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

Emmett, Bryan D.; Lévesque-Tremblay, Véronique; Harrison, Maria J.

doi:10.1038/s41396-021-00920-2

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

Journal Article · Mon Mar 01 00:00:00 EST 2021 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-021-00920-2· OSTI ID:1768659

; Lévesque-Tremblay, Véronique;

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.

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Research Organization:: Univ. of Nebraska, Lincoln, NE (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0014395

OSTI ID:: 1768659

Alternate ID(s):: OSTI ID: 1775488

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 8 Vol. 15; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (79)

The Myxobacteria Shimkets, Lawrence J.; Dworkin, Martin; Reichenbach, Hans The Prokaryotes, p. 31-115 https://doi.org/10.1007/0-387-30747-8_3	book	January 2006
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
Biological Soil Crusts from Different Soil Substrates Harbor Distinct Bacterial Groups with the Potential to Produce Exopolysaccharides and Lipopolysaccharides Cania, Barbara; Vestergaard, Gisle; Kublik, Susanne Microbial Ecology, Vol. 79, Issue 2 https://doi.org/10.1007/s00248-019-01415-6	journal	August 2019
Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates Agnolucci, Monica; Battini, Fabio; Cristani, Caterina Biology and Fertility of Soils, Vol. 51, Issue 3 https://doi.org/10.1007/s00374-014-0989-5	journal	January 2015
Phylogenetic distribution and evolution of mycorrhizas in land plants Wang, B.; Qiu, Y. -L. Mycorrhiza, Vol. 16, Issue 5 https://doi.org/10.1007/s00572-005-0033-6	journal	May 2006
Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralisation Paterson, Eric; Sim, Allan; Davidson, Jane Plant and Soil, Vol. 408, Issue 1-2 https://doi.org/10.1007/s11104-016-2928-8	journal	May 2016
Phosphatase activity in the rhizosphere and hyphosphere of VA mycorrhizal wheat supplied with inorganic and organic phosphorus Tarafdar, J. C.; Marschner, H. Soil Biology and Biochemistry, Vol. 26, Issue 3 https://doi.org/10.1016/0038-0717(94)90288-7	journal	March 1994
Mineral nutrition, toxic element accumulation and water relations of arbuscular mycorrhizal plants Smith, Sally E.; Read, David Mycorrhizal Symbiosis https://doi.org/10.1016/B978-012370526-6.50007-6	book	January 2008
Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots St-Arnaud, M.; Hamel, C.; Vimard, B. Mycological Research, Vol. 100, Issue 3 https://doi.org/10.1016/S0953-7562(96)80164-X	journal	March 1996
Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C. Cell Host & Microbe, Vol. 17, Issue 3 https://doi.org/10.1016/j.chom.2015.01.011	journal	March 2015
A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1 Floss, Daniela S.; Gomez, S. Karen; Park, Hee-Jin Current Biology, Vol. 27, Issue 8 https://doi.org/10.1016/j.cub.2017.03.003	journal	April 2017
Response of soil microbial communities to compost amendments Pérez-Piqueres, Ana; Edel-Hermann, Véronique; Alabouvette, Claude Soil Biology and Biochemistry, Vol. 38, Issue 3 https://doi.org/10.1016/j.soilbio.2005.05.025	journal	March 2006
Trapping of phosphate solubilizing bacteria on hyphae of the arbuscular mycorrhizal fungus Rhizophagus irregularis DAOM 197198 Taktek, Salma; Trépanier, Martin; Servin, Paola Magallon Soil Biology and Biochemistry, Vol. 90 https://doi.org/10.1016/j.soilbio.2015.07.016	journal	November 2015
UniFrac: an effective distance metric for microbial community comparison Lozupone, Catherine; Lladser, Manuel E.; Knights, Dan The ISME Journal, Vol. 5, Issue 2 https://doi.org/10.1038/ismej.2010.133	journal	September 2010
Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi Scheublin, Tanja R.; Sanders, Ian R.; Keel, Christoph The ISME Journal, Vol. 4, Issue 6 https://doi.org/10.1038/ismej.2010.5	journal	February 2010
Soil bacterial and fungal communities across a pH gradient in an arable soil Rousk, Johannes; Bååth, Erland; Brookes, Philip C. The ISME Journal, Vol. 4, Issue 10 https://doi.org/10.1038/ismej.2010.58	journal	May 2010
Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi Desirò, Alessandro; Salvioli, Alessandra; Ngonkeu, Eddy L. The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.151	journal	September 2013
Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota Bonfante, Paola; Desirò, Alessandro The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.21	journal	April 2017
Defining the core Arabidopsis thaliana root microbiome Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11237	journal	August 2012
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life Parks, Donovan H.; Chuvochina, Maria; Waite, David W. Nature Biotechnology, Vol. 36, Issue 10 https://doi.org/10.1038/nbt.4229	journal	August 2018
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota Svenningsen, Nanna B.; Watts-Williams, Stephanie J.; Joner, Erik J. The ISME Journal, Vol. 12, Issue 5 https://doi.org/10.1038/s41396-018-0059-3	journal	January 2018
Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium Zhang, Lin; Feng, Gu; Declerck, Stéphane The ISME Journal, Vol. 12, Issue 10 https://doi.org/10.1038/s41396-018-0171-4	journal	June 2018
Distribution and population structure of endobacteria in arbuscular mycorrhizal fungi at North Atlantic dunes Lastovetsky, Olga A.; Ahn, Ezekiel; Mondo, Stephen J. The ISME Journal, Vol. 12, Issue 12 https://doi.org/10.1038/s41396-018-0246-2	journal	August 2018
A novel outer membrane β-1,6-glucanase is deployed in the predation of fungi by myxobacteria Li, Zhoukun; Ye, Xianfeng; Liu, Muxing The ISME Journal, Vol. 13, Issue 9 https://doi.org/10.1038/s41396-019-0424-x	journal	May 2019
Niche differentiation is spatially and temporally regulated in the rhizosphere Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0582-x	journal	January 2020
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
Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition Hestrin, Rachel; Hammer, Edith C.; Mueller, Carsten W. Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0481-8	journal	June 2019
In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil Johnson, D.; Leake, J. R.; Ostle, N. New Phytologist, Vol. 153, Issue 2 https://doi.org/10.1046/j.0028-646X.2001.00316.x	journal	February 2002
Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil Hodge, Angela New Phytologist, Vol. 151, Issue 3 https://doi.org/10.1046/j.0028-646x.2001.00200.x	journal	September 2001
Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling Hodge, A.; Fitter, A. H. Proceedings of the National Academy of Sciences, Vol. 107, Issue 31 https://doi.org/10.1073/pnas.1005874107	journal	July 2010
Diversity and heritability of the maize rhizosphere microbiome under field conditions Peiffer, J. A.; Spor, A.; Koren, O. Proceedings of the National Academy of Sciences, Vol. 110, Issue 16 https://doi.org/10.1073/pnas.1302837110	journal	April 2013
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis Tisserant, E.; Malbreil, M.; Kuo, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 50 https://doi.org/10.1073/pnas.1313452110	journal	November 2013
Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives Schlaeppi, K.; Dombrowski, N.; Oter, R. G. Proceedings of the National Academy of Sciences, Vol. 111, Issue 2 https://doi.org/10.1073/pnas.1321597111	journal	December 2013
Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants Wang, Shuangshuang; Chen, Aiqun; Xie, Kun Proceedings of the National Academy of Sciences, Vol. 117, Issue 28 https://doi.org/10.1073/pnas.2000926117	journal	June 2020
Bacterial biofilm formation on the hyphae of ectomycorrhizal fungi: a widespread ability under controls? Miquel Guennoc, Cora; Rose, Christophe; Labbé, Jessy FEMS Microbiology Ecology, Vol. 94, Issue 7 https://doi.org/10.1093/femsec/fiy093	journal	May 2018
Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils Cruz-Paredes, Carla; Svenningsen, Nanna Bygvraa; Nybroe, Ole FEMS Microbiology Ecology, Vol. 95, Issue 3 https://doi.org/10.1093/femsec/fiz020	journal	February 2019
Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium Finlay, R. D. Journal of Experimental Botany, Vol. 59, Issue 5 https://doi.org/10.1093/jxb/ern059	journal	February 2008
In situ stable isotope probing of phosphate-solubilizing bacteria in the hyphosphere Wang, Fei; Shi, Ning; Jiang, Rongfeng Journal of Experimental Botany, Vol. 67, Issue 6 https://doi.org/10.1093/jxb/erv561	journal	January 2016
