Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States

Mackelprang, Rachel; Grube, Alyssa M.; Lamendella, Regina; Jesus, Ederson da C.; Copeland, Alex; Liang, Chao; Jackson, Randall D.; Rice, Charles W.; Kapucija, Stefanie; Parsa, Bayan; Tringe, Susannah G.; Tiedje, James M.; Jansson, Janet K.

doi:10.3389/fmicb.2018.01775

Title: Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States

Abstract

The North American prairie covered about 3.6 million-km2 of the continent prior to European contact. Only 1–2% of the original prairie remains, but the soils that developed under these prairies are some of the most productive and fertile in the world, containing over 35% of the soil carbon in the continental United States. Cultivation may alter microbial diversity and composition, influencing the metabolism of carbon, nitrogen, and other elements. Here, we explored the structure and functional potential of the soil microbiome in paired cultivated-corn (at the time of sampling) and never-cultivated native prairie soils across a three-states transect (Wisconsin, Iowa, and Kansas) using metagenomic and 16S rRNA gene sequencing and lipid analysis. At the Wisconsin site, we also sampled adjacent restored prairie and switchgrass plots. We found that agricultural practices drove differences in community composition and diversity across the transect. Microbial biomass in prairie samples was twice that of cultivated soils, but alpha diversity was higher with cultivation. Metagenome analyses revealed denitrification and starch degradation genes were abundant across all soils, as were core genes involved in response to osmotic stress, resource transport, and environmental sensing. Together, these data indicate that cultivation shifted the microbiome in consistent ways across differentmore »« less

Authors:: Mackelprang, Rachel; Grube, Alyssa M.; Lamendella, Regina; Jesus, Ederson da C.; Copeland, Alex; Liang, Chao; Jackson, Randall D.; Rice, Charles W.; Kapucija, Stefanie; Parsa, Bayan; Tringe, Susannah G.; Tiedje, James M.; Jansson, Janet K.

Publication Date:: Wed Aug 15 00:00:00 EDT 2018

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); PNNL Laboratory Directed Research and Development (LDRD) Program; National Science Foundation (NSF); Howard Hughes Medical Inst. (HHMI) (United States)

OSTI Identifier:: 1464646

Alternate Identifier(s):: OSTI ID: 1477362; OSTI ID: 1503565

Report Number(s):: PNNL-SA-134003
Journal ID: ISSN 1664-302X; 1775

Grant/Contract Number:: AC02-05CH11231; FC02-07ER64494; AC05-76RL01830; DBI-1248096; RCN 1051481

Resource Type:: Journal Article: Published Article

Journal Name:: Frontiers in Microbiology

Additional Journal Information:: Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X

Publisher:: Frontiers Media SA

Country of Publication:: Switzerland

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; soil microbiome; land management; metagenomics; native prairie; climate change; carbon cycle; nitrogen cycle; Soil Microbiome, land management, metagenomics, native prairie, climate change, carbon cycle, nitrogen cycle

Citation Formats


                    Mackelprang, Rachel, Grube, Alyssa M., Lamendella, Regina, Jesus, Ederson da C., Copeland, Alex, Liang, Chao, Jackson, Randall D., Rice, Charles W., Kapucija, Stefanie, Parsa, Bayan, Tringe, Susannah G., Tiedje, James M., and Jansson, Janet K. Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States.  Switzerland: N. p., 2018. 
        Web.  doi:10.3389/fmicb.2018.01775.

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                    Mackelprang, Rachel, Grube, Alyssa M., Lamendella, Regina, Jesus, Ederson da C., Copeland, Alex, Liang, Chao, Jackson, Randall D., Rice, Charles W., Kapucija, Stefanie, Parsa, Bayan, Tringe, Susannah G., Tiedje, James M., & Jansson, Janet K. Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States.  Switzerland.  https://doi.org/10.3389/fmicb.2018.01775

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                    Mackelprang, Rachel, Grube, Alyssa M., Lamendella, Regina, Jesus, Ederson da C., Copeland, Alex, Liang, Chao, Jackson, Randall D., Rice, Charles W., Kapucija, Stefanie, Parsa, Bayan, Tringe, Susannah G., Tiedje, James M., and Jansson, Janet K. 2018.  
        "Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States".  Switzerland.  https://doi.org/10.3389/fmicb.2018.01775.

