skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks

Journal Article · · Frontiers in Plant Science
 [1];  [2];  [3];  [4];  [5]
  1. Northern Arizona Univ., Flagstaff, AZ (United States). Dept. of Biological Sciences; Univ. of Miami, FL (United States). Dept. of Biology
  2. Oklahoma State Univ., Stillwater, OK (United States). Dept. of Natural Resource Ecology, Management
  3. Argonne National Lab. (ANL), Argonne, IL (United States). Environmental Science Division
  4. Northern Arizona Univ., Flagstaff, AZ (United States). Dept. of Biological Sciences
  5. Northern Arizona Univ., Flagstaff, AZ (United States). Dept. of Biological Sciences and School of Earth, Sustainability

Plants may actively cultivate microorganisms in their roots and rhizosphere that enhance their nutrition. To develop cropping strategies that substitute mineral fertilizers for beneficial root symbioses, we must first understand how microbial communities associated with plant roots differ among plant taxa and how they respond to fertilization. Arbuscular mycorrhizal (AM) fungi and rhizobacteria are of particular interest because they enhance nutrient availability to plants and perform a suite of nutrient cycling functions. The purpose of this experiment is to examine the root and soil microbiome in a longterm switchgrass (Panicum virgatum) biofuel feedstock experiment and determine how AM fungi and rhizobacteria respond to plant diversity and soil fertility. We hypothesize that intra- and interspecific plant diversity, nitrogen fertilization (+N), and their interaction will influence the biomass and community composition of AM fungi and rhizobacteria. We further hypothesize that +N will reduce the abundance of nitrogenase-encoding nifH genes on the rhizoplane. Roots and soils were sampled from three switchgrass cultivars (Cave-in-Rock, Kanlow, Southlow) grown in monoculture, intraspecific mixture, and interspecific planting mixtures with either Andropogon gerardii or diverse native tallgrass prairie species. Molecular sequencing was performed on root and soil samples, fatty acid extractions were assessed to determine microbial biomass, and quantitative polymerase chain reaction (qPCR) was performed on nifH genes from the rhizoplane. Sequence data determined core AM fungal and bacterial microbiomes and indicator taxa for plant diversity and +N treatments. We found that plant diversity and +N influenced AM fungal biomass and community structure. Across all plant diversity treatments, +N reduced the biomass of AM fungi and nifH gene abundance by more than 40%. The AM fungal genus Scutellospora was an indicator for +N, with relative abundance significantly greater under +N and in monoculture treatments. Community composition of rhizobacteria was influenced by plant diversity but not by +N. Verrucomicrobia and Proteobacteria were the dominant bacterial phyla in both roots and soils. Our findings provide evidence that soil fertility and plant diversity structure the root and soil microbiome. Optimization of soil communities for switchgrass production must take into account differences among cultivars and their unique responses to shifts in soil fertility.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States); Northern Arizona Univ., Flagstaff, AZ (United States)
Sponsoring Organization:
USDOE Office of Science (SC); USDA: National Institute of Food and Agriculture (NIFA)
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1628295
Journal Information:
Frontiers in Plant Science, Vol. 10; ISSN 1664-462X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 16 works
Citation information provided by
Web of Science

References (121)

Plant Growth-Promoting Rhizobacteria Allow Reduced Application Rates of Chemical Fertilizers journal May 2009
Effects of switchgrass cultivars and intraspecific differences in root structure on soil carbon inputs and accumulation journal January 2016
Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation journal January 2016
Microbial Phosphorus Solubilization and Its Potential for Use in Sustainable Agriculture journal June 2017
A new method for non-parametric multivariate analysis of variance journal February 2001
Nutrient cycling in the mycorrhizosphere journal January 2015
Regulation and function of root exudates journal June 2009
Diversity of Nitrogen-Fixing Bacteria Associated with Switchgrass in the Native Tallgrass Prairie of Northern Oklahoma journal July 2014
The Soil-Borne Legacy journal March 2018
Belowground biodiversity and ecosystem functioning journal November 2014
Examining the global distribution of dominant archaeal populations in soil journal November 2010
Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities journal June 2012
An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability journal June 2016
Unraveling the plant microbiome: looking back and future perspectives journal June 2014
The under-recognized dominance of Verrucomicrobia in soil bacterial communities journal July 2011
Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts journal January 2015
Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism journal January 2009
Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing journal December 2012
Molecular breeding of switchgrass for use as a biofuel crop journal December 2007
Evaluation of Switchgrass Rhizosphere Microflora for Enhancing Seedling Yield and Nutrient Uptake journal March 1907
Microbial immobilization of ammonium and nitrate in relation to ammonification and nitrification rates in organic and conventional cropping systems journal January 2003
Research priorities for harnessing plant microbiomes in sustainable agriculture journal March 2017
PyNAST: a flexible tool for aligning sequences to a template alignment journal November 2009
QIIME allows analysis of high-throughput community sequencing data journal April 2010
Evidence that soil nutrient stoichiometry controls the competitive abilities of arbuscular mycorrhizal vs. root-borne non-mycorrhizal fungi journal December 2013
Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro-ecosystems across the globe journal April 2018
Associations between species and groups of sites: indices and statistical inference journal December 2009
Improving indicator species analysis by combining groups of sites journal September 2010
Fungal/bacterial ratios in grasslands with contrasting nitrogen management journal August 2006
Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing journal February 2011
Mycorrhizal Community Dynamics Following Nitrogen Fertilization: a Cross-Site test in five Grasslands journal November 2007
Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States journal October 2013
Global patterns in belowground communities journal November 2009
The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil journal April 1996
Use and misuse of PLFA measurements in soils journal August 2011
A Comprehensive Evaluation of PCR Primers to Amplify the nifH Gene of Nitrogenase journal July 2012
Current understanding of the human microbiome journal April 2018
The Earth Microbiome project: successes and aspirations journal August 2014
Identifying the Active Microbiome Associated with Roots and Rhizosphere Soil of Oilseed Rape journal September 2017
Nitrogen transfer in the arbuscular mycorrhizal symbiosis journal June 2005
Multiple Climate Change Factors Interact to Alter Soil Microbial Community Structure in an Old-Field Ecosystem journal January 2011
Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture journal June 2017
Microbe management: application of mycorrhyzal fungi in sustainable agriculture journal December 2005
Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems journal June 2014
A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi journal March 2010
The economic value of grassland species for carbon storage journal April 2017
N addition undermines N supplied by arbuscular mycorrhizal fungi to native perennial grasses journal January 2018
Plant preferential allocation and fungal reward decline with soil phosphorus: implications for mycorrhizal mutualism journal May 2016
Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture journal April 2004
Can Fertilization of Soil Select Less Mutualistic Mycorrhizae? journal November 1993
Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales: Tansley review journal December 2009
Nitrogen Enrichment Alters Mycorrhizal Allocation at five Mesic to Semiarid Grasslands journal July 2003
Resource limitation is a driver of local adaptation in mycorrhizal symbioses journal January 2010
Mycorrhizal phenotypes and the Law of the Minimum journal November 2014
Interactions among mycorrhizae, atmospheric CO2 and soil N impact plant community composition journal June 2003
Mycorrhizae: Possible Explanation for Yield Decline with Continuous Corn and Soybean journal January 1992
Sanctions, Cooperation, and the Stability of Plant-Rhizosphere Mutualisms journal December 2008
Host sanctions and the legume–rhizobium mutualism journal September 2003
Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis journal August 2011
Community-level plant-soil feedbacks explain landscape distribution of native and non-native plants journal January 2018
The interactive effects of plant microbial symbionts: a review and meta-analysis journal September 2010
Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi: PCR primers for arbuscular mycorrhizal fungi journal August 2008
Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems journal August 2014
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities journal December 2005
Plant-Growth-Promoting Rhizobacteria journal October 2009
Swarm: robust and fast clustering method for amplicon-based studies journal January 2014
Native Perennial Grassland Species for Bioenergy: Establishment and Biomass Productivity journal January 2011
Enrichment of specific bacterial and eukaryotic microbes in the rhizosphere of switchgrass ( P anicum virgatum  L.) through root exudates : Root exudate-utilizing microbes in switchgrass rhizosphere journal March 2014
Phylogenetic conservatism of functional traits in microorganisms journal December 2012
Microbiomes in light of traits: A phylogenetic perspective journal November 2015
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea journal December 2011
