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

Abstract

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, andmore » 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.« less

Authors:
 [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
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States); Northern Arizona Univ., Flagstaff, AZ (United States)
Sponsoring Org.:
USDOE Office of Science (SC); USDA: National Institute of Food and Agriculture (NIFA)
OSTI Identifier:
1628295
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 10; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Plant sciences; soil microbiome; switchgrass; rhizobacteria; arbuscular mycorrhizal fungi; resource availability; plant–microbial interaction

Citation Formats

Revillini, Daniel, Wilson, Gail W. T., Miller, R. Michael, Lancione, Ryan, and Johnson, Nancy Collins. Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks. United States: N. p., 2019. Web. doi:10.3389/fpls.2019.01018.
Revillini, Daniel, Wilson, Gail W. T., Miller, R. Michael, Lancione, Ryan, & Johnson, Nancy Collins. Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks. United States. https://doi.org/10.3389/fpls.2019.01018
Revillini, Daniel, Wilson, Gail W. T., Miller, R. Michael, Lancione, Ryan, and Johnson, Nancy Collins. Wed . "Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks". United States. https://doi.org/10.3389/fpls.2019.01018. https://www.osti.gov/servlets/purl/1628295.
@article{osti_1628295,
title = {Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks},
author = {Revillini, Daniel and Wilson, Gail W. T. and Miller, R. Michael and Lancione, Ryan and Johnson, Nancy Collins},
abstractNote = {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.},
doi = {10.3389/fpls.2019.01018},
journal = {Frontiers in Plant Science},
number = ,
volume = 10,
place = {United States},
year = {Wed Aug 14 00:00:00 EDT 2019},
month = {Wed Aug 14 00:00:00 EDT 2019}
}

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Verrucomicrobial elevational distribution was strongly influenced by soil pH and carbon/nitrogen ratio
journal, March 2017


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

  • Oates, Lawrence G.; Duncan, David S.; Sanford, Gregg R.
  • Agriculture, Ecosystems & Environment, Vol. 233
  • DOI: 10.1016/j.agee.2016.09.008

Switchgrass selection as a “model” bioenergy crop: A history of the process
journal, June 2010


Plant community composition influences fine root production and biomass allocation in perennial bioenergy cropping systems of the upper Midwest, USA
journal, October 2017


The Soil-Borne Legacy
journal, March 2018


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


Molecular breeding of switchgrass for use as a biofuel crop
journal, December 2007


Effects of switchgrass cultivars and intraspecific differences in root structure on soil carbon inputs and accumulation
journal, January 2016


Use of specific phospholipid fatty acids for identifying and quantifying the external hyphae of the arbuscular mycorrhizal fungus Gigaspora rosea
journal, November 2004


Fungal/bacterial ratios in grasslands with contrasting nitrogen management
journal, August 2006


Use and misuse of PLFA measurements in soils
journal, August 2011


The under-recognized dominance of Verrucomicrobia in soil bacterial communities
journal, July 2011


Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems
journal, August 2014


Effects of 44 years of chronic nitrogen fertilization on the soil nitrifying community of permanent grassland
journal, December 2015


N addition undermines N supplied by arbuscular mycorrhizal fungi to native perennial grasses
journal, January 2018


An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability
journal, June 2016

  • Bender, S. Franz; Wagg, Cameron; van der Heijden, Marcel G. A.
  • Trends in Ecology & Evolution, Vol. 31, Issue 6
  • DOI: 10.1016/j.tree.2016.02.016

The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil
journal, May 1995


Examining the global distribution of dominant archaeal populations in soil
journal, November 2010

  • Bates, Scott T.; Berg-Lyons, Donna; Caporaso, J. Gregory
  • The ISME Journal, Vol. 5, Issue 5
  • DOI: 10.1038/ismej.2010.171

Phylogenetic conservatism of functional traits in microorganisms
journal, December 2012

  • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.160

A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment
journal, July 2015

  • van der Heijden, Marcel GA; Bruin, Susanne de; Luckerhoff, Ludo
  • The ISME Journal, Vol. 10, Issue 2
  • DOI: 10.1038/ismej.2015.120

Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture
journal, June 2017

  • Hannula, S. Emilia; Morriën, Elly; de Hollander, Mattias
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