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Title: Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA

Abstract

Rhizosphere microbial communities play an essential role in determining plant productivity, particularly in agriculturally marginal environments. Perennial plants like switchgrass (Panicum virgatum) are thought to particularly influence microbial community composition and function within their rhizosphere. We compared microbial communities in switchgrass rhizospheres and their associated bulk soils in two regions of the U.S. upper Midwest (Michigan and Wisconsin) with contrasting soil types, and at two site types with differing switchgrass establishment ages and management intensities. We characterized microbial communities with a range of culture-independent methods, including amplicon sequencing of 16S/18S rRNA and nifH genes, and membrane lipid profiling. In addition, we quantified abundances of soil amino sugars, a time-integrative indicator of microbial necromass. We found that amino sugar contents and microbial lipid profiles differed between rhizosphere and bulk soils, while DNA-based assays did not provide this discriminatory power. Differences between rhizosphere and bulk soils were not significantly affected by region or site type. Rhizosphere soils had higher microbial lipid abundances, particularly those associated with arbuscular mycorrhizal fungi and Gram-negative bacteria, while amino sugar abundances decreased in the rhizosphere. In conclusion, our findings suggest switchgrass rhizospheres systematically stimulate microbial growth and microbial residue turnover.

Authors:
 [1];  [2];  [3];  [4];  [3];  [3];  [2]
  1. University of Wisconsin, Madison, WI (United States); Chinese Academy of Sciences (CAS), Shenyang (China)
  2. University of Wisconsin, Madison, WI (United States); Michigan State University, East Lansing, MI (United States)
  3. University of Wisconsin, Madison, WI (United States)
  4. Michigan State University, East Lansing, MI (United States)
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1418539
Alternate Identifier(s):
OSTI ID: 1399029
Grant/Contract Number:  
FC02-07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
Soil Biology and Biochemistry
Additional Journal Information:
Journal Volume: 94; Journal Issue: C; Journal ID: ISSN 0038-0717
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; pyrosequencing; nifH; lipid; amino sugar; plant–microbe interaction; rhizosphere; switchgrass

Citation Formats

Liang, Chao, Jesus, Ederson da C., Duncan, David S., Quensen, John F., Jackson, Randall D., Balser, Teri C., and Tiedje, James M. Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA. United States: N. p., 2015. Web. doi:10.1016/j.soilbio.2015.11.020.
Liang, Chao, Jesus, Ederson da C., Duncan, David S., Quensen, John F., Jackson, Randall D., Balser, Teri C., & Tiedje, James M. Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA. United States. https://doi.org/10.1016/j.soilbio.2015.11.020
Liang, Chao, Jesus, Ederson da C., Duncan, David S., Quensen, John F., Jackson, Randall D., Balser, Teri C., and Tiedje, James M. Sat . "Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA". United States. https://doi.org/10.1016/j.soilbio.2015.11.020. https://www.osti.gov/servlets/purl/1418539.
@article{osti_1418539,
title = {Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA},
author = {Liang, Chao and Jesus, Ederson da C. and Duncan, David S. and Quensen, John F. and Jackson, Randall D. and Balser, Teri C. and Tiedje, James M.},
abstractNote = {Rhizosphere microbial communities play an essential role in determining plant productivity, particularly in agriculturally marginal environments. Perennial plants like switchgrass (Panicum virgatum) are thought to particularly influence microbial community composition and function within their rhizosphere. We compared microbial communities in switchgrass rhizospheres and their associated bulk soils in two regions of the U.S. upper Midwest (Michigan and Wisconsin) with contrasting soil types, and at two site types with differing switchgrass establishment ages and management intensities. We characterized microbial communities with a range of culture-independent methods, including amplicon sequencing of 16S/18S rRNA and nifH genes, and membrane lipid profiling. In addition, we quantified abundances of soil amino sugars, a time-integrative indicator of microbial necromass. We found that amino sugar contents and microbial lipid profiles differed between rhizosphere and bulk soils, while DNA-based assays did not provide this discriminatory power. Differences between rhizosphere and bulk soils were not significantly affected by region or site type. Rhizosphere soils had higher microbial lipid abundances, particularly those associated with arbuscular mycorrhizal fungi and Gram-negative bacteria, while amino sugar abundances decreased in the rhizosphere. In conclusion, our findings suggest switchgrass rhizospheres systematically stimulate microbial growth and microbial residue turnover.},
doi = {10.1016/j.soilbio.2015.11.020},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 94,
place = {United States},
year = {Sat Dec 19 00:00:00 EST 2015},
month = {Sat Dec 19 00:00:00 EST 2015}
}

