Depth matters: effects of precipitation regime on soil microbial activity upon rewetting of a plant-soil system
Abstract
Changes in frequency and amplitude of rain events, that is, precipitation patterns, result in different water conditions with soil depth, and likely affect plant growth and shape plant and soil microbial activity. Here, we used 18O stable isotope probing (SIP) to investigate bacterial and fungal communities that actively grew or not upon rewetting, at three different depths in soil mesocosms previously subjected to frequent or infrequent watering for 12 weeks (equal total water input). Phylogenetic marker genes for bacteria and fungi were sequenced after rewetting, and plant-soil microbial coupling documented by plant 13C-CO2 labeling. Soil depth, rather than precipitation pattern, was most influential in shaping microbial response to rewetting, and had differential effects on active and inactive bacterial and fungal communities. After rewetting, active bacterial communities were less rich, more even and phylogenetically related than the inactive, and reactivated throughout the soil profile. Active fungal communities after rewetting were less abundant and rich than the inactive. The coupling between plants and soil microbes decreased under infrequent watering in the top soil layer. In conclusion, we suggest that differences in fungal and bacterial abundance and relative activity could result in large effects on subsequent soil biogeochemical cycling.
- Authors:
-
- Univ. Bourgogne Franche-Comte, Dijon (France)
- Univ. Bourgogne Franche-Comte, Dijon (France); Iowa State Univ., Ames, IA (United States)
- Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
- Swiss Federal Research Institute WSL, Birmensdorf (Switzerland)
- Univ. Politecnica de Madrid, Madrid (Spain)
- Publication Date:
- Research Org.:
- Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA)
- OSTI Identifier:
- 1474362
- Report Number(s):
- LLNL-JRNL-738625
Journal ID: ISSN 1751-7362; 891882
- Grant/Contract Number:
- AC52-07NA27344
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 12; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Engelhardt, Ilonka C., Welty, Amy, Blazewicz, Steven J., Bru, David, Rouard, Nadine, Breuil, Marie -Christine, Gessler, Arthur, Galiano, Lucía, Miranda, José Carlos, Spor, Aymé, and Barnard, Romain L. Depth matters: effects of precipitation regime on soil microbial activity upon rewetting of a plant-soil system. United States: N. p., 2018.
Web. doi:10.1038/s41396-018-0079-z.
Engelhardt, Ilonka C., Welty, Amy, Blazewicz, Steven J., Bru, David, Rouard, Nadine, Breuil, Marie -Christine, Gessler, Arthur, Galiano, Lucía, Miranda, José Carlos, Spor, Aymé, & Barnard, Romain L. Depth matters: effects of precipitation regime on soil microbial activity upon rewetting of a plant-soil system. United States. https://doi.org/10.1038/s41396-018-0079-z
Engelhardt, Ilonka C., Welty, Amy, Blazewicz, Steven J., Bru, David, Rouard, Nadine, Breuil, Marie -Christine, Gessler, Arthur, Galiano, Lucía, Miranda, José Carlos, Spor, Aymé, and Barnard, Romain L. Fri .
"Depth matters: effects of precipitation regime on soil microbial activity upon rewetting of a plant-soil system". United States. https://doi.org/10.1038/s41396-018-0079-z. https://www.osti.gov/servlets/purl/1474362.
