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

Yuan, Mengting Maggie; Kakouridis, Anne; Starr, Evan; Nguyen, Nhu; Shi, Shengjing; Pett-Ridge, Jennifer; Nuccio, Erin; Zhou, Jizhong; Firestone, Mary

doi:10.1128/mbio.03509-20

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

Journal Article · Tue Apr 20 00:00:00 EDT 2021 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.03509-20· OSTI ID:1780928

Yuan, Mengting Maggie ^[1]; Kakouridis, Anne ^[1]; Starr, Evan ^[1]; Nguyen, Nhu ^[2]; Shi, Shengjing ^[3];

^[4]; Nuccio, Erin ^[4]; Zhou, Jizhong ^[5];

^[6]

Univ. of California, Berkeley, CA (United States)
Univ. of Hawaii at Manoa, Honolulu, HI (United States)
AgResearch Ltd., Lincoln Science Centre, Christchurch (New Zealand)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: University of California, Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: SC0020163; SC0010570; AC52-07NA27344

OSTI ID:: 1780928

Alternate ID(s):: OSTI ID: 1902596

Report Number(s):: LLNL-JRNL-826080

Journal Information:: mBio (Online), Vol. 12, Issue 2; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

References (89)

Interactions between mycorrhizal fungi and other soil organisms Fitter, A. H.; Garbaye, J. Plant and Soil, Vol. 159, Issue 1 https://doi.org/10.1007/BF00000101	journal	February 1994
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild Nguyen, Nhu H.; Song, Zewei; Bates, Scott T. Fungal Ecology, Vol. 20 https://doi.org/10.1016/j.funeco.2015.06.006	journal	April 2016
Rhizosphere fungi actively assimilating plant-derived carbon in a grassland soil Hannula, S. E.; Morriën, E.; van der Putten, W. H. Fungal Ecology, Vol. 48 https://doi.org/10.1016/j.funeco.2020.100988	journal	December 2020
Microbial interactions: from networks to models Faust, Karoline; Raes, Jeroen Nature Reviews Microbiology, Vol. 10, Issue 8 https://doi.org/10.1038/nrmicro2832	journal	July 2012
Btrim: A fast, lightweight adapter and quality trimming program for next-generation sequencing technologies Kong, Yong Genomics, Vol. 98, Issue 2 https://doi.org/10.1016/j.ygeno.2011.05.009	journal	August 2011
Multinucleate Spores Contribute to Evolutionary Longevity of Asexual Glomeromycota Jany, Jean‐Luc; Pawlowska, Teresa E. The American Naturalist, Vol. 175, Issue 4 https://doi.org/10.1086/650725	journal	April 2010
UCHIME improves sensitivity and speed of chimera detection Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C. Bioinformatics, Vol. 27, Issue 16 https://doi.org/10.1093/bioinformatics/btr381	journal	June 2011
Disentangling biotic interactions, environmental filters, and dispersal limitation as drivers of species co-occurrence D'Amen, Manuela; Mod, Heidi K.; Gotelli, Nicholas J. Ecography, Vol. 41, Issue 8 https://doi.org/10.1111/ecog.03148	journal	December 2017
The holistic rhizosphere: integrating zones, processes, and semantics in the soil influenced by roots York, Larry M.; Carminati, Andrea; Mooney, Sacha J. Journal of Experimental Botany, Vol. 67, Issue 12 https://doi.org/10.1093/jxb/erw108	journal	March 2016
Effect of Fungal Hyphae on the Access of Bacteria to Phenanthrene in Soil Wick, Lukas Y.; Remer, Rita; Würz, Birgit Environmental Science & Technology, Vol. 41, Issue 2 https://doi.org/10.1021/es061407s	journal	January 2007
The Case for Digging Deeper: Soil Organic Carbon Storage, Dynamics, and Controls in Our Changing World Gross, Cole D.; Harrison, Robert B. Soil Systems, Vol. 3, Issue 2 https://doi.org/10.3390/soilsystems3020028	journal	April 2019
Determinants of community structure in the global plankton interactome Lima-Mendez, G.; Faust, K.; Henry, N. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1262073	journal	May 2015
Plant-Growth-Promoting Rhizobacteria Lugtenberg, Ben; Kamilova, Faina Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.62.081307.162918	journal	October 2009
Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate‐solubilizing bacterium Zhang, Lin; Xu, Minggang; Liu, Yu New Phytologist, Vol. 210, Issue 3 https://doi.org/10.1111/nph.13838	journal	January 2016