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Cited by: 23 works
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Works referenced in this record:

Changes in Soil Microbial Community Structure in a Tallgrass Prairie Chronosequence
journal, January 2005

  • Allison, Victoria J.; Miller, R. Michael; Jastrow, Julie D.
  • Soil Science Society of America Journal, Vol. 69, Issue 5
  • DOI: 10.2136/sssaj2004.0252

Relationships between microbial indices in roots and silt loam soils forming a gradient in soil organic matter
journal, September 2006


Diversity of Nitrogen-Fixing Bacteria Associated with Switchgrass in the Native Tallgrass Prairie of Northern Oklahoma
journal, July 2014

  • Bahulikar, Rahul A.; Torres-Jerez, Ivone; Worley, Eric
  • Applied and Environmental Microbiology, Vol. 80, Issue 18
  • DOI: 10.1128/AEM.02091-14

Impacts of bulk soil microbial community structure on rhizosphere microbiomes of Zea mays
journal, March 2015

  • Bakker, Matthew G.; Chaparro, Jacqueline M.; Manter, Daniel K.
  • Plant and Soil, Vol. 392, Issue 1-2
  • DOI: 10.1007/s11104-015-2446-0

Hydrometer Method Improved for Making Particle Size Analyses of Soils1
journal, January 1962


Microbial Community Dynamics Associated with Rhizosphere Carbon Flow
journal, November 2003


Selective progressive response of soil microbial community to wild oat roots
journal, November 2008

  • DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z.
  • The ISME Journal, Vol. 3, Issue 2
  • DOI: 10.1038/ismej.2008.103

Microbial community composition and rhizodeposit-carbon assimilation in differently managed temperate grassland soils
journal, January 2009

  • Denef, Karolien; Roobroeck, Dries; Manimel Wadu, Mihiri C. W.
  • Soil Biology and Biochemistry, Vol. 41, Issue 1
  • DOI: 10.1016/j.soilbio.2008.10.008

Experimental factors affecting PCR-based estimates of microbial species richness and evenness
journal, January 2010

  • Engelbrektson, Anna; Kunin, Victor; Wrighton, Kelly C.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.153

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


Plant rhizospheric N processes: what we don't know and why we should care
journal, June 2009

  • Frank, Douglas A.; Groffman, Peter M.
  • Ecology, Vol. 90, Issue 6
  • DOI: 10.1890/08-0789.1

Rhizosphere microbial community and its response to plant species and soil history
journal, December 2007


MICROBIAL DIVERSITY IN SOIL: Selection of Microbial Populations by Plant and Soil Type and Implications for Disease Suppressiveness
journal, September 2004


Sustainable bioenergy production from marginal lands in the US Midwest
journal, January 2013

  • Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong
  • Nature, Vol. 493, Issue 7433
  • DOI: 10.1038/nature11811

Agroecology: the key role of arbuscular mycorrhizas in ecosystem services
journal, August 2010


Global patterns of root turnover for terrestrial ecosystems: RESEARCH Root turnover in terrestrial ecosystems
journal, July 2000


Determination of monosaccharides as aldononitrile, O-methyloxime, alditol, and cyclitol acetate derivatives by gas chromatography
journal, April 1984

  • Guerrant, Gordon O.; Moss, C. Wayne.
  • Analytical Chemistry, Vol. 56, Issue 4
  • DOI: 10.1021/ac00268a010

Bacterial and Fungal Cell-Wall Residues in Conventional and No-Tillage Agroecosystems
journal, January 1999

