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

Title: Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches

Abstract

Soil bacteria and fungi are known to form niche-specific communities that differ between actively growing and decaying roots. Yet almost nothing is known about the cross-kingdom interactions that frame these communities and the environmental filtering that defines these potentially friendly or competing neighbors. We explored the temporal and spatial patterns of soil fungal (mycorrhizal and nonmycorrhizal) and bacterial cooccurrence near roots of wild oat grass, Avena fatua, growing in its naturalized soil in a greenhouse experiment. Amplicon sequences of the fungal internal transcribed spacer (ITS) and bacterial 16S rRNA genes from rhizosphere and bulk soils collected at multiple plant growth stages were used to construct covariation-based networks as a step toward identifying fungal-bacterial associations. Corresponding stable-isotope-enabled metagenome-assembled genomes (MAGs) of bacteria identified in cooccurrence networks were used to inform potential mechanisms underlying the observed links. Bacterial-fungal networks were significantly different in rhizosphere versus bulk soils and between arbuscular mycorrhizal fungi (AMF) and nonmycorrhizal fungi. Over 12 weeks of plant growth, nonmycorrhizal fungi formed increasingly complex networks with bacteria in rhizosphere soils, while AMF more frequently formed networks with bacteria in bulk soils. Analysis of network-associated bacterial MAGs suggests that some of the fungal-bacterial links that we identified are potential indicatorsmore » of bacterial breakdown and consumption of fungal biomass, while others intimate shared ecological niches.« less

Authors:
 [1];  [1];  [1];  [2];  [3]; ORCiD logo [4];  [4];  [5]; ORCiD logo [6]
  1. Univ. of California, Berkeley, CA (United States)
  2. Univ. of Hawaii at Manoa, Honolulu, HI (United States)
  3. AgResearch Ltd., Lincoln Science Centre, Christchurch (New Zealand)
  4. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  5. Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
University of California, Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1780928
Alternate Identifier(s):
OSTI ID: 1902596
Report Number(s):
LLNL-JRNL-826080
Journal ID: ISSN 2150-7511
Grant/Contract Number:  
SC0020163; SC0010570; AC52-07NA27344
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 12; Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; Arbuscular Mycorrhizal Fungi (AMF); metagenome-assembled genome (MAG); cooccurrance network; rhizosphere; detritusphere; hyphosphere; stable-isotope probing (SIP); spatial heterogeneity

Citation Formats

Yuan, Mengting Maggie, Kakouridis, Anne, Starr, Evan, Nguyen, Nhu, Shi, Shengjing, Pett-Ridge, Jennifer, Nuccio, Erin, Zhou, Jizhong, and Firestone, Mary. Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches. United States: N. p., 2021. Web. doi:10.1128/mbio.03509-20.
Yuan, Mengting Maggie, Kakouridis, Anne, Starr, Evan, Nguyen, Nhu, Shi, Shengjing, Pett-Ridge, Jennifer, Nuccio, Erin, Zhou, Jizhong, & Firestone, Mary. Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches. United States. https://doi.org/10.1128/mbio.03509-20
Yuan, Mengting Maggie, Kakouridis, Anne, Starr, Evan, Nguyen, Nhu, Shi, Shengjing, Pett-Ridge, Jennifer, Nuccio, Erin, Zhou, Jizhong, and Firestone, Mary. Tue . "Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches". United States. https://doi.org/10.1128/mbio.03509-20. https://www.osti.gov/servlets/purl/1780928.
@article{osti_1780928,
title = {Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches},
author = {Yuan, Mengting Maggie and Kakouridis, Anne and Starr, Evan and Nguyen, Nhu and Shi, Shengjing and Pett-Ridge, Jennifer and Nuccio, Erin and Zhou, Jizhong and Firestone, Mary},
abstractNote = {Soil bacteria and fungi are known to form niche-specific communities that differ between actively growing and decaying roots. Yet almost nothing is known about the cross-kingdom interactions that frame these communities and the environmental filtering that defines these potentially friendly or competing neighbors. We explored the temporal and spatial patterns of soil fungal (mycorrhizal and nonmycorrhizal) and bacterial cooccurrence near roots of wild oat grass, Avena fatua, growing in its naturalized soil in a greenhouse experiment. Amplicon sequences of the fungal internal transcribed spacer (ITS) and bacterial 16S rRNA genes from rhizosphere and bulk soils collected at multiple plant growth stages were used to construct covariation-based networks as a step toward identifying fungal-bacterial associations. Corresponding stable-isotope-enabled metagenome-assembled genomes (MAGs) of bacteria identified in cooccurrence networks were used to inform potential mechanisms underlying the observed links. Bacterial-fungal networks were significantly different in rhizosphere versus bulk soils and between arbuscular mycorrhizal fungi (AMF) and nonmycorrhizal fungi. Over 12 weeks of plant growth, nonmycorrhizal fungi formed increasingly complex networks with bacteria in rhizosphere soils, while AMF more frequently formed networks with bacteria in bulk soils. Analysis of network-associated bacterial MAGs suggests that some of the fungal-bacterial links that we identified are potential indicators of bacterial breakdown and consumption of fungal biomass, while others intimate shared ecological niches.},
doi = {10.1128/mbio.03509-20},
journal = {mBio (Online)},
number = 2,
volume = 12,
place = {United States},
year = {Tue Apr 20 00:00:00 EDT 2021},
month = {Tue Apr 20 00:00:00 EDT 2021}
}