@article{osti_1474362,
title = {Depth matters: effects of precipitation regime on soil microbial activity upon rewetting of a plant-soil system},
author = {Engelhardt, Ilonka C. and Welty, Amy and Blazewicz, Steven J. and Bru, David and Rouard, Nadine and Breuil, Marie -Christine and Gessler, Arthur and Galiano, Lucía and Miranda, José Carlos and Spor, Aymé and Barnard, Romain L.},
abstractNote = {Changes in frequency and amplitude of rain events, that is, precipitation patterns, result in different water conditions with soil depth, and likely affect plant growth and shape plant and soil microbial activity. Here, we used 18O stable isotope probing (SIP) to investigate bacterial and fungal communities that actively grew or not upon rewetting, at three different depths in soil mesocosms previously subjected to frequent or infrequent watering for 12 weeks (equal total water input). Phylogenetic marker genes for bacteria and fungi were sequenced after rewetting, and plant-soil microbial coupling documented by plant 13C-CO2 labeling. Soil depth, rather than precipitation pattern, was most influential in shaping microbial response to rewetting, and had differential effects on active and inactive bacterial and fungal communities. After rewetting, active bacterial communities were less rich, more even and phylogenetically related than the inactive, and reactivated throughout the soil profile. Active fungal communities after rewetting were less abundant and rich than the inactive. The coupling between plants and soil microbes decreased under infrequent watering in the top soil layer. In conclusion, we suggest that differences in fungal and bacterial abundance and relative activity could result in large effects on subsequent soil biogeochemical cycling.},
doi = {10.1038/s41396-018-0079-z},
journal = {The ISME Journal},
number = ,
volume = 12,
place = {United States},
year = {2018},
month = {2}
}
Web of Science
Figures / Tables:

Works referenced in this record:
Dry Season Constrains Bacterial Phylogenetic Diversity in a Semi-Arid Rhizosphere System
journal, August 2016
- Taketani, Rodrigo Gouvêa; Lançoni, Milena Duarte; Kavamura, Vanessa Nessner
- Microbial Ecology, Vol. 73, Issue 1
Drying–Rewetting Cycles Affect Fungal and Bacterial Growth Differently in an Arable Soil
journal, July 2010
- Bapiri, Azadeh; Bååth, Erland; Rousk, Johannes
- Microbial Ecology, Vol. 60, Issue 2
Desiccation of sediments affects assimilate transport within aquatic plants and carbon transfer to microorganisms
journal, August 2016
- von Rein, I.; Kayler, Z. E.; Premke, K.
- Plant Biology, Vol. 18, Issue 6
The immediate and prolonged effects of climate extremes on soil respiration in a mesic grassland: Soil Respiration and Climate Extremes
journal, April 2016
- Hoover, David L.; Knapp, Alan K.; Smith, Melinda D.
- Journal of Geophysical Research: Biogeosciences, Vol. 121, Issue 4
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting
journal, July 2013
- Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K.
- The ISME Journal, Vol. 7, Issue 11
Drying and rewetting effects on soil microbial community composition and nutrient leaching
journal, February 2008
- Gordon, Helen; Haygarth, Philip M.; Bardgett, Richard D.
- Soil Biology and Biochemistry, Vol. 40, Issue 2
Phylogenetic organization of bacterial activity
journal, March 2016
- Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
- The ISME Journal, Vol. 10, Issue 9
Stability of above-ground and below-ground processes to extreme drought in model grassland ecosystems: Interactions with plant species diversity and soil nitrogen availability
journal, June 2012
- Bloor, Juliette M. G.; Bardgett, Richard D.
- Perspectives in Plant Ecology, Evolution and Systematics, Vol. 14, Issue 3
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups
journal, June 2012
- Placella, S. A.; Brodie, E. L.; Firestone, M. K.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
Land use alters the resistance and resilience of soil food webs to drought
journal, January 2012
- de Vries, Franciska T.; Liiri, Mira E.; Bjørnlund, Lisa
- Nature Climate Change, Vol. 2, Issue 4
High-resolution isotope measurements resolve rapid ecohydrological dynamics at the soil-plant interface
journal, February 2016
- Volkmann, Till H. M.; Haberer, Kristine; Gessler, Arthur
- New Phytologist, Vol. 210, Issue 3
Impacts of altered precipitation regimes on soil communities and biogeochemistry in arid and semi-arid ecosystems
journal, December 2014
- Nielsen, Uffe N.; Ball, Becky A.
