Plant-associated fungi support bacterial resilience following water limitation

Hestrin, Rachel; Kan, Megan; Lafler, Marissa; Wollard, Jessica; Kimbrel, Jeffrey A.; Ray, Prasun; Blazewicz, Steven J.; Stuart, Rhona; Craven, Kelly; Firestone, Mary; Nuccio, Erin E.; Pett-Ridge, Jennifer

doi:10.1038/s41396-022-01308-6

Plant-associated fungi support bacterial resilience following water limitation

Journal Article · Fri Sep 09 00:00:00 EDT 2022 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-022-01308-6· OSTI ID:1886421

; Kan, Megan; Lafler, Marissa; ; ; ; ; ; Craven, Kelly; Firestone, Mary; ;

Abstract

Drought disrupts soil microbial activity and many biogeochemical processes. Although plant-associated fungi can support plant performance and nutrient cycling during drought, their effects on nearby drought-exposed soil microbial communities are not well resolved. We used H218O quantitative stable isotope probing (qSIP) and 16S rRNA gene profiling to investigate bacterial community dynamics following water limitation in the hyphospheres of two distinct fungal lineages (Rhizophagus irregularis and Serendipita bescii) grown with the bioenergy model grass Panicum hallii. In uninoculated soil, a history of water limitation resulted in significantly lower bacterial growth potential and growth efficiency, as well as lower diversity in the actively growing bacterial community. In contrast, both fungal lineages had a protective effect on hyphosphere bacterial communities exposed to water limitation: bacterial growth potential, growth efficiency, and the diversity of the actively growing bacterial community were not suppressed by a history of water limitation in soils inoculated with either fungus. Despite their similar effects at the community level, the two fungal lineages did elicit different taxon-specific responses, and bacterial growth potential was greater in R. irregularis compared to S. bescii-inoculated soils. Several of the bacterial taxa that responded positively to fungal inocula belong to lineages that are considered drought susceptible. Overall, H218O qSIP highlighted treatment effects on bacterial community structure that were less pronounced using traditional 16S rRNA gene profiling. Together, these results indicate that fungal–bacterial synergies may support bacterial resilience to moisture limitation.

View Journal Article

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

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

Grant/Contract Number:: AC52-07NA27344; SC0014079

OSTI ID:: 1886421

Alternate ID(s):: OSTI ID: 2472054

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 12 Vol. 16; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (89)