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@article{osti_1464646,

  title        = {Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States},

  author       = {Mackelprang, Rachel and Grube, Alyssa M. and Lamendella, Regina and Jesus, Ederson da C. and Copeland, Alex and Liang, Chao and Jackson, Randall D. and Rice, Charles W. and Kapucija, Stefanie and Parsa, Bayan and Tringe, Susannah G. and Tiedje, James M. and Jansson, Janet K.},

  abstractNote = {The North American prairie covered about 3.6 million-km2 of the continent prior to European contact. Only 1–2% of the original prairie remains, but the soils that developed under these prairies are some of the most productive and fertile in the world, containing over 35% of the soil carbon in the continental United States. Cultivation may alter microbial diversity and composition, influencing the metabolism of carbon, nitrogen, and other elements. Here, we explored the structure and functional potential of the soil microbiome in paired cultivated-corn (at the time of sampling) and never-cultivated native prairie soils across a three-states transect (Wisconsin, Iowa, and Kansas) using metagenomic and 16S rRNA gene sequencing and lipid analysis. At the Wisconsin site, we also sampled adjacent restored prairie and switchgrass plots. We found that agricultural practices drove differences in community composition and diversity across the transect. Microbial biomass in prairie samples was twice that of cultivated soils, but alpha diversity was higher with cultivation. Metagenome analyses revealed denitrification and starch degradation genes were abundant across all soils, as were core genes involved in response to osmotic stress, resource transport, and environmental sensing. Together, these data indicate that cultivation shifted the microbiome in consistent ways across different regions of the prairie, but also suggest that many functions are resilient to changes caused by land management practices – perhaps reflecting adaptations to conditions common to tallgrass prairie soils in the region (e.g., soil type, parent material, development under grasses, temperature and rainfall patterns, and annual freeze-thaw cycles). These findings are important for understanding the long-term consequences of land management practices to prairie soil microbial communities and their genetic potential to carry out key functions.},

  doi          = {10.3389/fmicb.2018.01775},

  url          = {https://www.osti.gov/biblio/1464646},
  journal      = {Frontiers in Microbiology},

  issn         = {1664-302X},

  number       = ,

  volume       = 9,

  place        = {Switzerland},

  year         = {Wed Aug 15 00:00:00 EDT 2018},

  month        = {Wed Aug 15 00:00:00 EDT 2018}

}

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Fish, Jordan A.; Chai, Benli; Wang, Qiong
Frontiers in Microbiology, Vol. 4
https://doi.org/10.3389/fmicb.2013.00291

Influence of corn, switchgrass, and prairie cropping systems on soil microbial communities in the upper Midwest of the United States
journal, December 2015

Jesus, Ederson da C.; Liang, Chao; Quensen, John F.
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https://doi.org/10.1111/gcbb.12289

Redesigning Agriculture
journal, January 2006

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BioScience, Vol. 56, Issue 10
https://doi.org/10.1641/0006-3568(2006)56[839:RA]2.0.CO;2

Soil microbial community composition in tallgrass prairie restorations converge with remnants across a 27‐year chronosequence
journal, July 2017

Barber, Nicholas A.; Chantos‐Davidson, Karley M.; Amel Peralta, Rene
Environmental Microbiology, Vol. 19, Issue 8
https://doi.org/10.1111/1462-2920.13785

Microorganisms and their residues under restored perennial grassland communities of varying diversity
journal, December 2016

Liang, Chao; Kao-Kniffin, Jenny; Sanford, Gregg R.
Soil Biology and Biochemistry, Vol. 103
https://doi.org/10.1016/j.soilbio.2016.08.002