- Global Change Biology, Vol. 21, Issue 4
Prolonged summer droughts retard soil N processing and stabilization in organo-mineral fractions
journal, January 2014
- Bimüller, Carolin; Dannenmann, Michael; Tejedor, Javier
- Soil Biology and Biochemistry, Vol. 68
Vertical distribution of fungal communities in tallgrass prairie soil
journal, September 2010
- Jumpponen, Ari; Jones, Kenneth L.; Blair, John
- Mycologia, Vol. 102, Issue 5
Hydration dynamics promote bacterial coexistence on rough surfaces
journal, October 2012
- Wang, Gang; Or, Dani
- The ISME Journal, Vol. 7, Issue 2
Active and total prokaryotic communities in dryland soils
journal, June 2013
- Angel, Roey; Pasternak, Zohar; Soares, M. Ines M.
- FEMS Microbiology Ecology, Vol. 86, Issue 1
Exploring the Phylogenetic Structure of Ecological Communities: An Example for Rain Forest Trees
journal, August 2000
- Webb, Campbell O.
- The American Naturalist, Vol. 156, Issue 2
Forest understory plant and soil microbial response to an experimentally induced drought and heat-pulse event: the importance of maintaining the continuum
journal, April 2016
- von Rein, Isabell; Gessler, Arthur; Premke, Katrin
- Global Change Biology, Vol. 22, Issue 8
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
PEAR: a fast and accurate Illumina Paired-End reAd mergeR
journal, October 2013
- Zhang, J.; Kobert, K.; Flouri, T.
- Bioinformatics, Vol. 30, Issue 5
Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil
journal, July 2012
- Eilers, Kathryn G.; Debenport, Spencer; Anderson, Suzanne
- Soil Biology and Biochemistry, Vol. 50
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009
- Price, M. N.; Dehal, P. S.; Arkin, A. P.
- Molecular Biology and Evolution, Vol. 26, Issue 7
Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter?
journal, September 2011
- Evans, Sarah E.; Wallenstein, Matthew D.
- Biogeochemistry, Vol. 109, Issue 1-3
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005
- Lozupone, C.; Knight, R.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Stable isotope analysis of organic carbon in small (µg C) samples and dissolved organic matter using a GasBench preparation device: δ13C of organic compounds by GasBench
journal, December 2011
- Lang, Susan Q.; Bernasconi, Stefano M.; Früh-Green, Gretchen L.
- Rapid Communications in Mass Spectrometry, Vol. 26, Issue 1
Drought effects on allocation of recent carbon: from beech leaves to soil CO2 efflux
journal, October 2009
- Ruehr, Nadine K.; Offermann, Christine A.; Gessler, Arthur
- New Phytologist, Vol. 184, Issue 4
Drought history affects grassland plant and microbial carbon turnover during and after a subsequent drought event
journal, May 2016
- Fuchslueger, Lucia; Bahn, Michael; Hasibeder, Roland
- Journal of Ecology, Vol. 104, Issue 5
Controls on soil microbial community stability under climate change
journal, January 2013
- de Vries, Franciska T.; Shade, Ashley
- Frontiers in Microbiology, Vol. 4
Drought-resistant fungi control soil organic matter decomposition and its response to temperature: FUNGAL DIVERSITY CONTROL OVER SOIL C BALANCE
journal, September 2010
- Yuste, J. C.; PeÑUelas, J.; Estiarte, M.
- Global Change Biology, Vol. 17, Issue 3
PyNAST: a flexible tool for aligning sequences to a template alignment
journal, November 2009
- Caporaso, J. G.; Bittinger, K.; Bushman, F. D.
- Bioinformatics, Vol. 26, Issue 2
Prediction of soil water retention properties after stratification by combining texture, bulk density and the type of horizon
journal, December 2008
- Al Majou, H.; Bruand, A.; Duval, O.
- Soil Use and Management, Vol. 24, Issue 4
Altered precipitation regime affects the function and composition of soil microbial communities on multiple time scales
journal, October 2013
- Zeglin, L. H.; Bottomley, P. J.; Jumpponen, A.