Highways versus pipelines: contributions of two fungal transport mechanisms to efficient bioremediation: Fungal transport mechanisms enhance bioremediation Banitz, Thomas; Johst, Karin; Wick, Lukas Y. Environmental Microbiology Reports, Vol. 5, Issue 2 https://doi.org/10.1111/1758-2229.12002	journal	October 2012
Anti-fungal properties of chitinolytic dune soil bacteria De Boer, Wietse; Klein Gunnewiek, Paulien J. A.; Lafeber, Petra Soil Biology and Biochemistry, Vol. 30, Issue 2 https://doi.org/10.1016/S0038-0717(97)00100-4	journal	February 1998
Chalara heteroderae a fungal antagonist that parasitizes hyphae of Bipolaris sorokiniana Duczek, L. J.; White, G. P. Soil Biology and Biochemistry, Vol. 18, Issue 6 https://doi.org/10.1016/0038-0717(86)90090-8	journal	January 1986
Bacterial diversity among the fruit bodies of ectomycorrhizal and saprophytic fungi and their corresponding hyphosphere soils Liu, Yaping; Sun, Qibiao; Li, Jing Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-30120-6	journal	August 2018
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests Kaiser, Kristin; Wemheuer, Bernd; Korolkow, Vera Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33696	journal	September 2016
Correlation Network Analysis Applied to Complex Biofilm Communities Duran-Pinedo, Ana E.; Paster, Bruce; Teles, Ricardo PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028438	journal	December 2011
The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO ₂ Meier, Ina C.; Pritchard, Seth G.; Brzostek, Edward R. New Phytologist, Vol. 205, Issue 3 https://doi.org/10.1111/nph.13122	journal	October 2014
Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2 Zhou, Jizhong; Deng, Ye; Luo, Feng mBio, Vol. 2, Issue 4 https://doi.org/10.1128/mBio.00122-11	journal	July 2011
Food-web structure and network theory: The role of connectance and size Dunne, J. A.; Williams, R. J.; Martinez, N. D. Proceedings of the National Academy of Sciences, Vol. 99, Issue 20 https://doi.org/10.1073/pnas.192407699	journal	September 2002
Hitchhikers on the fungal highway: The helper effect for bacterial migration via fungal hyphae Warmink, J. A.; Nazir, R.; Corten, B. Soil Biology and Biochemistry, Vol. 43, Issue 4 https://doi.org/10.1016/j.soilbio.2010.12.009	journal	April 2011
Use and abuse of correlation analyses in microbial ecology Carr, Alex; Diener, Christian; Baliga, Nitin S. The ISME Journal, Vol. 13, Issue 11 https://doi.org/10.1038/s41396-019-0459-z	journal	June 2019
Fungal community assembly in drought-stressed sorghum shows stochasticity, selection, and universal ecological dynamics Gao, Cheng; Montoya, Liliam; Xu, Ling Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-13913-9	journal	January 2020
Absence of nuclear DNA synthesis in vesicular-arbuscular mycorrhizal fungi during in vitro development Burggraaf, A. J. P.; Beringer, J. E. New Phytologist, Vol. 111, Issue 1 https://doi.org/10.1111/j.1469-8137.1989.tb04214.x	journal	January 1989
Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant Interactions Pett-Ridge, Jennifer; Shi, Shengjing; Estera-Molina, Katerina Rhizosphere Biology: Interactions Between Microbes and Plants https://doi.org/10.1007/978-981-15-6125-2_2	book	August 2020
Insights on the susceptibility of plant pathogenic fungi to phenazine-1-carboxylic acid and its chemical derivatives Puopolo, Gerardo; Masi, Marco; Raio, Aida Natural Product Research, Vol. 27, Issue 11 https://doi.org/10.1080/14786419.2012.696257	journal	June 2013
Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition Herman, Donald J.; Firestone, Mary K.; Nuccio, Erin FEMS Microbiology Ecology, Vol. 80, Issue 1 https://doi.org/10.1111/j.1574-6941.2011.01292.x	journal	January 2012
The role of rhizodeposits in shaping rhizomicrobiome Tian, Tao; Reverdy, Alicyn; She, Qianxuan Environmental Microbiology Reports, Vol. 12, Issue 2 https://doi.org/10.1111/1758-2229.12816	journal	December 2019