Structure, fluctuation and magnitude of a natural grassland soil metagenome
journal, February 2012

Delmont, Tom O.; Prestat, Emmanuel; Keegan, Kevin P.
The ISME Journal, Vol. 6, Issue 9
https://doi.org/10.1038/ismej.2011.197

A high-resolution assessment on global nitrogen flows in cropland
journal, April 2010

Liu, Junguo; You, Liangzhi; Amini, Manouchehr
Proceedings of the National Academy of Sciences, Vol. 107, Issue 17
https://doi.org/10.1073/pnas.0913658107

A Recalibration of the Hydrometer Method for Making Mechanical Analysis of Soils1
journal, January 1951

Bouyoucos, George John
Agronomy Journal, Vol. 43, Issue 9
https://doi.org/10.2134/agronj1951.00021962004300090005x

Changes in soil Carbon Storage After Cultivation
journal, January 1986

Mann, L. K.
Soil Science, Vol. 142, Issue 5
https://doi.org/10.1097/00010694-198611000-00006

FOAM (Functional Ontology Assignments for Metagenomes): a Hidden Markov Model (HMM) database with environmental focus
journal, September 2014

Prestat, Emmanuel; David, Maude M.; Hultman, Jenni
Nucleic Acids Research, Vol. 42, Issue 19
https://doi.org/10.1093/nar/gku702

Diversity and dynamics of microbial communities in soils from agro-ecosystems
journal, June 2003

Buckley, Daniel H.; Schmidt, Thomas M.
Environmental Microbiology, Vol. 5, Issue 6
https://doi.org/10.1046/j.1462-2920.2003.00404.x

Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use
journal, November 2008

Acosta-Martínez, V.; Dowd, S.; Sun, Y.
Soil Biology and Biochemistry, Vol. 40, Issue 11
https://doi.org/10.1016/j.soilbio.2008.07.022

Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011

Hess, M.; Sczyrba, A.; Egan, R.
Science, Vol. 331, Issue 6016
https://doi.org/10.1126/science.1200387

Targeted Discovery of Glycoside Hydrolases from a Switchgrass-Adapted Compost Community
journal, January 2010

Allgaier, Martin; Reddy, Amitha; Park, Joshua I.
PLoS ONE, Vol. 5, Issue 1
https://doi.org/10.1371/journal.pone.0008812

Microbial Biomass and Community Structure in a Sequence of Soils with Increasing Fertility and Changing Land Use
journal, August 2000

Yao, H.; He, Z.; Wilson, M. J.
Microbial Ecology, Vol. 40, Issue 3
https://doi.org/10.1007/s002480000053

Works referencing / citing this record:

Metagenomic analysis of the microbial community structure in protected wetlands in the Maritza River Basin
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Iliev, Ivan; Marhova, Mariana; Kostadinova, Sonya
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Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
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https://doi.org/10.1128/msystems.00061-19

Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota
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The known and the unknown in soil microbial ecology
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PLOS ONE, Vol. 15, Issue 1
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Title: Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States

Abstract

Citation Formats

Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils journal, May 2005

IMG/M 4 version of the integrated metagenome comparative analysis system journal, October 2013

Soil depth and crop determinants of bacterial communities under ten biofuel cropping systems journal, September 2017

The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4) journal, October 2015

Beyond the Venn diagram: the hunt for a core microbiome: The hunt for a core microbiome journal, October 2011

Phylogenetic Analysis of Nitrite, Nitric Oxide, and Nitrous Oxide Respiratory Enzymes Reveal a Complex Evolutionary History for Denitrification journal, July 2008

Functional response of soil microbial communities to tillage, cover crops and nitrogen fertilization journal, December 2016

Long-Term No-tillage Effects on Soil Properties and Continuous Corn Yields journal, January 1994

