DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi

Abstract

Abstract Extraradical hyphae (ERH) of arbuscular mycorrhizal fungi (AMF) extend from plant roots into the soil environment and interact with soil microbial communities. Evidence of positive and negative interactions between AMF and soil bacteria point to functionally important ERH-associated communities. To characterize communities associated with ERH and test controls on their establishment and composition, we utilized an in-growth core system containing a live soil–sand mixture that allowed manual extraction of ERH for 16S rRNA gene amplicon profiling. Across experiments and soils, consistent enrichment of members of the Betaproteobacteriales, Myxococcales, Fibrobacterales, Cytophagales, Chloroflexales, and Cellvibrionales was observed on ERH samples, while variation among samples from different soils was observed primarily at lower taxonomic ranks. The ERH-associated community was conserved between two fungal species assayed, Glomus versiforme and Rhizophagus irregularis, though R. irregularis exerted a stronger selection and showed greater enrichment for taxa in the Alphaproteobacteria and Gammaproteobacteria. A distinct community established within 14 days of hyphal access to the soil, while temporal patterns of establishment and turnover varied between taxonomic groups. Identification of a conserved ERH-associated community is consistent with the concept of an AMF microbiome and can aid the characterization of facilitative and antagonistic interactions influencing the plant-fungal symbiosis.

Authors:
ORCiD logo; ; ORCiD logo
Publication Date:
Research Org.:
Univ. of Nebraska, Lincoln, NE (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1768659
Alternate Identifier(s):
OSTI ID: 1775488
Grant/Contract Number:  
SC0014395
Resource Type:
Published Article
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Name: The ISME Journal Journal Volume: 15 Journal Issue: 8; Journal ID: ISSN 1751-7362
Publisher:
Oxford University Press
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiome; Symbiosis

Citation Formats

Emmett, Bryan D., Lévesque-Tremblay, Véronique, and Harrison, Maria J. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. United Kingdom: N. p., 2021. Web. doi:10.1038/s41396-021-00920-2.
Emmett, Bryan D., Lévesque-Tremblay, Véronique, & Harrison, Maria J. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. United Kingdom. https://doi.org/10.1038/s41396-021-00920-2
Emmett, Bryan D., Lévesque-Tremblay, Véronique, and Harrison, Maria J. Mon . "Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi". United Kingdom. https://doi.org/10.1038/s41396-021-00920-2.
@article{osti_1768659,
title = {Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi},
author = {Emmett, Bryan D. and Lévesque-Tremblay, Véronique and Harrison, Maria J.},
abstractNote = {Abstract Extraradical hyphae (ERH) of arbuscular mycorrhizal fungi (AMF) extend from plant roots into the soil environment and interact with soil microbial communities. Evidence of positive and negative interactions between AMF and soil bacteria point to functionally important ERH-associated communities. To characterize communities associated with ERH and test controls on their establishment and composition, we utilized an in-growth core system containing a live soil–sand mixture that allowed manual extraction of ERH for 16S rRNA gene amplicon profiling. Across experiments and soils, consistent enrichment of members of the Betaproteobacteriales, Myxococcales, Fibrobacterales, Cytophagales, Chloroflexales, and Cellvibrionales was observed on ERH samples, while variation among samples from different soils was observed primarily at lower taxonomic ranks. The ERH-associated community was conserved between two fungal species assayed, Glomus versiforme and Rhizophagus irregularis, though R. irregularis exerted a stronger selection and showed greater enrichment for taxa in the Alphaproteobacteria and Gammaproteobacteria. A distinct community established within 14 days of hyphal access to the soil, while temporal patterns of establishment and turnover varied between taxonomic groups. Identification of a conserved ERH-associated community is consistent with the concept of an AMF microbiome and can aid the characterization of facilitative and antagonistic interactions influencing the plant-fungal symbiosis.},
doi = {10.1038/s41396-021-00920-2},
journal = {The ISME Journal},
number = 8,
volume = 15,
place = {United Kingdom},
year = {Mon Mar 01 00:00:00 EST 2021},
month = {Mon Mar 01 00:00:00 EST 2021}
}

Works referenced in this record:

Growth of Chitinolytic Dune Soil β-SubclassProteobacteria in Response to Invading Fungal Hyphae
journal, August 2001

  • De Boer, Wietse; Klein Gunnewiek, Paulien J. A.; Kowalchuk, George A.
  • Applied and Environmental Microbiology, Vol. 67, Issue 8
  • DOI: 10.1128/AEM.67.8.3358-3362.2001

Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralisation
journal, May 2016


Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling
journal, July 2010

  • Hodge, A.; Fitter, A. H.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 31
  • DOI: 10.1073/pnas.1005874107

Plant Phylogeny and Life History Shape Rhizosphere Bacterial Microbiome of Summer Annuals in an Agricultural Field
journal, December 2017

  • Emmett, Bryan D.; Youngblut, Nicholas D.; Buckley, Daniel H.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02414