Works referenced in this record:

Interactions between mycorrhizal fungi and other soil organisms
journal, February 1994


FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild
journal, April 2016


Rhizosphere fungi actively assimilating plant-derived carbon in a grassland soil
journal, December 2020


Microbial interactions: from networks to models
journal, July 2012

  • Faust, Karoline; Raes, Jeroen
  • Nature Reviews Microbiology, Vol. 10, Issue 8
  • DOI: 10.1038/nrmicro2832

Multinucleate Spores Contribute to Evolutionary Longevity of Asexual Glomeromycota
journal, April 2010

  • Jany, Jean‐Luc; Pawlowska, Teresa E.
  • The American Naturalist, Vol. 175, Issue 4
  • DOI: 10.1086/650725

UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


Disentangling biotic interactions, environmental filters, and dispersal limitation as drivers of species co-occurrence
journal, December 2017

  • D'Amen, Manuela; Mod, Heidi K.; Gotelli, Nicholas J.
  • Ecography, Vol. 41, Issue 8
  • DOI: 10.1111/ecog.03148

The holistic rhizosphere: integrating zones, processes, and semantics in the soil influenced by roots
journal, March 2016

  • York, Larry M.; Carminati, Andrea; Mooney, Sacha J.
  • Journal of Experimental Botany, Vol. 67, Issue 12
  • DOI: 10.1093/jxb/erw108

Effect of Fungal Hyphae on the Access of Bacteria to Phenanthrene in Soil
journal, January 2007

  • Wick, Lukas Y.; Remer, Rita; Würz, Birgit
  • Environmental Science & Technology, Vol. 41, Issue 2
  • DOI: 10.1021/es061407s

The Case for Digging Deeper: Soil Organic Carbon Storage, Dynamics, and Controls in Our Changing World
journal, April 2019


Determinants of community structure in the global plankton interactome
journal, May 2015


Plant-Growth-Promoting Rhizobacteria
journal, October 2009


Highways versus pipelines: contributions of two fungal transport mechanisms to efficient bioremediation: Fungal transport mechanisms enhance bioremediation
journal, October 2012

  • Banitz, Thomas; Johst, Karin; Wick, Lukas Y.
  • Environmental Microbiology Reports, Vol. 5, Issue 2
  • DOI: 10.1111/1758-2229.12002

Anti-fungal properties of chitinolytic dune soil bacteria
journal, February 1998

  • De Boer, Wietse; Klein Gunnewiek, Paulien J. A.; Lafeber, Petra
  • Soil Biology and Biochemistry, Vol. 30, Issue 2
  • DOI: 10.1016/S0038-0717(97)00100-4

Chalara heteroderae a fungal antagonist that parasitizes hyphae of Bipolaris sorokiniana
journal, January 1986


Bacterial diversity among the fruit bodies of ectomycorrhizal and saprophytic fungi and their corresponding hyphosphere soils
journal, August 2018


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


Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests
journal, September 2016

  • Kaiser, Kristin; Wemheuer, Bernd; Korolkow, Vera
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep33696

Correlation Network Analysis Applied to Complex Biofilm Communities
journal, December 2011


The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO 2
journal, October 2014

  • Meier, Ina C.; Pritchard, Seth G.; Brzostek, Edward R.
  • New Phytologist, Vol. 205, Issue 3
  • DOI: 10.1111/nph.13122

Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2
journal, July 2011


Food-web structure and network theory: The role of connectance and size
journal, September 2002