Interactions Between Myxobacteria, Plant Pathogenic Fungi, and Biocontrol Agents Bull, C. T.; Shetty, K. G.; Subbarao, K. V. Plant Disease, Vol. 86, Issue 8 https://doi.org/10.1094/PDIS.2002.86.8.889	journal	August 2002
'Candidatus Glomeribacter gigasporarum' gen. nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi Bianciotto, V. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 1 https://doi.org/10.1099/ijs.0.02382-0	journal	January 2003
Collimonas fungivorans gen. nov., sp. nov., a chitinolytic soil bacterium with the ability to grow on living fungal hyphae de Boer, W. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 3 https://doi.org/10.1099/ijs.0.02920-0	journal	May 2004
Phosphorus Uptake by Plants: From Soil to Cell Schachtman, Daniel P.; Reid, Robert J.; Ayling, S. M. Plant Physiology, Vol. 116, Issue 2 https://doi.org/10.1104/pp.116.2.447	journal	February 1998
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
Host signature effect on plant root-associated microbiomes revealed through analyses of resident vs . active communities : Host effect on plant root-associated microbiomes Ofek, Maya; Voronov-Goldman, Milana; Hadar, Yitzhak Environmental Microbiology, Vol. 16, Issue 7 https://doi.org/10.1111/1462-2920.12228	journal	August 2013
Bacterial predation: 75 years and counting!: Bacterial predation Pérez, Juana; Moraleda-Muñoz, Aurelio; Marcos-Torres, Francisco Javier Environmental Microbiology, Vol. 18, Issue 3 https://doi.org/10.1111/1462-2920.13171	journal	January 2016
Petroleum hydrocarbon contamination, plant identity and arbuscular mycorrhizal fungal (AMF) community determine assemblages of the AMF spore-associated microbes: Assemblages of AMF and their spore-associated microbes Iffis, Bachir; St-Arnaud, Marc; Hijri, Mohamed Environmental Microbiology, Vol. 18, Issue 8 https://doi.org/10.1111/1462-2920.13438	journal	July 2016
Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions Zhang, Lin; Shi, Ning; Fan, Jiequn Environmental Microbiology, Vol. 20, Issue 7 https://doi.org/10.1111/1462-2920.14289	journal	July 2018
At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margarita provides insights into plant, endobacterial and fungal interactions Venice, Francesco; Ghignone, Stefano; Salvioli di Fossalunga, Alessandra Environmental Microbiology, Vol. 22, Issue 1 https://doi.org/10.1111/1462-2920.14827	journal	October 2019
Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments Wilson, Gail W. T.; Rice, Charles W.; Rillig, Matthias C. Ecology Letters, Vol. 12, Issue 5 https://doi.org/10.1111/j.1461-0248.2009.01303.x	journal	May 2009
The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with 32P and 33P Pearson, J. N.; Jakobsen, I. New Phytologist, Vol. 124, Issue 3 https://doi.org/10.1111/j.1469-8137.1993.tb03840.x	journal	July 1993
Mycorrhizas and soil structure Rillig, Matthias C.; Mummey, Daniel L. New Phytologist, Vol. 171, Issue 1 https://doi.org/10.1111/j.1469-8137.2006.01750.x	journal	July 2006
The mycorrhiza helper bacteria revisited Frey-Klett, P.; Garbaye, J.; Tarkka, M. New Phytologist, Vol. 176, Issue 1 https://doi.org/10.1111/j.1469-8137.2007.02191.x	journal	October 2007
The Roles of host Evolutionary Relationships (Genus: Nasonia) and Development in Structuring Microbial Communities: Divergence In Nasonia Microbial Communities Brucker, Robert M.; Bordenstein, Seth R. Evolution, Vol. 66, Issue 2 https://doi.org/10.1111/j.1558-5646.2011.01454.x	journal	October 2011
Phylogeny of arbuscular mycorrhizal fungi predicts community composition of symbiosis-associated bacteria: AMF-associated bacterial communities Rillig, Matthias C.; Mummey, Daniel L.; Ramsey, Philip W. FEMS Microbiology Ecology, Vol. 57, Issue 3 https://doi.org/10.1111/j.1574-6941.2006.00129.x	journal	September 2006
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
Microdiversity of Burkholderiales associated with mycorrhizal and nonmycorrhizal roots of Medicago truncatula: Bacterial diversity associated with mycorrhizal roots Offre, Pierre; Pivato, Barbara; Mazurier, Sylvie FEMS Microbiology Ecology, Vol. 65, Issue 2 https://doi.org/10.1111/j.1574-6941.2008.00504.x	journal	August 2008
Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial: Soil microbial communities in arable fields Toljander, Jonas F.; Santos-GonzÃ¡lez, Juan C.; Tehler, Anders FEMS Microbiology Ecology, Vol. 65, Issue 2 https://doi.org/10.1111/j.1574-6941.2008.00512.x	journal	August 2008
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
Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species Toljander, Jonas F.; Artursson, Veronica; Paul, Leslie R. FEMS Microbiology Letters, Vol. 254, Issue 1 https://doi.org/10.1111/j.1574-6968.2005.00003.x	journal	January 2006
Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation Kaiser, Christina; Kilburn, Matt R.; Clode, Peta L. New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13138	journal	November 2014
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
Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme ) and its bacterial endosymbionts Sun, Xuepeng; Chen, Wenbo; Ivanov, Sergey New Phytologist, Vol. 221, Issue 3 https://doi.org/10.1111/nph.15472	journal	October 2018
Why farmers should manage the arbuscular mycorrhizal symbiosis Rillig, Matthias C.; Aguilar‐Trigueros, Carlos A.; Camenzind, Tessa New Phytologist, Vol. 222, Issue 3 https://doi.org/10.1111/nph.15602	journal	January 2019
Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina Morin, Emmanuelle; Miyauchi, Shingo; San Clemente, Hélène New Phytologist, Vol. 222, Issue 3 https://doi.org/10.1111/nph.15687	journal	February 2019
Rapid Turnover of Hyphae of Mycorrhizal Fungi Determined by AMS Microanalysis of 14C Staddon, P. L. Science, Vol. 300, Issue 5622 https://doi.org/10.1126/science.1084269	journal	May 2003
Evolution of Mammals and Their Gut Microbes Ley, R. E.; Hamady, M.; Lozupone, C. Science, Vol. 320, Issue 5883 https://doi.org/10.1126/science.1155725	journal	June 2008
Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale Lauber, C. L.; Hamady, M.; Knight, R. Applied and Environmental Microbiology, Vol. 75, Issue 15 https://doi.org/10.1128/AEM.00335-09	journal	June 2009
Identification of Bacterial Groups Preferentially Associated with Mycorrhizal Roots of Medicago truncatula Offre, P.; Pivato, B.; Siblot, S. Applied and Environmental Microbiology, Vol. 73, Issue 3 https://doi.org/10.1128/AEM.02042-06	journal	December 2006
Growth of Chitinolytic Dune Soil β-SubclassProteobacteria in Response to Invading Fungal Hyphae De Boer, Wietse; Klein Gunnewiek, Paulien J. A.; Kowalchuk, George A. Applied and Environmental Microbiology, Vol. 67, Issue 8 https://doi.org/10.1128/AEM.67.8.3358-3362.2001	journal	August 2001
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
cDNA arrays as a tool to identify mycorrhiza-regulated genes: identification of mycorrhiza-induced genes that encode or generate signaling molecules implicated in the control of root growth Liu, Jinyuan; Blaylock, Laura A.; Harrison, Maria J. Canadian Journal of Botany, Vol. 82, Issue 8 https://doi.org/10.1139/b04-048	journal	August 2004
The genome of Rhizophagus clarus HR1 reveals a common genetic basis for auxotrophy among arbuscular mycorrhizal fungi Kobayashi, Yuuki; Maeda, Taro; Yamaguchi, Katsushi BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4853-0	journal	June 2018
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible McMurdie, Paul J.; Holmes, Susan PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003531	journal	April 2014
Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus Lin, Kui; Limpens, Erik; Zhang, Zhonghua PLoS Genetics, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pgen.1004078	journal	January 2014
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Plant Phylogeny and Life History Shape Rhizosphere Bacterial Microbiome of Summer Annuals in an Agricultural Field Emmett, Bryan D.; Youngblut, Nicholas D.; Buckley, Daniel H. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02414	journal	December 2017
Phosphate Uptake from Phytate Due to Hyphae-Mediated Phytase Activity by Arbuscular Mycorrhizal Maize Wang, Xin-Xin; Hoffland, Ellis; Feng, Gu Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00684	journal	April 2017

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