Fungal-Bacterial Networks in the Populus Rhizobiome Are Impacted by Soil Properties and Host Genotype
Abstract
Plant root-associated microbial symbionts comprise the plant rhizobiome. These microbes function in provisioning nutrients and water to their hosts, impacting plant health and disease. The plant microbiome is shaped by plant species, plant genotype, soil and environmental conditions, but the contributions of these variables are hard to disentangle from each other in natural systems. We used bioassay common garden experiments to decouple plant genotype and soil property impacts on fungal and bacterial community structure in the Populus rhizobiome. High throughput amplification and sequencing of 16S, ITS, 28S and 18S rDNA was accomplished through 454 pyrosequencing. Co-association patterns of fungal and bacterial taxa were assessed with 16S and ITS datasets. Community bipartite fungal-bacterial networks and PERMANOVA results attribute significant difference in fungal or bacterial communities to soil origin, soil chemical properties and plant genotype. Indicator species analysis identified a common set of root bacteria as well as endophytic and ectomycorrhizal fungi associated with Populus in different soils. However, no single taxon, or consortium of microbes, was indicative of a particular Populus genotype. Fungal-bacterial networks were over-represented in arbuscular mycorrhizal, endophytic, and ectomycorrhizal fungi, as well as bacteria belonging to the orders Rhizobiales, Chitinophagales, Cytophagales, and Burkholderiales. These results demonstrate the importancemore »
- Authors:
-
- Michigan State Univ., East Lansing, MI (United States); Great Lakes Bioenergy Research Center, East Lansing, MI (United States)
- Duke Univ., Durham, NC (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
- Univ. of Florida, Quincy, FL (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1505327
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 3; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Populus deltoides; fungal communities; bacterial communities; microbiome; NGS sequencing; arbuscular mycorrhizal fungi; endophytes; rhizosphere
Citation Formats
Bonito, Gregory, Benucci, Gian Maria Niccolò, Hameed, Khalid, Weighill, Deborah A., Jones, Piet C., Chen, Ko -Hsuan, Jacobson, Daniel A., Schadt, Christopher Warren, and Vilgalys, Rytas. Fungal-Bacterial Networks in the Populus Rhizobiome Are Impacted by Soil Properties and Host Genotype. United States: N. p., 2019.
Web. doi:10.3389/fmicb.2019.00481.
Bonito, Gregory, Benucci, Gian Maria Niccolò, Hameed, Khalid, Weighill, Deborah A., Jones, Piet C., Chen, Ko -Hsuan, Jacobson, Daniel A., Schadt, Christopher Warren, & Vilgalys, Rytas. Fungal-Bacterial Networks in the Populus Rhizobiome Are Impacted by Soil Properties and Host Genotype. United States. https://doi.org/10.3389/fmicb.2019.00481
Bonito, Gregory, Benucci, Gian Maria Niccolò, Hameed, Khalid, Weighill, Deborah A., Jones, Piet C., Chen, Ko -Hsuan, Jacobson, Daniel A., Schadt, Christopher Warren, and Vilgalys, Rytas. Fri .
"Fungal-Bacterial Networks in the Populus Rhizobiome Are Impacted by Soil Properties and Host Genotype". United States. https://doi.org/10.3389/fmicb.2019.00481. https://www.osti.gov/servlets/purl/1505327.