Estimating taxon‐specific population dynamics in diverse microbial communities Koch, Benjamin J.; McHugh, Theresa A.; Hayer, Michaela Ecosphere, Vol. 9, Issue 1 https://doi.org/10.1002/ecs2.2090	journal	January 2018
Widespread co‐occurrence of Sebacinales and arbuscular mycorrhizal fungi in switchgrass roots and soils has limited dependence on soil carbon or nutrients Lee, Marissa R.; Hawkes, Christine V. PLANTS, PEOPLE, PLANET, Vol. 3, Issue 5 https://doi.org/10.1002/ppp3.10181	journal	January 2021
Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions Birhane, Emiru; Sterck, Frank J.; Fetene, Masresha Oecologia, Vol. 169, Issue 4 https://doi.org/10.1007/s00442-012-2258-3	journal	January 2012
Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies Ruiz-Lozano, Juan Manuel Mycorrhiza, Vol. 13, Issue 6 https://doi.org/10.1007/s00572-003-0237-6	journal	December 2003
Molecular diagnostic toolkit for Rhizophagus irregularis isolate DAOM-197198 using quantitative PCR assay targeting the mitochondrial genome Badri, Amine; Stefani, Franck O. P.; Lachance, Geneviève Mycorrhiza, Vol. 26, Issue 7 https://doi.org/10.1007/s00572-016-0708-1	journal	May 2016
Utilization of organic nitrogen by arbuscular mycorrhizal fungi—is there a specific role for protists and ammonia oxidizers? Bukovská, Petra; Bonkowski, Michael; Konvalinková, Tereza Mycorrhiza, Vol. 28, Issue 3 https://doi.org/10.1007/s00572-018-0825-0	journal	February 2018
Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almeriense-Terfezia claveryi Morte, A.; Lovisolo, C.; Schubert, A. Mycorrhiza, Vol. 10, Issue 3 https://doi.org/10.1007/s005720000066	journal	December 2000
A Novel Delivery System for the Root Symbiotic Fungus, Sebacina vermifera, and Consequent Biomass Enhancement of Low Lignin COMT Switchgrass Lines Ray, Prasun; Ishiga, Takako; Decker, Stephen R. BioEnergy Research, Vol. 8, Issue 3 https://doi.org/10.1007/s12155-015-9636-8	journal	June 2015
Effects of Glomus intraradices on the growth and reactive oxygen metabolism of foxtail millet under drought Gong, Minggui; You, Xiaoyan; Zhang, Qiaoming Annals of Microbiology, Vol. 65, Issue 1 https://doi.org/10.1007/s13213-014-0895-y	journal	April 2014
Conditional outcomes in mutualistic interactions Bronstein, Judith L. Trends in Ecology & Evolution, Vol. 9, Issue 6 https://doi.org/10.1016/0169-5347(94)90246-1	journal	June 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
Determination of the base composition of deoxyribonucleic acid from its buoyant density in CsCl Schildkraut, Carl L.; Marmur, Julius; Doty, Paul Journal of Molecular Biology, Vol. 4, Issue 6 https://doi.org/10.1016/S0022-2836(62)80100-4	journal	June 1962
Interactions of arbuscular-mycorrhizal fungi and Bacillus strains and their effects on plant growth, microbial rhizosphere activity (thymidine and leucine incorporation) and fungal biomass (ergosterol and chitin) Medina, A.; Probanza, A.; Gutierrez Mañero, F. J. Applied Soil Ecology, Vol. 22, Issue 1 https://doi.org/10.1016/S0929-1393(02)00112-9	journal	January 2003
Bias and artifacts in multitemplate polymerase chain reactions (PCR) Kanagawa, Takahiro Journal of Bioscience and Bioengineering, Vol. 96, Issue 4 https://doi.org/10.1016/S1389-1723(03)90130-7	journal	January 2003
Predominant bacterial and fungal assemblages in agricultural soils during a record drought/heat wave and linkages to enzyme activities of biogeochemical cycling Acosta-Martínez, V.; Cotton, J.; Gardner, T. Applied Soil Ecology, Vol. 84 https://doi.org/10.1016/j.apsoil.2014.06.005	journal	December 2014
Real-time PCR and microscopy: Are the two methods measuring the same unit of arbuscular mycorrhizal fungal abundance? Gamper, Hannes A.; Young, J. Peter W.; Jones, David L. Fungal Genetics and Biology, Vol. 45, Issue 5 https://doi.org/10.1016/j.fgb.2007.09.007	journal	May 2008
Microbiota accompanying different arbuscular mycorrhizal fungal isolates influence soil aggregation Rillig, Matthias C.; Lutgen, Emily R.; Ramsey, Philip W. Pedobiologia, Vol. 49, Issue 3 https://doi.org/10.1016/j.pedobi.2004.11.003	journal	June 2005
Crop yield sensitivity of global major agricultural countries to droughts and the projected changes in the future Leng, Guoyong; Hall, Jim Science of The Total Environment, Vol. 654 https://doi.org/10.1016/j.scitotenv.2018.10.434	journal	March 2019
Changes in variability of soil moisture alter microbial community C and N resource use Tiemann, Lisa K.; Billings, Sharon A. Soil Biology and Biochemistry, Vol. 43, Issue 9 https://doi.org/10.1016/j.soilbio.2011.04.020	journal	September 2011
Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils Hueso, S.; García, C.; Hernández, T. Soil Biology and Biochemistry, Vol. 50 https://doi.org/10.1016/j.soilbio.2012.03.026	journal	July 2012
Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland Alster, Charlotte J.; German, Donovan P.; Lu, Ying Soil Biology and Biochemistry, Vol. 64 https://doi.org/10.1016/j.soilbio.2013.03.034	journal	September 2013
Arbuscular mycorrhizal fungi reduce decomposition of woody plant litter while increasing soil aggregation Leifheit, E. F.; Verbruggen, E.; Rillig, M. C. Soil Biology and Biochemistry, Vol. 81 https://doi.org/10.1016/j.soilbio.2014.12.003	journal	February 2015
Clarifying the interpretation of carbon use efficiency in soil through methods comparison Geyer, Kevin M.; Dijkstra, Paul; Sinsabaugh, Robert Soil Biology and Biochemistry, Vol. 128 https://doi.org/10.1016/j.soilbio.2018.09.036	journal	January 2019
Microbial extracellular polysaccharide production and aggregate stability controlled by switchgrass (Panicum virgatum) root biomass and soil water potential Sher, Yonatan; Baker, Nameer R.; Herman, Don Soil Biology and Biochemistry, Vol. 143 https://doi.org/10.1016/j.soilbio.2020.107742	journal	April 2020
A phylum level perspective on bacterial cell envelope architecture Sutcliffe, Iain C. Trends in Microbiology, Vol. 18, Issue 10 https://doi.org/10.1016/j.tim.2010.06.005	journal	October 2010
Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra Zhang, Lin; Zhou, Jiachao; George, Timothy S. Trends in Plant Science, Vol. 27, Issue 4 https://doi.org/10.1016/j.tplants.2021.10.008	journal	April 2022
An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material Hodge, Angela; Campbell, Colin D.; Fitter, Alastair H. Nature, Vol. 413, Issue 6853 https://doi.org/10.1038/35095041	journal	September 2001
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
Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought Bouskill, Nicholas J.; Lim, Hsiao Chien; Borglin, Sharon The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.113	journal	November 2012
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.104	journal	July 2013
Optimization of lag time underlies antibiotic tolerance in evolved bacterial populations Fridman, Ofer; Goldberg, Amir; Ronin, Irine Nature, Vol. 513, Issue 7518 https://doi.org/10.1038/nature13469	journal	June 2014
Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes Kozarewa, Iwanka; Ning, Zemin; Quail, Michael A. Nature Methods, Vol. 6, Issue 4 https://doi.org/10.1038/nmeth.1311	journal	March 2009
Relic DNA is abundant in soil and obscures estimates of soil microbial diversity Carini, Paul; Marsden, Patrick J.; Leff, Jonathan W. Nature Microbiology, Vol. 2, Issue 3 https://doi.org/10.1038/nmicrobiol.2016.242	journal	December 2016
DNA stable-isotope probing Neufeld, Josh D.; Vohra, Jyotsna; Dumont, Marc G. Nature Protocols, Vol. 2, Issue 4 https://doi.org/10.1038/nprot.2007.109	journal	April 2007
Sporulation, bacterial cell envelopes and the origin of life Tocheva, Elitza I.; Ortega, Davi R.; Jensen, Grant J. Nature Reviews Microbiology, Vol. 14, Issue 8 https://doi.org/10.1038/nrmicro.2016.85	journal	June 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
Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change Malik, Ashish A.; Martiny, Jennifer B. H.; Brodie, Eoin L. The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396-019-0510-0	journal	September 2019
Environmental stress destabilizes microbial networks Hernandez, Damian J.; David, Aaron S.; Menges, Eric S. The ISME Journal, Vol. 15, Issue 6 https://doi.org/10.1038/s41396-020-00882-x	journal	January 2021
Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil Blazewicz, Steven J.; Hungate, Bruce A.; Koch, Benjamin J. The ISME Journal, Vol. 14, Issue 6 https://doi.org/10.1038/s41396-020-0617-3	journal	March 2020
Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi Emmett, Bryan D.; Lévesque-Tremblay, Véronique; Harrison, Maria J. The ISME Journal, Vol. 15, Issue 8 https://doi.org/10.1038/s41396-021-00920-2	journal	March 2021
Drought drives rapid shifts in tropical rainforest soil biogeochemistry and greenhouse gas emissions O’Connell, Christine S.; Ruan, Leilei; Silver, Whendee L. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03352-3	journal	April 2018
Microbial diversity drives carbon use efficiency in a model soil Domeignoz-Horta, Luiz A.; Pold, Grace; Liu, Xiao-Jun Allen Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17502-z	journal	July 2020