A microplate fluorimetric assay for the study of enzyme diversity in soils journal, October 2001

Long-Term Nitrogen Amendment Alters the Diversity and Assemblage of Soil Bacterial Communities in Tallgrass Prairie journal, June 2013

Long term tillage, cover crop, and fertilization effects on microbial community structure, activity: Implications for soil quality journal, October 2015

Changes in N-Transforming Archaea and Bacteria in Soil during the Establishment of Bioenergy Crops journal, September 2011

Soil carbon stocks and land use change: a meta analysis journal, April 2002

Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States journal, October 2013

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics journal, January 2009

The missing link in grassland restoration: arbuscular mycorrhizal fungi inoculation increases plant diversity and accelerates succession journal, December 2016

Bouncing Back: Plant-Associated Soil Microbes Respond Rapidly to Prairie Establishment journal, December 2014

Detection of short-term cropping system-induced changes to soil bacterial communities differs among four molecular characterization methods journal, May 2016

Soil carbon lost from Mollisols of the North Central U.S.A. with 20 years of agricultural best management practices journal, November 2012

Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe journal, August 2015

Lipid Analysis in Microbial Ecology journal, September 1989

Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils journal, November 2012

Global biogeography of microbial nitrogen-cycling traits in soil journal, July 2016

Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients journal, December 2011

The carbohydrate-active enzymes database (CAZy) in 2013 journal, November 2013

Carbon Budgets for a Prairie and Agroecosystems: Effects of land use and Interannual Variability journal, August 2002

Cross-phosphorylation of bacterial serine/threonine and tyrosine protein kinases on key regulatory residues journal, September 2014

Soil Microbial and Biochemical Changes Associated with Reduced Tillage1 journal, January 1980

Crop monoculture rather than agriculture reduces the spatial turnover of soil bacterial communities at a regional scale: Reduced turnover of soil bacterial communities journal, June 2014

Organic Carbon, pH, and Aggregation of the Soil of the Morrow Plats as Affected by Type of Cropping and Manurial Addition1 journal, January 1940

Basic local alignment search tool journal, October 1990

Back to the Future of Soil Metagenomics journal, February 2016

Quantity and Spatial Variability of Soil Carbon in the Conterminous United States journal, January 2006

A Rapid Method of Total Lipid Extraction and Purification journal, January 1959

Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes journal, February 2012

Long-Term Coffee Monoculture Alters Soil Chemical Properties and Microbial Communities journal, April 2018

Variations in microbial community composition through two soil depth profiles journal, January 2003

A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi journal, March 2010

FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix journal, April 2009

Measurements and Modeling of Carbon and Nitrogen Cycling in Agroecosystems of Southern Wisconsin: Potential for SOC Sequestration during the Next 50 Years journal, April 2001

Glucoamylases: structural and biotechnological aspects journal, December 2010

Changes in microbial community metabolism and labile organic matter fractions as early indicators of the impact of management on soil biological quality journal, April 2000

Development of soil microbial communities during tallgrass prairie restoration journal, February 2010

Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes journal, November 2004

No-Tillage Agriculture journal, June 1980

Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores journal, July 2010

Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2 journal, February 2012

Climate-smart soils journal, April 2016

Hemicelluloses journal, June 2010

Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea journal, August 2016

Nitrogen and Carbon Leaching in Agroecosystems and Their Role in Denitrification Potential journal, January 2001

Mycorrhizal ecology and evolution: the past, the present, and the future journal, February 2015

MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data journal, June 2016

A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria journal, July 2010

Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil journal, May 2016

Midwest Cropping System Effects on Soil Properties and on a Soil Quality Index journal, January 2011

Soil carbon debt of 12,000 years of human land use journal, August 2017

Enhancing the Multifunctionality of US Agriculture journal, January 2010

Shifts in the bacterial community composition along deep soil profiles in monospecific and mixed stands of Eucalyptus grandis and Acacia mangium journal, July 2017

