Plant Hosts Modify Belowground Microbial Community Response to Extreme Drought

Veach, Allison M.; Chen, Huaihai; Yang, Zamin Koo; Engle, Nancy L.; Tschaplinski, Timothy; Schadt, Christopher Warren; Cregger, Melissa

doi:10.1128/msystems.00092-20

Title: Plant Hosts Modify Belowground Microbial Community Response to Extreme Drought

Journal Article · Tue Jun 30 00:00:00 EDT 2020 · mSystems

DOI:https://doi.org/10.1128/msystems.00092-20· OSTI ID:1649570

^[1];

^[1]; Yang, Zamin Koo ^[1];

^[1];

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Drought stress negatively impacts microbial activity, yet the magnitude of stress responses is likely dependent on a diversity of belowground interactions. Populus trichocarpa individuals and no-plant bulk soils were exposed to extended drought (~0.03% gravimetric water content [GWC] after 12 days), rewet, and a 12-day “recovery” period to determine the effects of plant presence in mediating soil microbiome stability to water stress. Plant metabolomic analyses indicated that drought exposure increased host investment in C and N metabolic pathways (amino acids, fatty acids, phenolic glycosides) regardless of recovery. Several metabolites positively correlated with root-associated microbial alpha-diversity, but not those of soil communities. Soil bacterial community composition shifted with P. trichocarpa presence and with drought relative to irrigated controls, whereas soil fungal composition shifted only with plant presence. However, root fungal communities strongly shifted with drought, whereas root bacterial communities changed to a lesser degree. The proportion of bacterial water-stress opportunistic operational taxonomic units (OTUs) (enriched counts in drought) was high (~11%) at the end of drying phases and maintained after rewet and recovery phases in bulk soils, but it declined over time in soils with plants present. For root fungi, opportunistic OTUs were high at the end of recovery in drought treatments (~17% abundance), although relatively not responsive in soils, particularly planted soils (<0.5% abundance for sensitive or opportunistic). These data indicate that plants modulate soil and root-associated microbial drought responses via tight plant-microbe linkages during extreme drought scenarios, but trajectories after extreme drought vary with plant habitat and microbial functional groups.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