@article{osti_1505327,
title = {Fungal-Bacterial Networks in the Populus Rhizobiome Are Impacted by Soil Properties and Host Genotype},
author = {Bonito, Gregory and Benucci, Gian Maria Niccolò and Hameed, Khalid and Weighill, Deborah A. and Jones, Piet C. and Chen, Ko -Hsuan and Jacobson, Daniel A. and Schadt, Christopher Warren and Vilgalys, Rytas},
abstractNote = {Plant root-associated microbial symbionts comprise the plant rhizobiome. These microbes function in provisioning nutrients and water to their hosts, impacting plant health and disease. The plant microbiome is shaped by plant species, plant genotype, soil and environmental conditions, but the contributions of these variables are hard to disentangle from each other in natural systems. We used bioassay common garden experiments to decouple plant genotype and soil property impacts on fungal and bacterial community structure in the Populus rhizobiome. High throughput amplification and sequencing of 16S, ITS, 28S and 18S rDNA was accomplished through 454 pyrosequencing. Co-association patterns of fungal and bacterial taxa were assessed with 16S and ITS datasets. Community bipartite fungal-bacterial networks and PERMANOVA results attribute significant difference in fungal or bacterial communities to soil origin, soil chemical properties and plant genotype. Indicator species analysis identified a common set of root bacteria as well as endophytic and ectomycorrhizal fungi associated with Populus in different soils. However, no single taxon, or consortium of microbes, was indicative of a particular Populus genotype. Fungal-bacterial networks were over-represented in arbuscular mycorrhizal, endophytic, and ectomycorrhizal fungi, as well as bacteria belonging to the orders Rhizobiales, Chitinophagales, Cytophagales, and Burkholderiales. These results demonstrate the importance of soil and plant genotype on fungal-bacterial networks in the belowground plant microbiome.},
doi = {10.3389/fmicb.2019.00481},
journal = {Frontiers in Microbiology},
number = 3,
volume = 10,
place = {United States},
year = {Fri Mar 29 00:00:00 EDT 2019},
month = {Fri Mar 29 00:00:00 EDT 2019}
}
Web of Science
Works referenced in this record:
Endo- and Ectomycorrhizal Associations in Five Populus Species
journal, July 1974
- Vozzo, J. A.; Hacskaylo, Edward
- Bulletin of the Torrey Botanical Club, Vol. 101, Issue 4
Similarity Indices in Community Studies: Potential Pitfalls
journal, January 1981
- Bloom, Sa
- Marine Ecology Progress Series, Vol. 5
3-way Networks: Application of Hypergraphs for Modelling Increased Complexity in Comparative Genomics
journal, March 2015
- Weighill, Deborah A.; Jacobson, Daniel A.
- PLOS Computational Biology, Vol. 11, Issue 3
Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types
journal, July 2011
- Gottel, Neil R.; Castro, Hector F.; Kerley, Marilyn
- Applied and Environmental Microbiology, Vol. 77, Issue 17
Clone history shapes Populus drought responses
journal, July 2011
- Raj, S.; Brautigam, K.; Hamanishi, E. T.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 30
Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011
- Martin, Marcel
- EMBnet.journal, Vol. 17, Issue 1
Analysis of Data From Viral DNA Microchips
journal, December 2001
- Amaratunga, Dhammika; Cabrera, Javier
- Journal of the American Statistical Association, Vol. 96, Issue 456
Network Analysis Reveals Ecological Links between N-Fixing Bacteria and Wood-Decaying Fungi
journal, February 2014
- Hoppe, Björn; Kahl, Tiemo; Karasch, Peter
- PLoS ONE, Vol. 9, Issue 2
Early rooting of dormant hardwood cuttings of Populus : analysis of quantitative genetics and genotype × environment interactions
journal, April 2005
- Zalesny, Jr., Ronald S.; Riemenschneider, Don E.; Hall, Richard B.
- Canadian Journal of Forest Research, Vol. 35, Issue 4
Influence of exogenous organic matter on prokaryotic and eukaryotic microbiota in an agricultural soil. A multidisciplinary approach
journal, March 2015
- Pezzolla, Daniela; Marconi, Gianpiero; Turchetti, Benedetta
- Soil Biology and Biochemistry, Vol. 82
Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome: Prokaryotic communities of the lichen microbiome
journal, September 2011
- Hodkinson, Brendan P.; Gottel, Neil R.; Schadt, Christopher W.