Prolonged drought imparts lasting compositional changes to the rice root microbiome Santos-Medellín, Christian; Liechty, Zachary; Edwards, Joseph Nature Plants, Vol. 7, Issue 8 https://doi.org/10.1038/s41477-021-00967-1	journal	July 2021
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
Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2 Drigo, B.; Pijl, A. S.; Duyts, H. Proceedings of the National Academy of Sciences, Vol. 107, Issue 24 https://doi.org/10.1073/pnas.0912421107	journal	June 2010
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
Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria Xu, Ling; Naylor, Dan; Dong, Zhaobin Proceedings of the National Academy of Sciences, Vol. 115, Issue 18 https://doi.org/10.1073/pnas.1717308115	journal	April 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
Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought Duan, Xiangrong; Neuman, Dawn S.; Reiber, Janet M. Journal of Experimental Botany, Vol. 47, Issue 10 https://doi.org/10.1093/jxb/47.10.1541	journal	January 1996
Genome Sequence of the Plant Growth Promoting Fungus Serendipita vermifera subsp. bescii : The First Native Strain from North America Ray, Prasun; Chi, Myoung-Hwan; Guo, Yingqing Phytobiomes Journal, Vol. 2, Issue 2 https://doi.org/10.1094/PBIOMES-04-17-0017-A	journal	January 2018
Linking diversity, synchrony and stability in soil microbial communities Wagg, Cameron; Dudenhöffer, Jan-Hendrik; Widmer, Franco Functional Ecology, Vol. 32, Issue 5 https://doi.org/10.1111/1365-2435.13056	journal	February 2018
Do arbuscular mycorrhizal fungi stabilize litter-derived carbon in soil? Verbruggen, Erik; Jansa, Jan; Hammer, Edith C. Journal of Ecology, Vol. 104, Issue 1 https://doi.org/10.1111/1365-2745.12496	journal	November 2015
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
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
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
Serendipita bescii promotes winter wheat growth and modulates the host root transcriptome under phosphorus and nitrogen starvation Ray, Prasun; Guo, Yingqing; Chi, Myoung‐Hwan Environmental Microbiology https://doi.org/10.1111/1462-2920.15242	journal	October 2020
Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization See, Craig R.; Keller, Adrienne B.; Hobbie, Sarah E. Global Change Biology, Vol. 28, Issue 8 https://doi.org/10.1111/gcb.16073	journal	January 2022
Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants Jakobsen, I.; Rosendahl, L. New Phytologist, Vol. 115, Issue 1 https://doi.org/10.1111/j.1469-8137.1990.tb00924.x	journal	May 1990
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
Environmental and stoichiometric controls on microbial carbon-use efficiency in soils: Research review Manzoni, Stefano; Taylor, Philip; Richter, Andreas New Phytologist, Vol. 196, Issue 1 https://doi.org/10.1111/j.1469-8137.2012.04225.x	journal	July 2012
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
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
Effects of selected root exudate components on soil bacterial communities: Root exudate components and soil microbial communities Shi, Shengjing; Richardson, Alan E.; O'Callaghan, Maureen FEMS Microbiology Ecology, Vol. 77, Issue 3 https://doi.org/10.1111/j.1574-6941.2011.01150.x	journal	July 2011
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
The importance of being persistent: heterogeneity of bacterial populations under antibiotic stress Gefen, Orit; Balaban, Nathalie Q. FEMS Microbiology Reviews, Vol. 33, Issue 4 https://doi.org/10.1111/j.1574-6976.2008.00156.x	journal	July 2009
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
Biology and evolution of arbuscular mycorrhizal symbiosis in the light of genomics Kamel, Laurent; Keller-Pearson, Michelle; Roux, Christophe New Phytologist, Vol. 213, Issue 2 https://doi.org/10.1111/nph.14263	journal	October 2016
Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae Jiang, Feiyan; Zhang, Lin; Zhou, Jiachao New Phytologist, Vol. 230, Issue 1 https://doi.org/10.1111/nph.17081	journal	January 2021
Harnessing rhizosphere microbiomes for drought-resilient crop production de Vries, Franciska T.; Griffiths, Rob I.; Knight, Christopher G. Science, Vol. 368, Issue 6488 https://doi.org/10.1126/science.aaz5192	journal	April 2020
Suitability of Quantitative Real-Time PCR To Estimate the Biomass of Fungal Root Endophytes Tellenbach, Christoph; Grünig, Christoph R.; Sieber, Thomas N. Applied and Environmental Microbiology, Vol. 76, Issue 17 https://doi.org/10.1128/AEM.00907-10	journal	September 2010