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

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1649570

Journal Information:: mSystems, Vol. 5, Issue 3; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait: Root bacteria protect plants from drought Rolli, Eleonora; Marasco, Ramona; Vigani, Gianpiero Environmental Microbiology, Vol. 17, Issue 2 https://doi.org/10.1111/1462-2920.12439	journal	March 2014
Plant host and drought shape the root associated fungal microbiota in rice Andreo-Jimenez, Beatriz; Vandenkoornhuyse, Philippe; Lê Van, Amandine PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7463	journal	January 2019
Drought-resistant fungi control soil organic matter decomposition and its response to temperature: FUNGAL DIVERSITY CONTROL OVER SOIL C BALANCE Yuste, J. C.; PeÑUelas, J.; Estiarte, M. Global Change Biology, Vol. 17, Issue 3 https://doi.org/10.1111/j.1365-2486.2010.02300.x	journal	September 2010
Climate change alters ecological strategies of soil bacteria Evans, Sarah E.; Wallenstein, Matthew D. Ecology Letters, Vol. 17, Issue 2 https://doi.org/10.1111/ele.12206	journal	November 2013
Interactive effects of drought and pathogens in forest trees Desprez-Loustau, Marie-Laure; Marçais, Benoit; Nageleisen, Louis-Michel Annals of Forest Science, Vol. 63, Issue 6 https://doi.org/10.1051/forest:2006040	journal	September 2006
Assembly and ecological function of the root microbiome across angiosperm plant species Fitzpatrick, Connor R.; Copeland, Julia; Wang, Pauline W. Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1717617115	journal	January 2018
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
Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides x Populus nigra Monclus, Romain; Dreyer, Erwin; Villar, Marc New Phytologist, Vol. 169, Issue 4 https://doi.org/10.1111/j.1469-8137.2005.01630.x	journal	February 2006
Practical innovations for high-throughput amplicon sequencing Lundberg, Derek S.; Yourstone, Scott; Mieczkowski, Piotr Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2634	journal	September 2013
Drought Stress Results in a Compartment-Specific Restructuring of the Rice Root-Associated Microbiomes Santos-Medellín, Christian; Edwards, Joseph; Liechty, Zachary mBio, Vol. 8, Issue 4 https://doi.org/10.1128/mBio.00764-17	journal	July 2017
Abiotic Stress Responses and Microbe-Mediated Mitigation in Plants: The Omics Strategies Meena, Kamlesh K.; Sorty, Ajay M.; Bitla, Utkarsh M. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00172	journal	February 2017
Plant root exudation under drought: implications for ecosystem functioning Williams, Alex; Vries, Franciska T. New Phytologist, Vol. 225, Issue 5 https://doi.org/10.1111/nph.16223	journal	October 2019
The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters Abarenkov, Kessy; Henrik Nilsson, R.; Larsson, Karl-Henrik New Phytologist, Vol. 186, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03160.x	journal	March 2010
Soil microbial responses to drought and exotic plants shift carbon metabolism Pérez Castro, Sherlynette; Cleland, Elsa E.; Wagner, Robert The ISME Journal, Vol. 13, Issue 7 https://doi.org/10.1038/s41396-019-0389-9	journal	March 2019
The potential distribution of bioenergy crops in Europe under present and future climate Tuck, Gill; Glendining, Margaret J.; Smith, Pete Biomass and Bioenergy, Vol. 30, Issue 3 https://doi.org/10.1016/j.biombioe.2005.11.019	journal	March 2006
Revisiting life strategy concepts in environmental microbial ecology Ho, Adrian; Lonardo, D. Paolo Di; Bodelier, Paul L. E. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fix006	journal	January 2017
Modern Applied Statistics with S Venables, W. N.; Ripley, B. D. Statistics and Computing https://doi.org/10.1007/978-0-387-21706-2	book	August 2002
Microbial Stress-Response Physiology and its Implications for Ecosystem Function Schimel, Joshua; Balser, Teri C.; Wallenstein, Matthew Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/06-0219	journal	June 2007
Modification of plant cell wall chemistry impacts metabolome and microbiome composition in Populus PdKOR1 RNAi plants Veach, Allison M.; Yip, Daniel; Engle, Nancy L. Plant and Soil, Vol. 429, Issue 1-2 https://doi.org/10.1007/s11104-018-3692-8	journal	June 2018
Effects of drought stress on photosynthesis, rhizosphere respiration, and fine-root characteristics of beech saplings: A rhizotron field study Zang, Ulrich; Goisser, Michael; Häberle, Karl-Heinz Journal of Plant Nutrition and Soil Science, Vol. 177, Issue 2 https://doi.org/10.1002/jpln.201300196	journal	October 2013
Mapping the niche space of soil microorganisms using taxonomy and traits Lennon, Jay T.; Aanderud, Zachary T.; Lehmkuhl, B. K. Ecology, Vol. 93, Issue 8 https://doi.org/10.1890/11-1745.1	journal	August 2012
Poplar as a feedstock for biofuels: A review of compositional characteristics Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A. Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2 https://doi.org/10.1002/bbb.206	journal	March 2010
Proline accumulation in plants: a review Verbruggen, Nathalie; Hermans, Christian Amino Acids, Vol. 35, Issue 4 https://doi.org/10.1007/s00726-008-0061-6	journal	April 2008
Plant-driven selection of microbes Hartmann, Anton; Schmid, Michael; Tuinen, Diederik van Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-008-9814-y	journal	November 2008
Drought increases the frequencies of fungal functional genes related to carbon and nitrogen acquisition Treseder, Kathleen K.; Berlemont, Renaud; Allison, Steven D. PLOS ONE, Vol. 13, Issue 11 https://doi.org/10.1371/journal.pone.0206441	journal	November 2018
Root Exudation and Rhizosphere Biology: Fig. 1. Walker, Travis S.; Bais, Harsh Pal; Grotewold, Erich Plant Physiology, Vol. 132, Issue 1 https://doi.org/10.1104/pp.102.019661	journal	May 2003
A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees Shakya, Migun; Gottel, Neil; Castro, Hector PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0076382	journal	October 2013
Biotic Interactions in the Rhizosphere: A Diverse Cooperative Enterprise for Plant Productivity De-la-Pena, C.; Loyola-Vargas, V. M. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.241810	journal	August 2014
Soil bacterial networks are less stable under drought than fungal networks de Vries, Franciska T.; Griffiths, Rob I.; Bailey, Mark Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05516-7	journal	August 2018