Strong succession in arbuscular mycorrhizal fungal communities Gao, Cheng; Montoya, Liliam; Xu, Ling The ISME Journal, Vol. 13, Issue 1 https://doi.org/10.1038/s41396-018-0264-0	journal	August 2018
The Microbiome of Pinus muricata Ectomycorrhizae: Community Assemblages, Fungal Species Effects, and Burkholderia as Important Bacteria in Multipartnered Symbioses Nguyen, Nhu H.; Bruns, Thomas D. Microbial Ecology, Vol. 69, Issue 4 https://doi.org/10.1007/s00248-015-0574-y	journal	February 2015
Availability of phosphate and potassium as the result of interactions between root and soil in the rhizosphere Jungk, A.; Claassen, N. Zeitschrift für Pflanzenernährung und Bodenkunde, Vol. 149, Issue 4 https://doi.org/10.1002/jpln.19861490406	journal	January 1986
Resource availability underlies the plant-fungal diversity relationship in a grassland ecosystem Cline, Lauren C.; Hobbie, Sarah E.; Madritch, Michael D. Ecology, Vol. 99, Issue 1 https://doi.org/10.1002/ecy.2075	journal	December 2017
Investigating the mechanisms for the opposing pH relationships of fungal and bacterial growth in soil Rousk, Johannes; Brookes, Philip C.; Bååth, Erland Soil Biology and Biochemistry, Vol. 42, Issue 6 https://doi.org/10.1016/j.soilbio.2010.02.009	journal	June 2010
An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition: AMF alters soil bacterial community and N cycling Nuccio, Erin E.; Hodge, Angela; Pett-Ridge, Jennifer Environmental Microbiology, Vol. 15, Issue 6 https://doi.org/10.1111/1462-2920.12081	journal	January 2013
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
Observations of Nuclei in Vesicular-Arbuscular Mycorrhizal Fungi Cooke, John C.; Gemma, J. N.; Koske, R. E. Mycologia, Vol. 79, Issue 2 https://doi.org/10.2307/3807669	journal	March 1987
Rhizophagus irregularis influences As and P uptake by alfafa and the neighboring non-host pepperweed growing in an As-contaminated soil Zhang, Xin; Ren, Baihui; Wu, Songlin Journal of Environmental Sciences, Vol. 67 https://doi.org/10.1016/j.jes.2017.07.005	journal	May 2018
Bacterial-Fungal Interactions: Hyphens between Agricultural, Clinical, Environmental, and Food Microbiologists Frey-Klett, P.; Burlinson, P.; Deveau, A. Microbiology and Molecular Biology Reviews, Vol. 75, Issue 4 https://doi.org/10.1128/MMBR.00020-11	journal	November 2011
Microbial hotspots and hot moments in soil: Concept & review Kuzyakov, Yakov; Blagodatskaya, Evgenia Soil Biology and Biochemistry, Vol. 83 https://doi.org/10.1016/j.soilbio.2015.01.025	journal	April 2015
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Living in a fungal world: impact of fungi on soil bacterial niche development Boer, Wietse de; Folman, Larissa B.; Summerbell, Richard C. FEMS Microbiology Reviews, Vol. 29, Issue 4 https://doi.org/10.1016/j.femsre.2004.11.005	journal	September 2005
Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons Shi, Shengjing; Nuccio, Erin; Herman, Donald J. mBio, Vol. 6, Issue 4 https://doi.org/10.1128/mBio.00746-15	journal	August 2015
Towards a unified paradigm for sequence-based identification of fungi Kõljalg, Urmas; Nilsson, R. Henrik; Abarenkov, Kessy Molecular Ecology, Vol. 22, Issue 21 https://doi.org/10.1111/mec.12481	journal	September 2013
DNA Content of Vesicular-Arbuscular Mycorrhizal Fungal Spores Viera, Alejandro; Glenn, Marian G. Mycologia, Vol. 82, Issue 2 https://doi.org/10.2307/3759857	journal	March 1990
Molecular ecological network analyses Deng, Ye; Jiang, Yi-Huei; Yang, Yunfeng BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-113	journal	January 2012
Taking the Fungal Highway: Mobilization of Pollutant-Degrading Bacteria by Fungi Kohlmeier, Stefanie; Smits, Theo H. M.; Ford, Roseanne M. Environmental Science & Technology, Vol. 39, Issue 12 https://doi.org/10.1021/es047979z	journal	June 2005
Status of nuclear division in arbuscular mycorrhizal fungi during in vitro development B�card, G.; Pfeffer, P. E. Protoplasma, Vol. 174, Issue 1-2 https://doi.org/10.1007/BF01404043	journal	March 1993
