Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots

Argiroff, William A.; Zak, Donald R.; Upchurch, Rima A.; Salley, Sydney O.; Grandy, A. Stuart

doi:10.1111/gcb.14770

Title: Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots

Abstract

Abstract Fine root litter is a primary source of soil organic matter (SOM), which is a globally important pool of C that is responsive to climate change. We previously established that ~20 years of experimental nitrogen (N) deposition has slowed fine root decay and increased the storage of soil carbon (C; +18%) across a widespread northern hardwood forest ecosystem. However, the microbial mechanisms that have directly slowed fine root decay are unknown. Here, we show that experimental N deposition has decreased the relative abundance of Agaricales fungi (−31%) and increased that of partially ligninolytic Actinobacteria (+24%) on decaying fine roots. Moreover, experimental N deposition has increased the relative abundance of lignin‐derived compounds residing in SOM (+53%), and this biochemical response is significantly related to shifts in both fungal and bacterial community composition. Specifically, the accumulation of lignin‐derived compounds in SOM is negatively related to the relative abundance of ligninolytic Mycena and Kuehneromyces fungi, and positively related to Microbacteriaceae. Our findings suggest that by altering the composition of microbial communities on decaying fine roots such that their capacity for lignin degradation is reduced, experimental N deposition has slowed fine root litter decay, and increased the contribution of lignin‐derived compounds from fine rootsmore »« less

Authors:

^[1];

^[2];

^[1];

^[3]

School for Environment and Sustainability University of Michigan Ann Arbor MI USA
School for Environment and Sustainability University of Michigan Ann Arbor MI USA, Department of Ecology and Evolutionary Biology University of Michigan Ann Arbor MI USA
Department of Natural Resources and the Environment University of New Hampshire Durham NH USA

Publication Date:: Wed Aug 14 00:00:00 EDT 2019

Sponsoring Org.:: USDOE

OSTI Identifier:: 1557335

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: Global Change Biology

Additional Journal Information:: Journal Name: Global Change Biology Journal Volume: 25 Journal Issue: 12; Journal ID: ISSN 1354-1013

Publisher:: Wiley-Blackwell

Country of Publication:: United Kingdom

Language:: English

Citation Formats


                    Argiroff, William A., Zak, Donald R., Upchurch, Rima A., Salley, Sydney O., and Grandy, A. Stuart. Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots.  United Kingdom: N. p., 2019. 
Web.  doi:10.1111/gcb.14770.

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                    Argiroff, William A., Zak, Donald R., Upchurch, Rima A., Salley, Sydney O., & Grandy, A. Stuart. Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots.  United Kingdom.  https://doi.org/10.1111/gcb.14770

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                    Argiroff, William A., Zak, Donald R., Upchurch, Rima A., Salley, Sydney O., and Grandy, A. Stuart. Wed .  
"Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots".  United Kingdom.  https://doi.org/10.1111/gcb.14770.

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@article{osti_1557335,

  title        = {Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots},

  author       = {Argiroff, William A. and Zak, Donald R. and Upchurch, Rima A. and Salley, Sydney O. and Grandy, A. Stuart},

  abstractNote = {Abstract Fine root litter is a primary source of soil organic matter (SOM), which is a globally important pool of C that is responsive to climate change. We previously established that ~20 years of experimental nitrogen (N) deposition has slowed fine root decay and increased the storage of soil carbon (C; +18%) across a widespread northern hardwood forest ecosystem. However, the microbial mechanisms that have directly slowed fine root decay are unknown. Here, we show that experimental N deposition has decreased the relative abundance of Agaricales fungi (−31%) and increased that of partially ligninolytic Actinobacteria (+24%) on decaying fine roots. Moreover, experimental N deposition has increased the relative abundance of lignin‐derived compounds residing in SOM (+53%), and this biochemical response is significantly related to shifts in both fungal and bacterial community composition. Specifically, the accumulation of lignin‐derived compounds in SOM is negatively related to the relative abundance of ligninolytic Mycena and Kuehneromyces fungi, and positively related to Microbacteriaceae. Our findings suggest that by altering the composition of microbial communities on decaying fine roots such that their capacity for lignin degradation is reduced, experimental N deposition has slowed fine root litter decay, and increased the contribution of lignin‐derived compounds from fine roots to SOM. The microbial responses we observed may explain widespread findings that anthropogenic N deposition increases soil C storage in terrestrial ecosystems. More broadly, our findings directly link composition to function in soil microbial communities, and implicate compositional shifts in mediating biogeochemical processes of global significance.},