Bioenergy cropping systems that incorporate native grasses stimulate growth of plant-associated soil microbes in the absence of nitrogen fertilization journal, October 2016

Prairie Conservation in North America journal, June 1994

Search and clustering orders of magnitude faster than BLAST journal, August 2010

Velvet: Algorithms for de novo short read assembly using de Bruijn graphs journal, February 2008

Effects of Conservation Agriculture and Fertilization on Soil Microbial Diversity and Activity journal, July 2015

Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates journal, January 2010

Deep soil organic matter—a key but poorly understood component of terrestrial C cycle journal, May 2010

Soil nitrate analysis by cadmium reduction journal, January 1981

Computational Improvements Reveal Great Bacterial Diversity and High Metal Toxicity in Soil journal, August 2005

Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands journal, February 2000

Tackling soil diversity with the assembly of large, complex metagenomes journal, March 2014

Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest journal, April 2005

Influence of Herbicide Triasulfuron on Soil Microbial Community in an Unamended Soil and a Soil Amended with Organic Residues journal, March 2017

Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie journal, December 1998

Diversity and Activity of Free-Living Nitrogen-Fixing Bacteria and Total Bacteria in Organic and Conventionally Managed Soils journal, December 2010

Accelerated Profile HMM Searches journal, October 2011

FunGene: the functional gene pipeline and repository journal, January 2013

Influence of corn, switchgrass, and prairie cropping systems on soil microbial communities in the upper Midwest of the United States journal, December 2015

Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils
journal, May 2005

IMG/M 4 version of the integrated metagenome comparative analysis system
journal, October 2013

Soil depth and crop determinants of bacterial communities under ten biofuel cropping systems
journal, September 2017

The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4)
journal, October 2015

Beyond the Venn diagram: the hunt for a core microbiome: The hunt for a core microbiome
journal, October 2011

Phylogenetic Analysis of Nitrite, Nitric Oxide, and Nitrous Oxide Respiratory Enzymes Reveal a Complex Evolutionary History for Denitrification
journal, July 2008

Functional response of soil microbial communities to tillage, cover crops and nitrogen fertilization
journal, December 2016

Long-Term No-tillage Effects on Soil Properties and Continuous Corn Yields
journal, January 1994

A microplate fluorimetric assay for the study of enzyme diversity in soils
journal, October 2001

Long-Term Nitrogen Amendment Alters the Diversity and Assemblage of Soil Bacterial Communities in Tallgrass Prairie
journal, June 2013

Long term tillage, cover crop, and fertilization effects on microbial community structure, activity: Implications for soil quality
journal, October 2015

Changes in N-Transforming Archaea and Bacteria in Soil during the Establishment of Bioenergy Crops
journal, September 2011

Soil carbon stocks and land use change: a meta analysis
journal, April 2002

Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States
journal, October 2013

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

The missing link in grassland restoration: arbuscular mycorrhizal fungi inoculation increases plant diversity and accelerates succession
journal, December 2016

Bouncing Back: Plant-Associated Soil Microbes Respond Rapidly to Prairie Establishment
journal, December 2014

Detection of short-term cropping system-induced changes to soil bacterial communities differs among four molecular characterization methods
journal, May 2016

Soil carbon lost from Mollisols of the North Central U.S.A. with 20 years of agricultural best management practices
journal, November 2012

Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe
journal, August 2015

Lipid Analysis in Microbial Ecology
journal, September 1989

Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils
journal, November 2012

Global biogeography of microbial nitrogen-cycling traits in soil
journal, July 2016

Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients
journal, December 2011

The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

Carbon Budgets for a Prairie and Agroecosystems: Effects of land use and Interannual Variability
journal, August 2002

Cross-phosphorylation of bacterial serine/threonine and tyrosine protein kinases on key regulatory residues
journal, September 2014

Soil Microbial and Biochemical Changes Associated with Reduced Tillage1
journal, January 1980