  • Guggenberger, Georg; Frey, Serita D.; Six, Johan
  • Soil Science Society of America Journal, Vol. 63, Issue 5
  • DOI: 10.2136/sssaj1999.6351188x

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


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


Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties
journal, October 2011


Ergosterol and microbial biomass in the rhizosphere of grassland soils
journal, May 2000


Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture
journal, April 2004


Elevated CO2 differentially alters belowground plant and soil microbial community structure in reed canary grass-invaded experimental wetlands
journal, February 2007


Methods of studying soil microbial diversity
journal, August 2004

  • Kirk, Jennifer L.; Beaudette, Lee A.; Hart, Miranda
  • Journal of Microbiological Methods, Vol. 58, Issue 2
  • DOI: 10.1016/j.mimet.2004.04.006

rRNA Operon Copy Number Reflects Ecological Strategies of Bacteria
journal, April 2000


Filamentous Fungi: the Indeterminate Lifestyle and Microbial Ecology
journal, March 2004


Long-term plant growth legacies overwhelm short-term plant growth effects on soil microbial community structure
journal, April 2011


Review: Factors affecting rhizosphere priming effects
journal, August 2002


Microbial seed banks: the ecological and evolutionary implications of dormancy
journal, January 2011

  • Lennon, Jay T.; Jones, Stuart E.
  • Nature Reviews Microbiology, Vol. 9, Issue 2
  • DOI: 10.1038/nrmicro2504

Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy
journal, November 2010


Soil microbial residue storage linked to soil legacy under biofuel cropping systems in southern Wisconsin, USA
journal, February 2013


Microbial lipid and amino sugar responses to long-term simulated global environmental changes in a California annual grassland
journal, May 2015

  • Liang, Chao; Gutknecht, Jessica L. M.; Balser, Teri C.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00385

Soil microbial communities under model biofuel cropping systems in southern Wisconsin, USA: Impact of crop species and soil properties
journal, March 2012


Diversity and heritability of the maize rhizosphere microbiome under field conditions
journal, April 2013

  • Peiffer, J. A.; Spor, A.; Koren, O.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
  • DOI: 10.1073/pnas.1302837110

Going back to the roots: the microbial ecology of the rhizosphere
journal, September 2013

  • Philippot, Laurent; Raaijmakers, Jos M.; Lemanceau, Philippe
  • Nature Reviews Microbiology, Vol. 11, Issue 11
  • DOI: 10.1038/nrmicro3109

Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil
journal, January 2001


Spatial structure in soil chemical and microbiological properties in an upland grassland
journal, August 2004


Microbially Derived Inputs to Soil Organic Matter: Are Current Estimates Too Low?
journal, December 2007

  • Simpson, André J.; Simpson, Myrna J.; Smith, Emma
  • Environmental Science & Technology, Vol. 41, Issue 23
  • DOI: 10.1021/es071217x

Influence of grass species and soil type on rhizosphere microbial community structure in grassland soils
journal, June 2007


Bulk and Rhizosphere Soil Bacterial Communities Studied by Denaturing Gradient Gel Electrophoresis: Plant-Dependent Enrichment and Seasonal Shifts Revealed
journal, October 2001


Azospirillum , a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects
journal, October 2000


Soil microbial community composition and land use history in cultivated and grassland ecosystems of coastal California
journal, November 2002

  • Steenwerth, Kerri L.; Jackson, Louise E.; Calderón, Francisco J.
  • Soil Biology and Biochemistry, Vol. 34, Issue 11
  • DOI: 10.1016/S0038-0717(02)00144-X

Shifts in the microbial community in rhizosphere and non-rhizosphere soils during the growth of Agrostis stolonifera
journal, June 2000


Xander: employing a novel method for efficient gene-targeted metagenomic assembly
journal, August 2015


Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes
journal, January 2014

  • Werling, B. P.; Dickson, T. L.; Isaacs, R.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 4
  • DOI: 10.1073/pnas.1309492111

Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils
journal, September 1996