  doi          = {10.1111/gcb.14770},

  journal      = {Global Change Biology},

  number       = 12,

  volume       = 25,

  place        = {United Kingdom},

  year         = {Wed Aug 14 00:00:00 EDT 2019},

  month        = {Wed Aug 14 00:00:00 EDT 2019}

}

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Soil Biology and Biochemistry, Vol. 110
DOI: 10.1016/j.soilbio.2017.03.002

Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina)
journal, May 2008

Martinez, Diego; Berka, Randy M.; Henrissat, Bernard
Nature Biotechnology, Vol. 26, Issue 5
DOI: 10.1038/nbt1403

Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing
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Simulated chronic NO ₃ ⁻ deposition reduces soil respiration in northern hardwood forests
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Burton, Andrew J.; Pregitzer, Kurt S.; Crawford, Jeffrey N.
Global Change Biology, Vol. 10, Issue 7
DOI: 10.1111/j.1365-2486.2004.00737.x

Molecular-level changes in soil organic matter composition after 10 years of litter, root and nitrogen manipulation in a temperate forest
journal, October 2018

vandenEnden, Lori; Frey, Serita D.; Nadelhoffer, Knute J.
Biogeochemistry, Vol. 141, Issue 2
DOI: 10.1007/s10533-018-0512-4

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Integrating microbial ecology into ecosystem models: challenges and priorities
journal, September 2011

Treseder, Kathleen K.; Balser, Teri C.; Bradford, Mark A.
Biogeochemistry, Vol. 109, Issue 1-3
DOI: 10.1007/s10533-011-9636-5

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Similar Records

Title: Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots

Abstract

Citation Formats

Anthropogenic N deposition, fungal gene expression, and an increasing soil carbon sink in the Northern Hemisphere journal, July 2019

Ephemeral root modules in Fraxinus mandshurica journal, September 2010

Total carbon and nitrogen in the soils of the world journal, June 1996

Long-term nitrogen addition suppresses microbial degradation, enhances soil carbon storage, and alters the molecular composition of soil organic matter journal, January 2019

Widespread Occurrence of Expressed Fungal Secretory Peroxidases in Forest Soils journal, April 2014

Exploring the genomic diversity of black yeasts and relatives ( Chaetothyriales , Ascomycota ) journal, March 2017

Contrasting soil fungal community responses to experimental nitrogen addition using the large subunit rRNA taxonomic marker and cellobiohydrolase I functional marker journal, August 2014

Extracellular laccases in ascomycetesTrichoderma atroviride andTrichoderma harzianum journal, August 2002

Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes journal, March 2015

A new method for non-parametric multivariate analysis of variance: NON-PARAMETRIC MANOVA FOR ECOLOGY journal, February 2001

Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible journal, April 2014

Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy journal, June 2007

Management intensity alters decomposition via biological pathways journal, August 2010

A Large and Persistent Carbon Sink in the World's Forests journal, July 2011

Anthropogenic N deposition increases soil organic matter accumulation without altering its biochemical composition journal, October 2016

Clearcutting alters decomposition processes and initiates complex restructuring of fungal communities in soil and tree roots journal, January 2018

Lignin-degrading ability of litter-decomposing basidiomycetes from Picea forests of Hokkaido journal, January 2000

Ribosomal Database Project: data and tools for high throughput rRNA analysis journal, November 2013

Nitrogen Cycles: Past, Present, and Future journal, September 2004

The emerging role for bacteria in lignin degradation and bio-product formation journal, June 2011

Simulated nitrogen deposition favors stress-tolerant fungi with low potential for decomposition journal, October 2018

Chronic nitrogen deposition influences the chemical dynamics of leaf litter and fine roots during decomposition journal, September 2017