  • Dunne, J. A.; Williams, R. J.; Martinez, N. D.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 20
  • DOI: 10.1073/pnas.192407699

Hitchhikers on the fungal highway: The helper effect for bacterial migration via fungal hyphae
journal, April 2011


Use and abuse of correlation analyses in microbial ecology
journal, June 2019


Fungal community assembly in drought-stressed sorghum shows stochasticity, selection, and universal ecological dynamics
journal, January 2020


Absence of nuclear DNA synthesis in vesicular-arbuscular mycorrhizal fungi during in vitro development
journal, January 1989


Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant Interactions
book, August 2020

  • Pett-Ridge, Jennifer; Shi, Shengjing; Estera-Molina, Katerina
  • Rhizosphere Biology: Interactions Between Microbes and Plants
  • DOI: 10.1007/978-981-15-6125-2_2

Insights on the susceptibility of plant pathogenic fungi to phenazine-1-carboxylic acid and its chemical derivatives
journal, June 2013


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


The role of rhizodeposits in shaping rhizomicrobiome
journal, December 2019

  • Tian, Tao; Reverdy, Alicyn; She, Qianxuan
  • Environmental Microbiology Reports, Vol. 12, Issue 2
  • DOI: 10.1111/1758-2229.12816

Strong succession in arbuscular mycorrhizal fungal communities
journal, August 2018


Availability of phosphate and potassium as the result of interactions between root and soil in the rhizosphere
journal, January 1986

  • Jungk, A.; Claassen, N.
  • Zeitschrift für Pflanzenernährung und Bodenkunde, Vol. 149, Issue 4
  • DOI: 10.1002/jpln.19861490406

Resource availability underlies the plant-fungal diversity relationship in a grassland ecosystem
journal, December 2017

  • Cline, Lauren C.; Hobbie, Sarah E.; Madritch, Michael D.
  • Ecology, Vol. 99, Issue 1
  • DOI: 10.1002/ecy.2075

Investigating the mechanisms for the opposing pH relationships of fungal and bacterial growth in soil
journal, June 2010


FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011


Observations of Nuclei in Vesicular-Arbuscular Mycorrhizal Fungi
journal, March 1987

  • Cooke, John C.; Gemma, J. N.; Koske, R. E.
  • Mycologia, Vol. 79, Issue 2
  • DOI: 10.2307/3807669

Rhizophagus irregularis influences As and P uptake by alfafa and the neighboring non-host pepperweed growing in an As-contaminated soil
journal, May 2018


Bacterial-Fungal Interactions: Hyphens between Agricultural, Clinical, Environmental, and Food Microbiologists
journal, November 2011

  • Frey-Klett, P.; Burlinson, P.; Deveau, A.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 4
  • DOI: 10.1128/MMBR.00020-11

Microbial hotspots and hot moments in soil: Concept & review
journal, April 2015


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Living in a fungal world: impact of fungi on soil bacterial niche development
journal, September 2005


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


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
  • DOI: 10.1111/mec.12481

DNA Content of Vesicular-Arbuscular Mycorrhizal Fungal Spores
journal, March 1990

  • Viera, Alejandro; Glenn, Marian G.
  • Mycologia, Vol. 82, Issue 2
  • DOI: 10.2307/3759857

Molecular ecological network analyses
journal, January 2012


Taking the Fungal Highway:  Mobilization of Pollutant-Degrading Bacteria by Fungi
journal, June 2005

  • Kohlmeier, Stefanie; Smits, Theo H. M.; Ford, Roseanne M.
  • Environmental Science & Technology, Vol. 39, Issue 12
  • DOI: 10.1021/es047979z

Status of nuclear division in arbuscular mycorrhizal fungi during in vitro development
journal, March 1993


Wall texture in the spore of a vesicular-arbuscular mycorrhizal fungus
journal, February 1984

  • Bonfante-Fasolo, Paola; Vian, Brigitte
  • Protoplasma, Vol. 120, Issue 1-2
  • DOI: 10.1007/BF01287617

Exploiting the fungal highway: development of a novel tool for the in situ isolation of bacteria migrating along fungal mycelium
journal, October 2015

  • Simon, Anaele; Bindschedler, Saskia; Job, Daniel
  • FEMS Microbiology Ecology, Vol. 91, Issue 11
  • DOI: 10.1093/femsec/fiv116

Estimation of the influx and the radius of the depletion zone developing around a root during nutrient uptake
journal, August 1995