- Environmental Microbiology, Vol. 14, Issue 1
Assembly and ecological function of the root microbiome across angiosperm plant species
journal, January 2018
- Fitzpatrick, Connor R.; Copeland, Julia; Wang, Pauline W.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 6
Tree genetics defines fungal partner communities that may confer drought tolerance
journal, September 2017
- Gehring, Catherine A.; Sthultz, Christopher M.; Flores-Rentería, Lluvia
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 42
Fold change rank ordering statistics: a new method for detecting differentially expressed genes
journal, January 2014
- Dembélé, Doulaye; Kastner, Philippe
- BMC Bioinformatics, Vol. 15, Issue 1
A new method for non-parametric multivariate analysis of variance: NON-PARAMETRIC MANOVA FOR ECOLOGY
journal, February 2001
- Anderson, Marti J.
- Austral Ecology, Vol. 26, Issue 1
Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible
journal, April 2014
- McMurdie, Paul J.; Holmes, Susan
- PLoS Computational Biology, Vol. 10, Issue 4
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007
- Wang, Q.; Garrity, G. M.; Tiedje, J. M.
- Applied and Environmental Microbiology, Vol. 73, Issue 16
Ecologically meaningful transformations for ordination of species data
journal, October 2001
- Legendre, Pierre; Gallagher, Eugene D.
- Oecologia, Vol. 129, Issue 2
Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi: PCR primers for arbuscular mycorrhizal fungi
journal, August 2008
- Lee, Jaikoo; Lee, Sangsun; Young, J. Peter W.
- FEMS Microbiology Ecology, Vol. 65, Issue 2
Defining the core Arabidopsis thaliana root microbiome
journal, August 2012
- Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
- Nature, Vol. 488, Issue 7409
Metaxa: a software tool for automated detection and discrimination among ribosomal small subunit (12S/16S/18S) sequences of archaea, bacteria, eukaryotes, mitochondria, and chloroplasts in metagenomes and environmental sequencing datasets
journal, June 2011
- Bengtsson, Johan; Eriksson, K. Martin; Hartmann, Martin
- Antonie van Leeuwenhoek, Vol. 100, Issue 3
CoNet app: inference of biological association networks using Cytoscape
journal, January 2016
- Faust, Karoline; Raes, Jeroen
- F1000Research, Vol. 5
Graph Clustering Via a Discrete Uncoupling Process
journal, January 2008
- Van Dongen, Stijn
- SIAM Journal on Matrix Analysis and Applications, Vol. 30, Issue 1
A novel baiting microcosm approach used to identify the bacterial community associated with Penicillium bilaii hyphae in soil
journal, October 2017
- Ghodsalavi, Behnoushsadat; Svenningsen, Nanna Bygvraa; Hao, Xiuli
- PLOS ONE, Vol. 12, Issue 10
Isolating a functionally relevant guild of fungi from the root microbiome of Populus
journal, August 2016
- Bonito, Gregory; Hameed, Khalid; Ventura, Rafael
- Fungal Ecology, Vol. 22
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees
journal, October 2013
- Shakya, Migun; Gottel, Neil; Castro, Hector
- PLoS ONE, Vol. 8, Issue 10
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
Distance-Based Tests for Homogeneity of Multivariate Dispersions
journal, October 2005
- Anderson, Marti J.
- Biometrics, Vol. 62, Issue 1
UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013
- Edgar, Robert C.
- Nature Methods, Vol. 10, Issue 10
Removing Noise From Pyrosequenced Amplicons
journal, January 2011
- Quince, Christopher; Lanzen, Anders; Davenport, Russell J.
- BMC Bioinformatics, Vol. 12, Issue 1
Towards a unified paradigm for sequence-based identification of fungi
journal, September 2013
- Kõljalg, Urmas; Nilsson, R. Henrik; Abarenkov, Kessy
- Molecular Ecology, Vol. 22, Issue 21
Genetic architecture of qualitative and quantitative Melampsora larici-populina leaf rust resistance in hybrid poplar: genetic mapping and QTL detection
journal, April 2005
- Jorge, V.; Dowkiw, A.; Faivre-Rampant, P.