The genome of Rhizophagus clarus HR1 reveals a common genetic basis for auxotrophy among arbuscular mycorrhizal fungi
journal, June 2018


Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species
journal, January 2006


Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018


Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota
journal, January 2018

  • Svenningsen, Nanna B.; Watts-Williams, Stephanie J.; Joner, Erik J.
  • The ISME Journal, Vol. 12, Issue 5
  • DOI: 10.1038/s41396-018-0059-3

Evolution of Mammals and Their Gut Microbes
journal, June 2008


'Candidatus Glomeribacter gigasporarum' gen. nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi
journal, January 2003

  • Bianciotto, V.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 1
  • DOI: 10.1099/ijs.0.02382-0

At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margarita provides insights into plant, endobacterial and fungal interactions
journal, October 2019

  • Venice, Francesco; Ghignone, Stefano; Salvioli di Fossalunga, Alessandra
  • Environmental Microbiology, Vol. 22, Issue 1
  • DOI: 10.1111/1462-2920.14827

The mycorrhiza helper bacteria revisited
journal, October 2007


Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible
journal, April 2014


Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale
journal, June 2009

  • Lauber, C. L.; Hamady, M.; Knight, R.
  • Applied and Environmental Microbiology, Vol. 75, Issue 15
  • DOI: 10.1128/AEM.00335-09

Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives
journal, December 2013

  • Schlaeppi, K.; Dombrowski, N.; Oter, R. G.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 2
  • DOI: 10.1073/pnas.1321597111

Phylogenetic distribution and evolution of mycorrhizas in land plants
journal, May 2006


Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition
journal, January 2012


UniFrac: an effective distance metric for microbial community comparison
journal, September 2010

  • Lozupone, Catherine; Lladser, Manuel E.; Knights, Dan
  • The ISME Journal, Vol. 5, Issue 2
  • DOI: 10.1038/ismej.2010.133

Response of soil microbial communities to compost amendments
journal, March 2006

  • Pérez-Piqueres, Ana; Edel-Hermann, Véronique; Alabouvette, Claude
  • Soil Biology and Biochemistry, Vol. 38, Issue 3
  • DOI: 10.1016/j.soilbio.2005.05.025

Defining the core Arabidopsis thaliana root microbiome
journal, August 2012

  • Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11237

Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates
journal, January 2015

  • Agnolucci, Monica; Battini, Fabio; Cristani, Caterina
  • Biology and Fertility of Soils, Vol. 51, Issue 3
  • DOI: 10.1007/s00374-014-0989-5

Interactions Between Myxobacteria, Plant Pathogenic Fungi, and Biocontrol Agents
journal, August 2002


Phosphatase activity in the rhizosphere and hyphosphere of VA mycorrhizal wheat supplied with inorganic and organic phosphorus
journal, March 1994


A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1
journal, April 2017


A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life
journal, August 2018

  • Parks, Donovan H.; Chuvochina, Maria; Waite, David W.
  • Nature Biotechnology, Vol. 36, Issue 10
  • DOI: 10.1038/nbt.4229

Mycorrhizas and soil structure
journal, July 2006


Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi
journal, September 2013

  • Desirò, Alessandro; Salvioli, Alessandra; Ngonkeu, Eddy L.
  • The ISME Journal, Vol. 8, Issue 2
  • DOI: 10.1038/ismej.2013.151

Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial: Soil microbial communities in arable fields
journal, August 2008


Bacterial predation: 75 years and counting!: Bacterial predation
journal, January 2016

  • Pérez, Juana; Moraleda-Muñoz, Aurelio; Marcos-Torres, Francisco Javier
  • Environmental Microbiology, Vol. 18, Issue 3
  • DOI: 10.1111/1462-2920.13171

Bacterial biofilm formation on the hyphae of ectomycorrhizal fungi: a widespread ability under controls?
journal, May 2018

  • Miquel Guennoc, Cora; Rose, Christophe; Labbé, Jessy
  • FEMS Microbiology Ecology, Vol. 94, Issue 7
  • DOI: 10.1093/femsec/fiy093

Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants
journal, June 2020

  • Wang, Shuangshuang; Chen, Aiqun; Xie, Kun
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 28
  • DOI: 10.1073/pnas.2000926117

Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils
journal, February 2019

  • Cruz-Paredes, Carla; Svenningsen, Nanna Bygvraa; Nybroe, Ole
  • FEMS Microbiology Ecology, Vol. 95, Issue 3
  • DOI: 10.1093/femsec/fiz020

Collimonas fungivorans gen. nov., sp. nov., a chitinolytic soil bacterium with the ability to grow on living fungal hyphae
journal, May 2004

  • de Boer, W.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 3
  • DOI: 10.1099/ijs.0.02920-0

phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013


Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
journal, August 2015


Niche differentiation is spatially and temporally regulated in the rhizosphere
journal, January 2020