- Ecology, Vol. 94, Issue 10
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011
- McDonald, Daniel; Price, Morgan N.; Goodrich, Julia
- The ISME Journal, Vol. 6, Issue 3
Seasonal Effects Stronger than Three-Year Climate Manipulation on Grassland Soil Microbial Community
journal, January 2015
- Slaughter, Lindsey C.; Weintraub, Michael N.; McCulley, Rebecca L.
- Soil Science Society of America Journal, Vol. 79, Issue 5
Hydration-controlled bacterial motility and dispersal on surfaces
journal, July 2010
- Dechesne, A.; Wang, G.; Gulez, G.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 32
Changing precipitation pattern alters soil microbial community response to wet-up under a Mediterranean-type climate
journal, October 2014
- Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K.
- The ISME Journal, Vol. 9, Issue 4
Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling
journal, February 2015
- Canarini, Alberto; Dijkstra, Feike A.
- Soil Biology and Biochemistry, Vol. 81
The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters
journal, March 2010
- Abarenkov, Kessy; Henrik Nilsson, R.; Larsson, Karl-Henrik
- New Phytologist, Vol. 186, Issue 2
Phylogenies and Community Ecology
journal, November 2002
- Webb, Campbell O.; Ackerly, David D.; McPeek, Mark A.
- Annual Review of Ecology and Systematics, Vol. 33, Issue 1
Effects of simulated drought and nitrogen fertilizer on plant productivity and nitrous oxide (N2O) emissions of two pastures
journal, May 2012
- Hartmann, Adrian A.; Niklaus, Pascal A.
- Plant and Soil, Vol. 361, Issue 1-2
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Living in a fungal world: impact of fungi on soil bacterial niche development
journal, September 2005
- Boer, Wietse de; Folman, Larissa B.; Summerbell, Richard C.
- FEMS Microbiology Reviews, Vol. 29, Issue 4
An extraction method for measuring soil microbial biomass C
journal, January 1987
- Vance, E. D.; Brookes, P. C.; Jenkinson, D. S.
- Soil Biology and Biochemistry, Vol. 19, Issue 6
Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow
journal, October 2013
- Fuchslueger, Lucia; Bahn, Michael; Fritz, Karina
- New Phytologist, Vol. 201, Issue 3
VSEARCH: a versatile open source tool for metagenomics
journal, January 2016
- Rognes, Torbjørn; Flouri, Tomáš; Nichols, Ben
- PeerJ, Vol. 4
Development of a Prokaryotic Universal Primer for Simultaneous Analysis of Bacteria and Archaea Using Next-Generation Sequencing
journal, August 2014
- Takahashi, Shunsuke; Tomita, Junko; Nishioka, Kaori
- PLoS ONE, Vol. 9, Issue 8
Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils
journal, October 2008
- Sowerby, Alwyn; Emmett, Bridget A.; Tietema, Albert
- Global Change Biology, Vol. 14, Issue 10
Dynamics of 18O Incorporation from H 2 18O into Soil Microbial DNA
journal, March 2011
- Blazewicz, Steven J.; Schwartz, Egbert
- Microbial Ecology, Vol. 61, Issue 4
Summer drought alters carbon allocation to roots and root respiration in mountain grassland
journal, November 2014
- Hasibeder, Roland; Fuchslueger, Lucia; Richter, Andreas
- New Phytologist, Vol. 205, Issue 3
Tallgrass prairie soil fungal communities are resilient to climate change
journal, August 2014
- Jumpponen, Ari; Jones, Kenneth L.
- Fungal Ecology, Vol. 10
Bacterial flagellar motility on hydrated rough surfaces controlled by aqueous film thickness and connectedness
journal, January 2016
- Tecon, Robin; Or, Dani
- Scientific Reports, Vol. 6, Issue 1
Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
journal, September 2011
- Berry, David; Ben Mahfoudh, Karim; Wagner, Michael
- Applied and Environmental Microbiology, Vol. 77, Issue 21
Impact of seasonal changes on fungal diversity of a semi-arid ecosystem revealed by 454 pyrosequencing
journal, April 2015
- Vargas-Gastélum, Lluvia; Romero-Olivares, Adriana L.; Escalante, Ana E.