Phosphorus depletion and pH decrease at the root–soil and hyphae–soil interfaces of VA mycorrhizal white clover fertilized with ammonium
journal, November 1991


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


Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
journal, July 2019


Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil
journal, September 1991

  • Li, Xiao-Lin; George, Eckhard; Marschner, Horst
  • Plant and Soil, Vol. 136, Issue 1
  • DOI: 10.1007/BF02465218

Using network analysis to explore co-occurrence patterns in soil microbial communities
journal, September 2011

  • Barberán, Albert; Bates, Scott T.; Casamayor, Emilio O.
  • The ISME Journal, Vol. 6, Issue 2
  • DOI: 10.1038/ismej.2011.119

‘Candidatus Moeniiplasma glomeromycotorum’, an endobacterium of arbuscular mycorrhizal fungi
journal, May 2017

  • Naito, Mizue; Desirò, Alessandro; González, Jonathan B.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 5, p. 1177-1184
  • DOI: 10.1099/ijsem.0.001785

The rhizosphere microbiome and plant health
journal, August 2012

  • Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M.
  • Trends in Plant Science, Vol. 17, Issue 8
  • DOI: 10.1016/j.tplants.2012.04.001

Fungal diversity regulates plant-soil feedbacks in temperate grassland
journal, November 2018

  • Semchenko, Marina; Leff, Jonathan W.; Lozano, Yudi M.
  • Science Advances, Vol. 4, Issue 11
  • DOI: 10.1126/sciadv.aau4578

Stability of Ecological Communities and the Architecture of Mutualistic and Trophic Networks
journal, August 2010


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

Deciphering Underlying Drivers of Disease Suppressiveness Against Pathogenic Fusarium oxysporum
journal, November 2019


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Bacterial associations with decaying wood: a review
journal, January 1996


Interdomain ecological networks between plants and microbes
journal, September 2019


Interactions between mycorrhizal fungi and mycorrhizosphere bacteria during mineral weathering: Budget analysis and bacterial quantification
journal, September 2009


Impact of white-rot fungi on numbers and community composition of bacteria colonizing beech wood from forest soil: Impact of white-rot fungi on bacteria colonizing wood
journal, February 2008


Universal and species-specific bacterial ‘fungiphiles’ in the mycospheres of different basidiomycetous fungi
journal, February 2009


Bacterial community establishment in native and non-native soils and the effect of fungal colonization
journal, January 2013

  • Nazir, Rashid; Semenov, Alexander V.; Sarigul, Nermin
  • Microbiology Discovery, Vol. 1, Issue 1
  • DOI: 10.7243/2052-6180-1-8

Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth
journal, January 2006


Ecological networks and their fragility
journal, July 2006

  • Montoya, José M.; Pimm, Stuart L.; Solé, Ricard V.
  • Nature, Vol. 442, Issue 7100
  • DOI: 10.1038/nature04927

Wood-Decaying Ascomycetes and Fungi Imperfecti
journal, July 1966

  • Duncan, Catherine G.; Eslyn, Wallace E.
  • Mycologia, Vol. 58, Issue 4
  • DOI: 10.2307/3757045

Modularity and community structure in networks
journal, May 2006

  • Newman, M. E. J.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 23
  • DOI: 10.1073/pnas.0601602103

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

The modularity of pollination networks
journal, December 2007

  • Olesen, J. M.; Bascompte, J.; Dupont, Y. L.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 50
  • DOI: 10.1073/pnas.0706375104

Indices, Graphs and Null Models: Analyzing Bipartite Ecological Networks
journal, February 2009


Self versus non-self: fungal cell wall degradation in Trichoderma
journal, January 2012


Tansley Review No. 76 Helper bacteria: a new dimension to the mycorrhizal symbiosis
journal, October 1994


Co‐occurrence is not evidence of ecological interactions
journal, May 2020

  • Blanchet, F. Guillaume; Cazelles, Kevin; Gravel, Dominique
  • Ecology Letters, Vol. 23, Issue 7
  • DOI: 10.1111/ele.13525

Zygospores and asexual spores of Gigaspora decipiens, an arbuscular mycorrhizal fungus
journal, October 1990


The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
journal, June 2016

  • Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.
  • Ecology Letters, Vol. 19, Issue 8
  • DOI: 10.1111/ele.12630

Microbial interactions and biocontrol in the rhizosphere
journal, March 2001


Folsomia candida, a “fungivorous” collembolan, feeds preferentially on nematodes rather than soil fungi
journal, April 1996