microbial community structure and ecosystem processes remains poorly understood. Here, we address a fundamental and unanswered question in microbial ecology: ‘When do we need to understand microbial community structure to accurately predict function?’ We present a statistical analysis investigating the value of environmental data and microbial community structure independently and in combination for explaining rates of carbon and nitrogen cycling processes within 82 global datasets. Environmental variables were the strongest predictors of process rates but left 44% of variation unexplained on average, suggesting the potential for microbial data to increase model accuracy. Although only 29% of our datasets were significantly improved by adding information on microbial community structure, we observed improvement in models of processes mediated by narrow phylogenetic guilds via functional gene data, and conversely, improvement in models of facultative microbial processes via community diversity metrics. Our results also suggest that microbial diversity can strengthen predictions of respiration rates beyond microbial biomass parameters, as 53% of models were improved by incorporating both sets of predictors compared to 35% by microbial biomass alone. Our analysis represents the first comprehensive analysis of research examining links between microbial community structure and ecosystem function. Taken together, our results indicate that a greater understanding of microbial communities informed by ecological principles may enhance our ability to predict ecosystem process rates relative to assessments based on environmental variables and microbial physiology.http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00214/fullCarbon CycleDenitrificationNitrificationNitrogen CycleRespirationmicrobial ecology
spellingShingle Emily B. Graham
Emily B. Graham
Joseph E. Knelman
Joseph E. Knelman
Andreas eSchindlbacher
Steven eSiciliano
Marc eBreulmann
Anthony eYannarell
J. Michael eBeman
Guy eAbell
Laurent ePhilippot
James eProsser
Arnaud eFoulquier
Jorge Curiel eYuste
Helen C. eGlanville
Davey eJones
Roey eAngel
Janne eSalminen
Ryan J Newton
Helmut eBürgmann
Lachlan J. Ingram
Ute eHamer
Henri MP Siljanen
Krista ePeltoniemi
Karin ePotthast
Lluís eBañeras
Martin eHartmann
Samiran eBanerjee
Ri-Qing eYu
Geraldine eNogaro
Andreas eRichter
Marianne eKoranda
Sarah eCastle
Marta eGoberna
Bongkeun eSong
Amitava eChatterjee
Olga Cristina Nunes
Ana Rita Lopes
Yiping eCao
Aurore eKaisermann
Sara eHallin
Michael S Strickland
Jordi eGarcia-Pausas
Josep eBarba
Hojeong eKang
Kazuo eIsobe
Sokratis ePapaspyrou
Roberta ePastorelli
Alessandra eLagomarsino
Eva eLindström
Nathan eBasiliko
Diana Reid Nemergut
Diana Reid Nemergut
Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?
Frontiers in Microbiology
Carbon Cycle
Denitrification
Nitrification
Nitrogen Cycle
Respiration
microbial ecology
title Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?
title_full Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?
title_fullStr Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?
title_full_unstemmed Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?
title_short Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?
title_sort microbes as engines of ecosystem function when does community structure enhance predictions of ecosystem processes
topic Carbon Cycle
Denitrification
Nitrification
Nitrogen Cycle
Respiration
microbial ecology
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00214/full
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