- New Phytologist, Vol. 167, Issue 1
Refining the stress-gradient hypothesis for competition and facilitation in plant communities
journal, March 2009
- Maestre, Fernando T.; Callaway, Ragan M.; Valladares, Fernando
- Journal of Ecology, Vol. 97, Issue 2
Computing topological parameters of biological networks
journal, November 2007
- Assenov, Yassen; Ramírez, Fidel; Schelhorn, Sven-Eric
- Bioinformatics, Vol. 24, Issue 2
Host Genotype Shapes the Foliar Fungal Microbiome of Balsam Poplar (Populus balsamifera)
journal, January 2013
- Bálint, Miklós; Tiffin, Peter; Hallström, Björn
- PLoS ONE, Vol. 8, Issue 1
Improving indicator species analysis by combining groups of sites
journal, September 2010
- De Cáceres, Miquel; Legendre, Pierre; Moretti, Marco
- Oikos, Vol. 119, Issue 10
Facultative root-colonizing fungi dominate endophytic assemblages in roots of nonmycorrhizal Microthlaspi species
journal, November 2017
- Glynou, Kyriaki; Nam, Bora; Thines, Marco
- New Phytologist, Vol. 217, Issue 3
Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level
journal, December 2011
- Krüger, Manuela; Krüger, Claudia; Walker, Christopher
- New Phytologist, Vol. 193, Issue 4
Fungal soil communities in a young transgenic poplar plantation form a rich reservoir for fungal root communities
journal, July 2012
- Danielsen, L.; Thürmer, A.; Meinicke, P.
- Ecology and Evolution, Vol. 2, Issue 8
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
Genetic variation for resistance to herbivores and plant pathogens: hypotheses, mechanisms and evolutionary implications
journal, September 2013
- Keith, R.; Mitchell-Olds, T.
- Plant Pathology, Vol. 62
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
The Cacti Microbiome: Interplay between Habitat-Filtering and Host-Specificity
journal, February 2016
- Fonseca-García, Citlali; Coleman-Derr, Devin; Garrido, Etzel
- Frontiers in Microbiology, Vol. 7
clusterMaker: a multi-algorithm clustering plugin for Cytoscape
journal, November 2011
- Morris, John H.; Apeltsin, Leonard; Newman, Aaron M.
- BMC Bioinformatics, Vol. 12, Issue 1
The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome
journal, February 2018
- Cregger, M. A.; Veach, A. M.; Yang, Z. K.
- Microbiome, Vol. 6, Issue 1
The responses of three riparian cottonwood species to water table decline
journal, October 1998
- Kranjcec, Julie; Mahoney, John M.; Rood, Stewart B.
- Forest Ecology and Management, Vol. 110, Issue 1-3
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data
journal, August 2009
- Hamady, Micah; Lozupone, Catherine; Knight, Rob
- The ISME Journal, Vol. 4, Issue 1
Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation
journal, January 2016
- Agler, Matthew T.; Ruhe, Jonas; Kroll, Samuel
- PLOS Biology, Vol. 14, Issue 1
Atractiella rhizophila , sp. nov., an endorrhizal fungus isolated from the Populus root microbiome
journal, January 2017
- Bonito, Gregory; Hameed, Khalid; Toome-Heller, Merje
- Mycologia, Vol. 109, Issue 1
The influence of soil moisture and flooding on formation of VA-endo- and ectomycorrhizae in Populus and Salix
journal, July 1989
- Lodge, D. J.
- Plant and Soil, Vol. 117, Issue 2
Propagation technique of arbuscular mycorrhizal fungi isolated from coastal reclamation land
journal, May 2016
- Selvakumar, Gopal; Krishnamoorthy, Ramasamy; Kim, Kiyoon
- European Journal of Soil Biology, Vol. 74
Evaluating the impacts of multiple generalist fungal pathogens on temperate tree seedling survival
journal, March 2012
- Hersh, Michelle H.; Vilgalys, Rytas; Clark, James S.
