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Linking Nitrogen Load to the Structure and Function of Wetland Soil and Rhizosphere Microbial Communities

Wetland ecosystems are important reservoirs of biodiversity and significantly contribute to emissions of the greenhouse gases CO(2), N(2)O, and CH(4). High anthropogenic nitrogen (N) inputs from agriculture and fossil fuel combustion have been recognized as a severe threat to biodiversity and ecosys...

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Autores principales: Hester, Eric R., Harpenslager, Sarah F., van Diggelen, Josepha M. H., Lamers, Leon L., Jetten, Mike S. M., Lüke, Claudia, Lücker, Sebastian, Welte, Cornelia U.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5790874/
https://www.ncbi.nlm.nih.gov/pubmed/29404427
http://dx.doi.org/10.1128/mSystems.00214-17
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author Hester, Eric R.
Harpenslager, Sarah F.
van Diggelen, Josepha M. H.
Lamers, Leon L.
Jetten, Mike S. M.
Lüke, Claudia
Lücker, Sebastian
Welte, Cornelia U.
author_facet Hester, Eric R.
Harpenslager, Sarah F.
van Diggelen, Josepha M. H.
Lamers, Leon L.
Jetten, Mike S. M.
Lüke, Claudia
Lücker, Sebastian
Welte, Cornelia U.
author_sort Hester, Eric R.
collection PubMed
description Wetland ecosystems are important reservoirs of biodiversity and significantly contribute to emissions of the greenhouse gases CO(2), N(2)O, and CH(4). High anthropogenic nitrogen (N) inputs from agriculture and fossil fuel combustion have been recognized as a severe threat to biodiversity and ecosystem functioning, such as control of greenhouse gas emissions. Therefore, it is important to understand how increased N input into pristine wetlands affects the composition and activity of microorganisms, especially in interaction with dominant wetland plants. In a series of incubations analyzed over 90 days, we disentangled the effects of N fertilization on the microbial community in bulk soil and the rhizosphere of Juncus acutiflorus, a common and abundant graminoid wetland plant. We observed an increase in greenhouse gas emissions when N is increased in incubations with J. acutiflorus, changing the system from a greenhouse gas sink to a source. Using 16S rRNA gene amplicon sequencing, we determined that the bacterial orders Opitutales, subgroup 6 Acidobacteria, and Sphingobacteriales significantly responded to high N availability. Based on metagenomic data, we hypothesize that these groups are contributing to the increased greenhouse gas emissions. These results indicated that increased N input leads to shifts in microbial activity within the rhizosphere, altering N cycling dynamics. Our study provides a framework for connecting environmental conditions of wetland bulk and rhizosphere soil to the structure and metabolic output of microbial communities. IMPORTANCE Microorganisms living within the rhizospheres of wetland plants significantly contribute to greenhouse gas emissions. Understanding how microbes produce these gases under conditions that have been imposed by human activities (i.e., nitrogen pollution) is important to the development of future management strategies. Our results illustrate that within the rhizosphere of the wetland plant Juncus acutiflorus, physiological differences associated with nitrogen availability can influence microbial activity linked to greenhouse gas production. By pairing taxonomic information and environmental conditions like nitrogen availability with functional outputs of a system such as greenhouse gas fluxes, we present a framework to link certain taxa to both nitrogen load and greenhouse gas production. We view this type of combined information as essential in moving forward in our understanding of complex systems such as rhizosphere microbial communities.
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spelling pubmed-57908742018-02-05 Linking Nitrogen Load to the Structure and Function of Wetland Soil and Rhizosphere Microbial Communities Hester, Eric R. Harpenslager, Sarah F. van Diggelen, Josepha M. H. Lamers, Leon L. Jetten, Mike S. M. Lüke, Claudia Lücker, Sebastian Welte, Cornelia U. mSystems Research Article Wetland ecosystems are important reservoirs of biodiversity and significantly contribute to emissions of the greenhouse gases CO(2), N(2)O, and CH(4). High anthropogenic nitrogen (N) inputs from agriculture and fossil fuel combustion have been recognized as a severe threat to biodiversity and ecosystem functioning, such as control of greenhouse gas emissions. Therefore, it is important to understand how increased N input into pristine wetlands affects the composition and activity of microorganisms, especially in interaction with dominant wetland plants. In a series of incubations analyzed over 90 days, we disentangled the effects of N fertilization on the microbial community in bulk soil and the rhizosphere of Juncus acutiflorus, a common and abundant graminoid wetland plant. We observed an increase in greenhouse gas emissions when N is increased in incubations with J. acutiflorus, changing the system from a greenhouse gas sink to a source. Using 16S rRNA gene amplicon sequencing, we determined that the bacterial orders Opitutales, subgroup 6 Acidobacteria, and Sphingobacteriales significantly responded to high N availability. Based on metagenomic data, we hypothesize that these groups are contributing to the increased greenhouse gas emissions. These results indicated that increased N input leads to shifts in microbial activity within the rhizosphere, altering N cycling dynamics. Our study provides a framework for connecting environmental conditions of wetland bulk and rhizosphere soil to the structure and metabolic output of microbial communities. IMPORTANCE Microorganisms living within the rhizospheres of wetland plants significantly contribute to greenhouse gas emissions. Understanding how microbes produce these gases under conditions that have been imposed by human activities (i.e., nitrogen pollution) is important to the development of future management strategies. Our results illustrate that within the rhizosphere of the wetland plant Juncus acutiflorus, physiological differences associated with nitrogen availability can influence microbial activity linked to greenhouse gas production. By pairing taxonomic information and environmental conditions like nitrogen availability with functional outputs of a system such as greenhouse gas fluxes, we present a framework to link certain taxa to both nitrogen load and greenhouse gas production. We view this type of combined information as essential in moving forward in our understanding of complex systems such as rhizosphere microbial communities. American Society for Microbiology 2018-01-30 /pmc/articles/PMC5790874/ /pubmed/29404427 http://dx.doi.org/10.1128/mSystems.00214-17 Text en Copyright © 2018 Hester et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Hester, Eric R.
Harpenslager, Sarah F.
van Diggelen, Josepha M. H.
Lamers, Leon L.
Jetten, Mike S. M.
Lüke, Claudia
Lücker, Sebastian
Welte, Cornelia U.
Linking Nitrogen Load to the Structure and Function of Wetland Soil and Rhizosphere Microbial Communities
title Linking Nitrogen Load to the Structure and Function of Wetland Soil and Rhizosphere Microbial Communities
title_full Linking Nitrogen Load to the Structure and Function of Wetland Soil and Rhizosphere Microbial Communities
title_fullStr Linking Nitrogen Load to the Structure and Function of Wetland Soil and Rhizosphere Microbial Communities
title_full_unstemmed Linking Nitrogen Load to the Structure and Function of Wetland Soil and Rhizosphere Microbial Communities
title_short Linking Nitrogen Load to the Structure and Function of Wetland Soil and Rhizosphere Microbial Communities
title_sort linking nitrogen load to the structure and function of wetland soil and rhizosphere microbial communities
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5790874/
https://www.ncbi.nlm.nih.gov/pubmed/29404427
http://dx.doi.org/10.1128/mSystems.00214-17
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