Effects of long-term nitrogen deposition on fine root decomposition and its extracellular enzyme activities in temperate forests journal, February 2016

Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests journal, July 2014

Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions journal, May 2008

Fungal community on decomposing leaf litter undergoes rapid successional changes journal, October 2012

Nitrogen Deposition Modifies soil Carbon Storage Through Changes in Microbial Enzymatic Activity journal, August 2004

A trait-based approach for modelling microbial litter decomposition journal, May 2012

Simulated Atmospheric Nitrogen Deposition Alters Actinobacterial Community Composition in Forest Soils journal, January 2010

A flexible and efficient template format for circular consensus sequencing and SNP detection journal, June 2010

Fine root decomposition, nutrient mobilization and fungal communities in a pine forest ecosystem journal, April 2015

Long-Term Simulated Atmospheric Nitrogen Deposition Alters Leaf and Fine Root Decomposition journal, April 2017

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities journal, October 2009

Decomposition patterns for foliar litter – A theory for influencing factors journal, November 2014

Contrasting Effects of Substrate and Fertilizer Nitrogen on the Early Stages of Litter Decomposition journal, September 2005

Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi journal, February 2018

Fine root Architecture of nine North American Trees journal, May 2002

Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. journal, August 1990

Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest journal, October 2016

Manganese limitation as a mechanism for reduced decomposition in soils under atmospheric nitrogen deposition journal, December 2018

The influence of microbial communities, management, and soil texture on soil organic matter chemistry journal, May 2009

Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution journal, October 2017

Enzyme production by Mycena galopus mycelium in artificial media and in Picea sitchensis F1 horizon needle litter journal, August 2003

Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species journal, November 2008

Identification of a Novel Toluene-Degrading Bacterium from the Candidate Phylum TM7, as Determined by DNA Stable Isotope Probing journal, May 2009

Review: lignin conversion by manganese peroxidase (MnP) journal, April 2002

UCHIME improves sensitivity and speed of chimera detection journal, June 2011

Anthropogenic N Deposition Alters the Composition of Expressed Class II Fungal Peroxidases journal, February 2018

The Ecology of Soil Carbon: Pools, Vulnerabilities, and Biotic and Abiotic Controls journal, November 2017

Nitrogen deposition increases root production and turnover but slows root decomposition in Pinus elliottii plantations journal, March 2018

Chronic N deposition does not apparently alter the biochemical composition of forest floor and soil organic matter journal, November 2012

Isolation, characterization and function of laccase from Trichoderma journal, November 1992

Anthropogenic N Deposition Slows Decay by Favoring Bacterial Metabolism: Insights from Metagenomic Analyses journal, March 2016

Limited Effects of Variable-Retention Harvesting on Fungal Communities Decomposing Fine Roots in Coastal Temperate Rainforests journal, February 2018

Enzymatic "Combustion": The Microbial Degradation of Lignin journal, October 1987

Use of multivariate methods in forest research site selection journal, November 1991

Atmospheric Nitrate Deposition, Microbial Community Composition, and Enzyme Activity in Northern Hardwood Forests journal, January 2004

Fine root decomposition rates do not mirror those of leaf litter among temperate tree species journal, October 2009

Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation journal, February 2005

Factors That Affect Large Subunit Ribosomal DNA Amplicon Sequencing Studies of Fungal Communities: Classification Method, Primer Choice, and Error journal, April 2012

Accurate, Rapid Taxonomic Classification of Fungal Large-Subunit rRNA Genes journal, December 2011

Microbial phylogenetic profiling with the Pacific Biosciences sequencing platform journal, March 2013

Atmospheric N Deposition Increases Bacterial Laccase-Like Multicopper Oxidases: Implications for Organic Matter Decay journal, May 2014

Anthropogenic nitrogen deposition enhances carbon sequestration in boreal soils journal, April 2015

phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data journal, April 2013

Linking litter decomposition of above- and below-ground organs to plant-soil feedbacks worldwide journal, June 2013

Resilience vs. historical contingency in microbial responses to environmental change journal, May 2015

Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions journal, October 2008

A keystone microbial enzyme for nitrogen control of soil carbon storage journal, August 2018