Crop monoculture rather than agriculture reduces the spatial turnover of soil bacterial communities at a regional scale: Reduced turnover of soil bacterial communities
journal, June 2014

Organic Carbon, pH, and Aggregation of the Soil of the Morrow Plats as Affected by Type of Cropping and Manurial Addition1
journal, January 1940

Basic local alignment search tool
journal, October 1990

Back to the Future of Soil Metagenomics
journal, February 2016

Quantity and Spatial Variability of Soil Carbon in the Conterminous United States
journal, January 2006

A Rapid Method of Total Lipid Extraction and Purification
journal, January 1959

Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes
journal, February 2012

Long-Term Coffee Monoculture Alters Soil Chemical Properties and Microbial Communities
journal, April 2018

Variations in microbial community composition through two soil depth profiles
journal, January 2003

A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi
journal, March 2010

FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009

Measurements and Modeling of Carbon and Nitrogen Cycling in Agroecosystems of Southern Wisconsin: Potential for SOC Sequestration during the Next 50 Years
journal, April 2001

Glucoamylases: structural and biotechnological aspects
journal, December 2010

Changes in microbial community metabolism and labile organic matter fractions as early indicators of the impact of management on soil biological quality
journal, April 2000

Development of soil microbial communities during tallgrass prairie restoration
journal, February 2010

Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes
journal, November 2004

No-Tillage Agriculture
journal, June 1980

Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores
journal, July 2010

Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2
journal, February 2012

Climate-smart soils
journal, April 2016

Hemicelluloses
journal, June 2010

Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea
journal, August 2016

Nitrogen and Carbon Leaching in Agroecosystems and Their Role in Denitrification Potential
journal, January 2001

Mycorrhizal ecology and evolution: the past, the present, and the future
journal, February 2015

MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data
journal, June 2016

A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria
journal, July 2010

Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil
journal, May 2016

Midwest Cropping System Effects on Soil Properties and on a Soil Quality Index
journal, January 2011

Soil carbon debt of 12,000 years of human land use
journal, August 2017

Enhancing the Multifunctionality of US Agriculture
journal, January 2010

Shifts in the bacterial community composition along deep soil profiles in monospecific and mixed stands of Eucalyptus grandis and Acacia mangium
journal, July 2017

Bioenergy cropping systems that incorporate native grasses stimulate growth of plant-associated soil microbes in the absence of nitrogen fertilization
journal, October 2016

Prairie Conservation in North America
journal, June 1994

Search and clustering orders of magnitude faster than BLAST
journal, August 2010

Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008

Effects of Conservation Agriculture and Fertilization on Soil Microbial Diversity and Activity
journal, July 2015

Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates
journal, January 2010

Deep soil organic matter—a key but poorly understood component of terrestrial C cycle
journal, May 2010

Soil nitrate analysis by cadmium reduction
journal, January 1981

Computational Improvements Reveal Great Bacterial Diversity and High Metal Toxicity in Soil
journal, August 2005

Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands
journal, February 2000

Tackling soil diversity with the assembly of large, complex metagenomes
journal, March 2014

Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest
journal, April 2005

Influence of Herbicide Triasulfuron on Soil Microbial Community in an Unamended Soil and a Soil Amended with Organic Residues
journal, March 2017

Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie
journal, December 1998

Diversity and Activity of Free-Living Nitrogen-Fixing Bacteria and Total Bacteria in Organic and Conventionally Managed Soils
journal, December 2010

Accelerated Profile HMM Searches
journal, October 2011

FunGene: the functional gene pipeline and repository
journal, January 2013

Influence of corn, switchgrass, and prairie cropping systems on soil microbial communities in the upper Midwest of the United States
journal, December 2015

Redesigning Agriculture
journal, January 2006

Soil microbial community composition in tallgrass prairie restorations converge with remnants across a 27‐year chronosequence
journal, July 2017

Microorganisms and their residues under restored perennial grassland communities of varying diversity
journal, December 2016