Non-parametric multivariate analyses of changes in community structure Clarke, K. R. Austral Ecology, Vol. 18, Issue 1 https://doi.org/10.1111/j.1442-9993.1993.tb00438.x	journal	March 1993
Abiotic Stresses Shift Belowground Populus-Associated Bacteria Toward a Core Stress Microbiome Timm, Collin M.; Carter, Kelsey R.; Carrell, Alyssa A. mSystems, Vol. 3, Issue 1 https://doi.org/10.1128/mSystems.00070-17	journal	January 2018
Climate change effects on beneficial plant-microorganism interactions: Climate change and beneficial plant-microorganism interactions Compant, Stéphane; Van Der Heijden, Marcel G. A.; Sessitsch, Angela FEMS Microbiology Ecology https://doi.org/10.1111/j.1574-6941.2010.00900.x	journal	May 2010
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
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
Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa Lebeis, S. L.; Paredes, S. H.; Lundberg, D. S. Science, Vol. 349, Issue 6250 https://doi.org/10.1126/science.aaa8764	journal	July 2015
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
Climate Trends and Global Crop Production Since 1980 Lobell, D. B.; Schlenker, W.; Costa-Roberts, J. Science, Vol. 333, Issue 6042 https://doi.org/10.1126/science.1204531	journal	May 2011
Genomics of cellulosic biofuels Rubin, Edward M. Nature, Vol. 454, Issue 7206 https://doi.org/10.1038/nature07190	journal	August 2008
How tree roots respond to drought Brunner, Ivano; Herzog, Claude; Dawes, Melissa A. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00547	journal	July 2015
Untangling the fungal niche: the trait-based approach Crowther, Thomas W.; Maynard, Daniel S.; Crowther, Terence R. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00579	journal	October 2014
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
Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin Veach, Allison M.; Morris, Reese; Yip, Daniel Z. Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0668-8	journal	May 2019
The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome Cregger, M. A.; Veach, A. M.; Yang, Z. K. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0413-8	journal	February 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
Permutation tests for univariate or multivariate analysis of variance and regression Anderson, Marti J. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 58, Issue 3 https://doi.org/10.1139/f01-004	journal	March 2001
Microbiome Datasets Are Compositional: And This Is Not Optional Gloor, Gregory B.; Macklaim, Jean M.; Pawlowsky-Glahn, Vera Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02224	journal	November 2017
The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts Courty, Pierre-Emmanuel; Buée, Marc; Diedhiou, Abdala Gamby Soil Biology and Biochemistry, Vol. 42, Issue 5 https://doi.org/10.1016/j.soilbio.2009.12.006	journal	May 2010
Bacillus subtilis Early Colonization of Arabidopsis thaliana Roots Involves Multiple Chemotaxis Receptors Allard-Massicotte, Rosalie; Tessier, Laurence; Lécuyer, Frédéric mBio, Vol. 7, Issue 6 https://doi.org/10.1128/mBio.01664-16	journal	November 2016
Opposite metabolic responses of shoots and roots to drought Gargallo-Garriga, Albert; Sardans, Jordi; Pérez-Trujillo, Míriam Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06829	journal	October 2014
Influence of extreme weather disasters on global crop production Lesk, Corey; Rowhani, Pedram; Ramankutty, Navin Nature, Vol. 529, Issue 7584 https://doi.org/10.1038/nature16467	journal	January 2016
Topographic position modulates the mycorrhizal response of oak trees to interannual rainfall variability Querejeta, JoséI.; Egerton-Warburton, Louise M.; Allen, Michael F. Ecology, Vol. 90, Issue 3 https://doi.org/10.1890/07-1696.1	journal	March 2009
Warming differentially influences the effects of drought on stoichiometry and metabolomics in shoots and roots Gargallo-Garriga, Albert; Sardans, Jordi; Pérez-Trujillo, Míriam New Phytologist, Vol. 207, Issue 3 https://doi.org/10.1111/nph.13377	journal	March 2015
Towards a holistic understanding of the beneficial interactions across the Populus microbiome Hacquard, Stéphane; Schadt, Christopher W. New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13133	journal	November 2014
Second generation bioenergy crops and climate change: a review of the effects of elevated atmospheric CO ₂ and drought on water use and the implications for yield Oliver, Rebecca J.; Finch, Jon W.; Taylor, Gail GCB Bioenergy, Vol. 1, Issue 2 https://doi.org/10.1111/j.1757-1707.2009.01011.x	journal	April 2009
Survival of Mycorrhiza Formed by Cenococcum Geophilum fr. in dry Soils Pigott, C. D. New Phytologist, Vol. 92, Issue 4 https://doi.org/10.1111/j.1469-8137.1982.tb03409.x	journal	December 1982
Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants Bonito, Gregory; Reynolds, Hannah; Robeson, Michael S. Molecular Ecology, Vol. 23, Issue 13 https://doi.org/10.1111/mec.12821	journal	June 2014
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
Drought and host selection influence bacterial community dynamics in the grass root microbiome Naylor, Dan; DeGraaf, Stephanie; Purdom, Elizabeth The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.118	journal	July 2017
Toward an Ecological Classification of soil Bacteria Fierer, Noah; Bradford, Mark A.; Jackson, Robert B. Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/05-1839	journal	June 2007

Similar Records

Chronic drought differentially alters the belowground microbiome of drought tolerant and drought susceptible genotypes of Populus trichocarpa

Journal Article · Wed Jul 13 00:00:00 EDT 2022 · Phytobiomes Journal · OSTI ID:1649570

Kristy, Brandon David; Carrell, Alyssa A.; Johnston, Eric R.; +7 more

Rapid remodeling of the soil lipidome in response to a drying-rewetting event

Journal Article · Mon Feb 27 00:00:00 EST 2023 · Microbiome · OSTI ID:1649570

Couvillion, Sneha P.; Danczak, Robert E.; Naylor, Dan; +15 more

Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin

Journal Article · Sat May 18 00:00:00 EDT 2019 · Microbiome · OSTI ID:1649570

Veach, Allison M.; Morris, Reese; Yip, Daniel Z.; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Plant Hosts Modify Belowground Microbial Community Response to Extreme Drought

Citation Formats

References (59)

Similar Records

Related Subjects