- Ecology, Vol. 93, Issue 3
Characterization of a novel, ubiquitous fungal endophyte from the rhizosphere and root endosphere of Populus trees
journal, June 2017
- Vélez, Jessica M.; Tschaplinski, Timothy J.; Vilgalys, Rytas
- Fungal Ecology, Vol. 27
Endemism and functional convergence across the North American soil mycobiome
journal, April 2014
- Talbot, J. M.; Bruns, T. D.; Taylor, J. W.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants
journal, June 2014
- Bonito, Gregory; Reynolds, Hannah; Robeson, Michael S.
- Molecular Ecology, Vol. 23, Issue 13
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
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
journal, January 1995
- Benjamini, Yoav; Hochberg, Yosef
- Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005
- Lozupone, C.; Knight, R.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
A new method for non-parametric multivariate analysis of variance
journal, February 2001
- Anderson, Marti J.
- Austral Ecology, Vol. 26, Issue 1
A sand fly salivary protein acts as a neutrophil chemoattractant
journal, May 2021
- Guimaraes-Costa, Anderson B.; Shannon, John P.; Waclawiak, Ingrid
- Nature Communications, Vol. 12, Issue 1
A new method for non-parametric multivariate analysis of variance
journal, February 2001
- Anderson, Marti J.
- Austral Ecology, Vol. 26, Issue 1
Aging features of the migratory locust at physiological and transcriptional levels
journal, April 2021
- Guo, Siyuan; Yang, Pengcheng; Liang, Bo
- BMC Genomics, Vol. 22, Issue 1
Succession of endophytic fungi and arbuscular mycorrhizal fungi associated with the growth of plant and their correlation with secondary metabolites in the roots of plants
journal, April 2021
- Dang, Hanli; Zhang, Tao; Wang, Zhongke
- BMC Plant Biology, Vol. 21, Issue 1
Defining the core Arabidopsis thaliana root microbiome
text, January 2012
- E., Ley, Ruth; Julien, Tremblay,; L., Dangl, Jeffery
- The University of North Carolina at Chapel Hill University Libraries
CoNet app: inference of biological association networks using Cytoscape
journal, January 2016
- Faust, Karoline; Raes, Jeroen
- F1000Research, Vol. 5
Diversity and heritability of the maize rhizosphere microbiome under field conditions
text, January 2013
- Z., Jin,; S., Buckler, E.; O., Koren,
- The University of North Carolina at Chapel Hill University Libraries
Waste Not, Want Not: Why Rarefying Microbiome Data is Inadmissible
text, January 2013
- McMurdie, Paul J.; Holmes, Susan
- arXiv
Works referencing / citing this record:
Prokaryotic taxa play keystone roles in the soil microbiome associated with woody perennial plants in the genus Buxus
journal, August 2019
- LeBlanc, Nicholas; Crouch, Jo Anne
- Ecology and Evolution, Vol. 9, Issue 19
Prokaryotic taxa play keystone roles in the soil microbiome associated with woody perennial plants in the genus Buxus
journal, August 2019
- LeBlanc, Nicholas; Crouch, Jo Anne
- Ecology and Evolution, Vol. 9, Issue 19
Evidence for Co-evolutionary History of Early Diverging Lycopodiaceae Plants With Fungi
journal, January 2020
- Benucci, Gian Maria Niccolò; Burnard, Delaney; Shepherd, Lara D.
- Frontiers in Microbiology, Vol. 10
The Bacterial Microbiome of Meloidogyne-Based Disease Complex in Coffee and Tomato
journal, February 2020
- Lamelas, Araceli; Desgarennes, Damaris; López-Lima, Daniel
- Frontiers in Plant Science, Vol. 11