Phosphorus Uptake by Plants: From Soil to Cell
journal, February 1998

  • Schachtman, Daniel P.; Reid, Robert J.; Ayling, S. M.
  • Plant Physiology, Vol. 116, Issue 2
  • DOI: 10.1104/pp.116.2.447

Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis
journal, November 2013

  • Tisserant, E.; Malbreil, M.; Kuo, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
  • DOI: 10.1073/pnas.1313452110

Soil bacterial and fungal communities across a pH gradient in an arable soil
journal, May 2010

  • Rousk, Johannes; Bååth, Erland; Brookes, Philip C.
  • The ISME Journal, Vol. 4, Issue 10
  • DOI: 10.1038/ismej.2010.58

Rapid Turnover of Hyphae of Mycorrhizal Fungi Determined by AMS Microanalysis of 14C
journal, May 2003


Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina
journal, February 2019

  • Morin, Emmanuelle; Miyauchi, Shingo; San Clemente, Hélène
  • New Phytologist, Vol. 222, Issue 3
  • DOI: 10.1111/nph.15687

Phosphate Uptake from Phytate Due to Hyphae-Mediated Phytase Activity by Arbuscular Mycorrhizal Maize
journal, April 2017


Why farmers should manage the arbuscular mycorrhizal symbiosis
journal, January 2019

  • Rillig, Matthias C.; Aguilar‐Trigueros, Carlos A.; Camenzind, Tessa
  • New Phytologist, Vol. 222, Issue 3
  • DOI: 10.1111/nph.15602

Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure: Effects of AM mycelial exudates on soil bacteria
journal, August 2007


Phylogeny of arbuscular mycorrhizal fungi predicts community composition of symbiosis-associated bacteria: AMF-associated bacterial communities
journal, September 2006


Distribution and population structure of endobacteria in arbuscular mycorrhizal fungi at North Atlantic dunes
journal, August 2018


Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley
journal, March 2015

  • Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C.
  • Cell Host & Microbe, Vol. 17, Issue 3
  • DOI: 10.1016/j.chom.2015.01.011

Cellular interactions between arbuscular mycorrhizal fungi and rhizosphere bacteria
journal, March 1996

  • Bianciotto, V.; Minerdi, D.; Perotto, S.
  • Protoplasma, Vol. 193, Issue 1-4
  • DOI: 10.1007/BF01276640

In situ stable isotope probing of phosphate-solubilizing bacteria in the hyphosphere
journal, January 2016

  • Wang, Fei; Shi, Ning; Jiang, Rongfeng
  • Journal of Experimental Botany, Vol. 67, Issue 6
  • DOI: 10.1093/jxb/erv561

DADA2: High-resolution sample inference from Illumina amplicon data
journal, May 2016

  • Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J.
  • Nature Methods, Vol. 13, Issue 7
  • DOI: 10.1038/nmeth.3869

Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus
journal, January 2014


Trapping of phosphate solubilizing bacteria on hyphae of the arbuscular mycorrhizal fungus Rhizophagus irregularis DAOM 197198
journal, November 2015


Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme ) and its bacterial endosymbionts
journal, October 2018

  • Sun, Xuepeng; Chen, Wenbo; Ivanov, Sergey
  • New Phytologist, Vol. 221, Issue 3
  • DOI: 10.1111/nph.15472

Evolutionary history of mycorrhizal symbioses and global host plant diversity
journal, January 2018

  • Brundrett, Mark C.; Tedersoo, Leho
  • New Phytologist, Vol. 220, Issue 4
  • DOI: 10.1111/nph.14976

Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation
journal, November 2014

  • Kaiser, Christina; Kilburn, Matt R.; Clode, Peta L.
  • New Phytologist, Vol. 205, Issue 4
  • DOI: 10.1111/nph.13138

Identification of Bacterial Groups Preferentially Associated with Mycorrhizal Roots of Medicago truncatula
journal, December 2006

  • Offre, P.; Pivato, B.; Siblot, S.
  • Applied and Environmental Microbiology, Vol. 73, Issue 3
  • DOI: 10.1128/AEM.02042-06

Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi
journal, February 2010

  • Scheublin, Tanja R.; Sanders, Ian R.; Keel, Christoph
  • The ISME Journal, Vol. 4, Issue 6
  • DOI: 10.1038/ismej.2010.5

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

Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota
journal, April 2017


The Myxobacteria
book, January 2006

  • Shimkets, Lawrence J.; Dworkin, Martin; Reichenbach, Hans
  • The Prokaryotes, p. 31-115
  • DOI: 10.1007/0-387-30747-8_3

A novel outer membrane β-1,6-glucanase is deployed in the predation of fungi by myxobacteria
journal, May 2019


Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition
journal, June 2019

  • Hestrin, Rachel; Hammer, Edith C.; Mueller, Carsten W.
  • Communications Biology, Vol. 2, Issue 1
  • DOI: 10.1038/s42003-019-0481-8

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014