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools journal, November 2012

SIMULATED ATMOSPHERIC NO 3 − DEPOSITION INCREASES SOIL ORGANIC MATTER BY SLOWING DECOMPOSITION journal, December 2008

Microbial Mechanisms Mediating Increased Soil C Storage under Elevated Atmospheric N Deposition journal, December 2012

Development of novel assays for lignin degradation: comparative analysis of bacterial and fungal lignin degraders journal, January 2010

Isolation of bacterial strains able to metabolize lignin from screening of environmental samples journal, June 2012

The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes journal, June 2012

Simulated chronic nitrogen deposition increases carbon storage in Northern Temperate forests journal, November 2007

Chronic nitrate additions dramatically increase the export of carbon and nitrogen from northern hardwood ecosystems journal, April 2004

Anthropogenic N deposition, fungal gene expression, and an increasing soil carbon sink in the Northern Hemisphere
journal, July 2019

Ephemeral root modules in Fraxinus mandshurica
journal, September 2010

Total carbon and nitrogen in the soils of the world
journal, June 1996

Long-term nitrogen addition suppresses microbial degradation, enhances soil carbon storage, and alters the molecular composition of soil organic matter
journal, January 2019

Widespread Occurrence of Expressed Fungal Secretory Peroxidases in Forest Soils
journal, April 2014

Exploring the genomic diversity of black yeasts and relatives ( Chaetothyriales , Ascomycota )
journal, March 2017

Contrasting soil fungal community responses to experimental nitrogen addition using the large subunit rRNA taxonomic marker and cellobiohydrolase I functional marker
journal, August 2014

Extracellular laccases in ascomycetesTrichoderma atroviride andTrichoderma harzianum
journal, August 2002

Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes
journal, March 2015

A new method for non-parametric multivariate analysis of variance: NON-PARAMETRIC MANOVA FOR ECOLOGY
journal, February 2001

Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible
journal, April 2014

Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

Management intensity alters decomposition via biological pathways
journal, August 2010

A Large and Persistent Carbon Sink in the World's Forests
journal, July 2011

Anthropogenic N deposition increases soil organic matter accumulation without altering its biochemical composition
journal, October 2016

Clearcutting alters decomposition processes and initiates complex restructuring of fungal communities in soil and tree roots
journal, January 2018

Lignin-degrading ability of litter-decomposing basidiomycetes from Picea forests of Hokkaido
journal, January 2000

Ribosomal Database Project: data and tools for high throughput rRNA analysis
journal, November 2013

Nitrogen Cycles: Past, Present, and Future
journal, September 2004

The emerging role for bacteria in lignin degradation and bio-product formation
journal, June 2011

Simulated nitrogen deposition favors stress-tolerant fungi with low potential for decomposition
journal, October 2018

Chronic nitrogen deposition influences the chemical dynamics of leaf litter and fine roots during decomposition
journal, September 2017

Effects of long-term nitrogen deposition on fine root decomposition and its extracellular enzyme activities in temperate forests
journal, February 2016

Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests
journal, July 2014

Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions
journal, May 2008

Fungal community on decomposing leaf litter undergoes rapid successional changes
journal, October 2012

Nitrogen Deposition Modifies soil Carbon Storage Through Changes in Microbial Enzymatic Activity
journal, August 2004

A trait-based approach for modelling microbial litter decomposition
journal, May 2012

Simulated Atmospheric Nitrogen Deposition Alters Actinobacterial Community Composition in Forest Soils
journal, January 2010

A flexible and efficient template format for circular consensus sequencing and SNP detection
journal, June 2010

Fine root decomposition, nutrient mobilization and fungal communities in a pine forest ecosystem
journal, April 2015

Long-Term Simulated Atmospheric Nitrogen Deposition Alters Leaf and Fine Root Decomposition
journal, April 2017

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

Decomposition patterns for foliar litter – A theory for influencing factors
journal, November 2014

Contrasting Effects of Substrate and Fertilizer Nitrogen on the Early Stages of Litter Decomposition
journal, September 2005

Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi
journal, February 2018

Fine root Architecture of nine North American Trees
journal, May 2002

Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species.
journal, August 1990

Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest
journal, October 2016

Manganese limitation as a mechanism for reduced decomposition in soils under atmospheric nitrogen deposition
journal, December 2018

The influence of microbial communities, management, and soil texture on soil organic matter chemistry
journal, May 2009

Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution
journal, October 2017

Enzyme production by Mycena galopus mycelium in artificial media and in Picea sitchensis F1 horizon needle litter
journal, August 2003

Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species
journal, November 2008

Identification of a Novel Toluene-Degrading Bacterium from the Candidate Phylum TM7, as Determined by DNA Stable Isotope Probing
journal, May 2009

Review: lignin conversion by manganese peroxidase (MnP)
journal, April 2002

UCHIME improves sensitivity and speed of chimera detection
journal, June 2011

Anthropogenic N Deposition Alters the Composition of Expressed Class II Fungal Peroxidases
journal, February 2018

The Ecology of Soil Carbon: Pools, Vulnerabilities, and Biotic and Abiotic Controls
journal, November 2017

Nitrogen deposition increases root production and turnover but slows root decomposition in Pinus elliottii plantations
journal, March 2018

Chronic N deposition does not apparently alter the biochemical composition of forest floor and soil organic matter
journal, November 2012

Isolation, characterization and function of laccase from Trichoderma
journal, November 1992

Anthropogenic N Deposition Slows Decay by Favoring Bacterial Metabolism: Insights from Metagenomic Analyses
journal, March 2016

Limited Effects of Variable-Retention Harvesting on Fungal Communities Decomposing Fine Roots in Coastal Temperate Rainforests
journal, February 2018

Enzymatic "Combustion": The Microbial Degradation of Lignin
journal, October 1987

Use of multivariate methods in forest research site selection
journal, November 1991

Atmospheric Nitrate Deposition, Microbial Community Composition, and Enzyme Activity in Northern Hardwood Forests
journal, January 2004

Fine root decomposition rates do not mirror those of leaf litter among temperate tree species
journal, October 2009

Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation
journal, February 2005

Factors That Affect Large Subunit Ribosomal DNA Amplicon Sequencing Studies of Fungal Communities: Classification Method, Primer Choice, and Error
journal, April 2012

Accurate, Rapid Taxonomic Classification of Fungal Large-Subunit rRNA Genes
journal, December 2011

Microbial phylogenetic profiling with the Pacific Biosciences sequencing platform
journal, March 2013

Atmospheric N Deposition Increases Bacterial Laccase-Like Multicopper Oxidases: Implications for Organic Matter Decay
journal, May 2014

Anthropogenic nitrogen deposition enhances carbon sequestration in boreal soils
journal, April 2015

phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013

Linking litter decomposition of above- and below-ground organs to plant-soil feedbacks worldwide
journal, June 2013

Resilience vs. historical contingency in microbial responses to environmental change
journal, May 2015

Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions
journal, October 2008

A keystone microbial enzyme for nitrogen control of soil carbon storage
journal, August 2018

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

SIMULATED ATMOSPHERIC NO ₃ ⁻ DEPOSITION INCREASES SOIL ORGANIC MATTER BY SLOWING DECOMPOSITION
journal, December 2008

Microbial Mechanisms Mediating Increased Soil C Storage under Elevated Atmospheric N Deposition
journal, December 2012

Development of novel assays for lignin degradation: comparative analysis of bacterial and fungal lignin degraders
journal, January 2010

Isolation of bacterial strains able to metabolize lignin from screening of environmental samples
journal, June 2012

The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012

Simulated chronic nitrogen deposition increases carbon storage in Northern Temperate forests
journal, November 2007

Chronic nitrate additions dramatically increase the export of carbon and nitrogen from northern hardwood ecosystems
journal, April 2004

The contentious nature of soil organic matter
journal, November 2015

Formation of soil organic matter via biochemical and physical pathways of litter mass loss
journal, September 2015

Are Basidiomycete Laccase Gene Abundance and Composition Related to Reduced Lignolytic Activity Under Elevated Atmospheric NO3 − Deposition in a Northern Hardwood Forest?
journal, September 2008