Wall texture in the spore of a vesicular-arbuscular mycorrhizal fungus Bonfante-Fasolo, Paola; Vian, Brigitte Protoplasma, Vol. 120, Issue 1-2 https://doi.org/10.1007/BF01287617	journal	February 1984
Exploiting the fungal highway: development of a novel tool for the in situ isolation of bacteria migrating along fungal mycelium Simon, Anaele; Bindschedler, Saskia; Job, Daniel FEMS Microbiology Ecology, Vol. 91, Issue 11 https://doi.org/10.1093/femsec/fiv116	journal	October 2015
Estimation of the influx and the radius of the depletion zone developing around a root during nutrient uptake Syring, K. M.; Claassen, N. Plant and Soil, Vol. 175, Issue 1 https://doi.org/10.1007/BF02413016	journal	August 1995
Phosphorus depletion and pH decrease at the root–soil and hyphae–soil interfaces of VA mycorrhizal white clover fertilized with ammonium Li, Xiao‐Lin; George, Eckhard; Marschner, Horst New Phytologist, Vol. 119, Issue 3 https://doi.org/10.1111/j.1469-8137.1991.tb00039.x	journal	November 1991
Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure: Effects of AM mycelial exudates on soil bacteria Toljander, Jonas F.; Lindahl, BjÃ¶rn D.; Paul, Leslie R. FEMS Microbiology Ecology, Vol. 61, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00337.x	journal	August 2007
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil Li, Xiao-Lin; George, Eckhard; Marschner, Horst Plant and Soil, Vol. 136, Issue 1 https://doi.org/10.1007/BF02465218	journal	September 1991
Using network analysis to explore co-occurrence patterns in soil microbial communities Barberán, Albert; Bates, Scott T.; Casamayor, Emilio O. The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.119	journal	September 2011
‘Candidatus Moeniiplasma glomeromycotorum’, an endobacterium of arbuscular mycorrhizal fungi Naito, Mizue; Desirò, Alessandro; González, Jonathan B. International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 5, p. 1177-1184 https://doi.org/10.1099/ijsem.0.001785	journal	May 2017
The rhizosphere microbiome and plant health Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M. Trends in Plant Science, Vol. 17, Issue 8 https://doi.org/10.1016/j.tplants.2012.04.001	journal	August 2012
Fungal diversity regulates plant-soil feedbacks in temperate grassland Semchenko, Marina; Leff, Jonathan W.; Lozano, Yudi M. Science Advances, Vol. 4, Issue 11 https://doi.org/10.1126/sciadv.aau4578	journal	November 2018
Stability of Ecological Communities and the Architecture of Mutualistic and Trophic Networks Thebault, E.; Fontaine, C. Science, Vol. 329, Issue 5993 https://doi.org/10.1126/science.1188321	journal	August 2010
Cellular interactions between arbuscular mycorrhizal fungi and rhizosphere bacteria Bianciotto, V.; Minerdi, D.; Perotto, S. Protoplasma, Vol. 193, Issue 1-4 https://doi.org/10.1007/BF01276640	journal	March 1996
Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria: Interactions between AM fungi and bacteria in organic matter Leigh, Joanne; Fitter, Alastair H.; Hodge, Angela FEMS Microbiology Ecology, Vol. 76, Issue 3 https://doi.org/10.1111/j.1574-6941.2011.01066.x	journal	March 2011
Deciphering Underlying Drivers of Disease Suppressiveness Against Pathogenic Fusarium oxysporum Ou, Yannan; Penton, C. Ryan; Geisen, Stefan Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02535	journal	November 2019
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Bacterial associations with decaying wood: a review Clausen, Carol A. International Biodeterioration & Biodegradation, Vol. 37, Issue 1-2 https://doi.org/10.1016/0964-8305(95)00109-3	journal	January 1996
Interdomain ecological networks between plants and microbes Feng, Kai; Zhang, Yuguang; He, Zhili Molecular Ecology Resources, Vol. 19, Issue 6 https://doi.org/10.1111/1755-0998.13081	journal	September 2019
Interactions between mycorrhizal fungi and mycorrhizosphere bacteria during mineral weathering: Budget analysis and bacterial quantification Koele, Nina; Turpault, Marie-Pierre; Hildebrand, Ernst E. Soil Biology and Biochemistry, Vol. 41, Issue 9 https://doi.org/10.1016/j.soilbio.2009.06.017	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 Folman, Larissa B.; Klein Gunnewiek, Paulien J. A.; Boddy, Lynne FEMS Microbiology Ecology, Vol. 63, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00425.x	journal	February 2008