Quantitative Microbial Ecology through Stable Isotope Probing Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert Applied and Environmental Microbiology, Vol. 81, Issue 21 https://doi.org/10.1128/AEM.02280-15	journal	August 2015
Stable Isotope Probing with 15N Achieved by Disentangling the Effects of Genome G+C Content and Isotope Enrichment on DNA Density Buckley, D. H.; Huangyutitham, V.; Hsu, S. -F. Applied and Environmental Microbiology, Vol. 73, Issue 10 https://doi.org/10.1128/AEM.02609-06	journal	March 2007
Enhancement of Switchgrass (Panicum virgatum L.) Biomass Production under Drought Conditions by the Ectomycorrhizal Fungus Sebacina vermifera Ghimire, Sita R.; Craven, Kelly D. Applied and Environmental Microbiology, Vol. 77, Issue 19 https://doi.org/10.1128/AEM.05225-11	journal	August 2011
DNA Extraction from Soils: Old Bias for New Microbial Diversity Analysis Methods Martin-Laurent, F.; Philippot, L.; Hallet, S. Applied and Environmental Microbiology, Vol. 67, Issue 5 https://doi.org/10.1128/AEM.67.5.2354-2359.2001	journal	May 2001
Effects of arbuscular-mycorrhizal glomus species on drought tolerance: physiological and nutritional plant responses Ruiz-Lozano, J. M.; Azcon, R.; Gomez, M. Applied and Environmental Microbiology, Vol. 61, Issue 2 https://doi.org/10.1128/aem.61.2.456-460.1995	journal	February 1995
How, When, and Where Relic DNA Affects Microbial Diversity Lennon, J. T.; Muscarella, M. E.; Placella, S. A. mBio, Vol. 9, Issue 3 https://doi.org/10.1128/mBio.00637-18	journal	June 2018
Different Arbuscular Mycorrhizal Fungi Cocolonizing on a Single Plant Root System Recruit Distinct Microbiomes Zhou, Jiachao; Chai, Xiaofen; Zhang, Lin mSystems, Vol. 5, Issue 6 https://doi.org/10.1128/mSystems.00929-20	journal	December 2020
Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes Schimel, Joshua P. Annual Review of Ecology, Evolution, and Systematics, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110617-062614	journal	November 2018
Correcting for 16S rRNA gene copy numbers in microbiome surveys remains an unsolved problem Louca, Stilianos; Doebeli, Michael; Parfrey, Laura Wegener Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0420-9	journal	February 2018
Arbuscular mycorrhizal fungal spores host bacteria that affect nutrient biodynamics and biocontrol of soil-borne plant pathogens Cruz, Andre Freire; Ishii, Takaaki Biology Open, Vol. 1, Issue 1 https://doi.org/10.1242/bio.2011014	journal	November 2011
Root Exudation of Phytochemicals in Arabidopsis Follows Specific Patterns That Are Developmentally Programmed and Correlate with Soil Microbial Functions Chaparro, Jacqueline M.; Badri, Dayakar V.; Bakker, Matthew G. PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0055731	journal	February 2013
Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica Zuccaro, Alga; Lahrmann, Urs; Güldener, Ulrich PLoS Pathogens, Vol. 7, Issue 10 https://doi.org/10.1371/journal.ppat.1002290	journal	October 2011
Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil Blazewicz, Steven J.; Schwartz, Egbert; Firestone, Mary K. Ecology, Vol. 95, Issue 5 https://doi.org/10.1890/13-1031.1	journal	May 2014
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton Apprill, A.; McNally, S.; Parsons, R. Aquatic Microbial Ecology, Vol. 75, Issue 2 https://doi.org/10.3354/ame01753	journal	June 2015
The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe Dias, Teresa; Pimentel, Vívian; Cogo, Antônio Jesus Dorighetto Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.562238	journal	September 2020
Effects of Rhizophagus irregularis on Photosynthesis and Antioxidative Enzymatic System in Robinia pseudoacacia L. under Drought Stress He, Fei; Sheng, Min; Tang, Ming Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00183	journal	February 2017
Drought Stress and Root-Associated Bacterial Communities Naylor, Dan; Coleman-Derr, Devin Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02223	journal	January 2018

Similar Records

Plant Hosts Modify Belowground Microbial Community Response to Extreme Drought

Journal Article · Mon Jun 29 20:00:00 EDT 2020 · mSystems · OSTI ID:1649570

Related Subjects

54 ENVIRONMENTAL SCIENCES
Biological Sciences
Environmental Sciences & Ecology
Microbial Ecology
Microbiology
Science and Mathematics

Plant-associated fungi support bacterial resilience following water limitation

Citation Formats

References (89)

Similar Records

Related Subjects