Mehlich 3 soil test extractant: A modification of Mehlich 2 extractant journal December 1984
Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes journal October 2015
Genotypic diversity effects on biomass production in native perennial bioenergy cropping systems journal January 2016
The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling journal November 2008
Bioenergy cropping systems that incorporate native grasses stimulate growth of plant-associated soil microbes in the absence of nitrogen fertilization journal October 2016
The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota) journal June 2010
The Biology and Agronomy of Switchgrass for Biofuels journal September 2005
Differential abundance analysis for microbial marker-gene surveys journal September 2013
US Billion Ton Update: Biomass supply for a bioenergy and bioproducts industry (executive summary) journal October 2011
The ecological coherence of high bacterial taxonomic ranks journal June 2010
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix journal April 2009
Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide journal November 2014
Plant-fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply journal May 2016
Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes journal February 2012
Functional Ecology of Free-Living Nitrogen Fixation: A Contemporary Perspective journal December 2011
The role of locally adapted mycorrhizas and rhizobacteria in plant-soil feedback systems journal April 2016
Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture journal May 2005
Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis journal March 2017
Use of specific phospholipid fatty acids for identifying and quantifying the external hyphae of the arbuscular mycorrhizal fungus Gigaspora rosea journal November 2004
The Plant Microbiome at Work journal March 2015
Fungal diversity regulates plant-soil feedbacks in temperate grassland journal November 2018
Comparison of biochemical and microscopic methods for quantification of arbuscular mycorrhizal fungi in soil and roots journal November 2015
Verrucomicrobial elevational distribution was strongly influenced by soil pH and carbon/nitrogen ratio journal March 2017
Plant compartment and genetic variation drive microbiome composition in switchgrass roots journal January 2019
Plant community composition influences fine root production and biomass allocation in perennial bioenergy cropping systems of the upper Midwest, USA journal October 2017
Considering fungal:bacterial dominance in soils – Methods, controls, and ecosystem implications journal September 2010
Carbon-Negative Biofuels from Low-Input High-Diversity Grassland Biomass journal December 2006
Core microbiomes for sustainable agroecosystems journal April 2018
Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling: Role of mesophilic crenarchaeota in nitrogen cycling journal September 2005
The Phyllosphere: Microbial Jungle at the Plant–Climate Interface journal November 2016
A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment journal July 2015
Plant-soil feedbacks: the past, the present and future challenges journal February 2013
The importance of the microbiome of the plant holobiont journal February 2015
Mycorrhizal fungi associated with high soil N:P ratios are more likely to be lost upon conversion from grasslands to arable agriculture journal July 2015
The influence of biotic interactions on soil biodiversity journal July 2006
Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems journal October 2013
Aboveground productivity and root–shoot allocation differ between native and introduced grass species journal August 2006
Switchgrass selection as a “model” bioenergy crop: A history of the process journal June 2010
Sustainable intensification of high-diversity biomass production for optimal biofuel benefits journal November 2018
Nitrogenase gene diversity and microbial community structure: a cross-system comparison journal July 2003
Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist journal September 2014
Effects of 44 years of chronic nitrogen fertilization on the soil nitrifying community of permanent grassland journal December 2015
Compositional and Functional Shifts in Microbial Communities Due to Soil Warming journal January 1997
Climate, but not trait, effects on plant-soil feedback depend on mycorrhizal type in temperate forests journal March 2018
Seasonal and diurnal soil respiration dynamics under different land management practices in the sub-tropical highland agroecology of Ethiopia journal November 2022
The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil journal May 1995
Microbiota-accessible carbohydrates suppress Clostridium difficile infection in a murine model journal April 2018
Infant gut microbiota characteristics generally do not modify effects of lipid-based nutrient supplementation on growth or inflammation: secondary analysis of a randomized controlled trial in Malawi journal September 2020
Stoichiometric N:P flexibility and mycorrhizal symbiosis favour plant resistance against drought journal February 2017
Core microbiomes for sustainable agroecosystems text January 2018