Universal and species-specific bacterial ‘fungiphiles’ in the mycospheres of different basidiomycetous fungi Warmink, J. A.; Nazir, R.; van Elsas, J. D. Environmental Microbiology, Vol. 11, Issue 2 https://doi.org/10.1111/j.1462-2920.2008.01767.x	journal	February 2009
Bacterial community establishment in native and non-native soils and the effect of fungal colonization Nazir, Rashid; Semenov, Alexander V.; Sarigul, Nermin Microbiology Discovery, Vol. 1, Issue 1 https://doi.org/10.7243/2052-6180-1-8	journal	January 2013
Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth Artursson, Veronica; Finlay, Roger D.; Jansson, Janet K. Environmental Microbiology, Vol. 8, Issue 1 https://doi.org/10.1111/j.1462-2920.2005.00942.x	journal	January 2006
Ecological networks and their fragility Montoya, José M.; Pimm, Stuart L.; Solé, Ricard V. Nature, Vol. 442, Issue 7100 https://doi.org/10.1038/nature04927	journal	July 2006
Wood-Decaying Ascomycetes and Fungi Imperfecti Duncan, Catherine G.; Eslyn, Wallace E. Mycologia, Vol. 58, Issue 4 https://doi.org/10.2307/3757045	journal	July 1966
Modularity and community structure in networks Newman, M. E. J. Proceedings of the National Academy of Sciences, Vol. 103, Issue 23 https://doi.org/10.1073/pnas.0601602103	journal	May 2006
Evolutionary history of mycorrhizal symbioses and global host plant diversity Brundrett, Mark C.; Tedersoo, Leho New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.14976	journal	January 2018
The modularity of pollination networks Olesen, J. M.; Bascompte, J.; Dupont, Y. L. Proceedings of the National Academy of Sciences, Vol. 104, Issue 50 https://doi.org/10.1073/pnas.0706375104	journal	December 2007
Indices, Graphs and Null Models: Analyzing Bipartite Ecological Networks Dormann, Carsten F.; Frund, Jochen; Bluthgen, Nico The Open Ecology Journal, Vol. 2, Issue 1 https://doi.org/10.2174/1874213000902010007	journal	February 2009
Self versus non-self: fungal cell wall degradation in Trichoderma Gruber, Sabine; Seidl-Seiboth, Verena Microbiology, Vol. 158, Issue 1 https://doi.org/10.1099/mic.0.052613-0	journal	January 2012
Tansley Review No. 76 Helper bacteria: a new dimension to the mycorrhizal symbiosis Garbaye, J. New Phytologist, Vol. 128, Issue 2 https://doi.org/10.1111/j.1469-8137.1994.tb04003.x	journal	October 1994
Co‐occurrence is not evidence of ecological interactions Blanchet, F. Guillaume; Cazelles, Kevin; Gravel, Dominique Ecology Letters, Vol. 23, Issue 7 https://doi.org/10.1111/ele.13525	journal	May 2020
Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions Wu, Qiang-Sheng; Xia, Ren-Xue Journal of Plant Physiology, Vol. 163, Issue 4 https://doi.org/10.1016/j.jplph.2005.04.024	journal	March 2006
Zygospores and asexual spores of Gigaspora decipiens, an arbuscular mycorrhizal fungus Tommerup, I. C.; Sivasithamparam, K. Mycological Research, Vol. 94, Issue 7 https://doi.org/10.1016/S0953-7562(09)81303-8	journal	October 1990
The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J. Ecology Letters, Vol. 19, Issue 8 https://doi.org/10.1111/ele.12630	journal	June 2016
Network succession reveals the importance of competition in response to emulsified vegetable oil amendment for uranium bioremediation: Competition in bioremediation system Deng, Ye; Zhang, Ping; Qin, Yujia Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.12981	journal	August 2015
Microbial interactions and biocontrol in the rhizosphere Whipps, J. M. Journal of Experimental Botany, Vol. 52, Issue suppl 1 https://doi.org/10.1093/jexbot/52.suppl_1.487	journal	March 2001
Folsomia candida, a “fungivorous” collembolan, feeds preferentially on nematodes rather than soil fungi Lee, Queena; Widden, Paul Soil Biology and Biochemistry, Vol. 28, Issue 4-5 https://doi.org/10.1016/0038-0717(95)00158-1	journal	April 1996

Similar Records

HT-SIP: a semi-automated stable isotope probing pipeline identifies cross-kingdom interactions in the hyphosphere of arbuscular mycorrhizal fungi

Journal Article · Fri Nov 25 00:00:00 EST 2022 · Microbiome · OSTI ID:1780928

Nuccio, Erin E.; Blazewicz, Steven J.; Lafler, Marissa; +11 more

Routes to roots: direct evidence of water transport by arbuscular mycorrhizal fungi to host plants

Journal Article · Fri Jul 01 00:00:00 EDT 2022 · New Phytologist · OSTI ID:1780928

Kakouridis, Anne; Hagen, John A.; Kan, Megan P.; +6 more

The rhizosphere and cropping system, but not arbuscular mycorrhizae, affect ammonia oxidizing archaea and bacteria abundances in two agricultural soils

Journal Article · Wed Jul 01 00:00:00 EDT 2020 · Applied Soil Ecology · OSTI ID:1780928

Wattenburger, Cassandra; Gutknecht, Jessica; Zhang, Quan; +3 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
Arbuscular Mycorrhizal Fungi (AMF)
metagenome-assembled genome (MAG)
cooccurrance network
rhizosphere
detritusphere
hyphosphere
stable-isotope probing (SIP)
spatial heterogeneity

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

Citation Formats

References (89)

Similar Records

Related Subjects