- FEMS Microbiology Ecology, Vol. 91, Issue 5
Hydration and diffusion processes shape microbial community organization and function in model soil aggregates: HYDRATION AFFECTS MICROBIAL ACTIVITY IN SOIL AGGREGATES
journal, December 2015
- Ebrahimi, Ali; Or, Dani
- Water Resources Research, Vol. 51, Issue 12
fdrtool: a versatile R package for estimating local and tail area-based false discovery rates
journal, April 2008
- Strimmer, K.
- Bioinformatics, Vol. 24, Issue 12
Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland
journal, March 2009
- Cruz-Martínez, Karelyn; Suttle, K. Blake; Brodie, Eoin L.
- The ISME Journal, Vol. 3, Issue 6
Responses of soil heterotrophic respiration to moisture availability: An exploration of processes and models
journal, April 2013
- Moyano, Fernando E.; Manzoni, Stefano; Chenu, Claire
- Soil Biology and Biochemistry, Vol. 59
Picante: R tools for integrating phylogenies and ecology
journal, April 2010
- Kembel, S. W.; Cowan, P. D.; Helmus, M. R.
- Bioinformatics, Vol. 26, Issue 11
The sensitivity of annual grassland carbon cycling to the quantity and timing of rainfall
journal, June 2008
- Chou, Wendy W.; Silver, Whendee L.; Jackson, Randall D.
- Global Change Biology, Vol. 14, Issue 6
Shifts in Microbial Biomass and the Bacteria: Fungi Ratio Occur Under Field Conditions Within 3 h After Rainfall
journal, March 2011
- Landesman, William J.; Dighton, John
- Microbial Ecology, Vol. 62, Issue 1
Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
journal, December 2011
- Berry, David; Ben Mahfoudh, Karim; Wagner, Michael
- Applied and Environmental Microbiology, Vol. 78, Issue 2
Effects of lime application on nitrogen and phosphorus availability in humic soils
journal, May 2020
- Mkhonza, N. P.; Buthelezi-Dube, N. N.; Muchaonyerwa, P.
- Scientific Reports, Vol. 10, Issue 1
Effects of simulated drought and nitrogen fertilizer on plant productivity and nitrous oxide (N2O) emissions of two pastures
text, January 2012
- Hartmann, Adrian A.; Niklaus, Pascal A.
- Springer
VSEARCH: a versatile open source tool for metagenomics
text, January 2016
- Rognes, Torbjorn; Flouri, Tomas; Nichols, Ben
- Karlsruhe
Effects of simulated drought and nitrogen fertilizer on plant productivity and nitrous oxide (N2O) emissions of two pastures
text, January 2012
- Hartmann, Adrian A.; Niklaus, Pascal A.
- ETH Zurich
Bacterial flagellar motility on hydrated rough surfaces controlled by aqueous film thickness and connectedness
text, January 2016
- Robin, Tecon,; Dani, Or,
- ETH Zurich
Works referencing / citing this record:
Soil microbial moisture dependences and responses to drying–rewetting: The legacy of 18 years drought
journal, December 2018
- de Nijs, Evy A.; Hicks, Lettice C.; Leizeaga, Ainara
- Global Change Biology, Vol. 25, Issue 3
Rapid Shifts in Bacterial Community Assembly under Static and Dynamic Hydration Conditions in Porous Media
journal, October 2019
- Kleyer, Hannah; Tecon, Robin; Or, Dani
- Applied and Environmental Microbiology, Vol. 86, Issue 1
Contrasting Biogeographic Patterns of Bacterial and Archaeal Diversity in the Top- and Subsoils of Temperate Grasslands
journal, October 2019
- Liu, Nana; Hu, Huifeng; Ma, Wenhong
- mSystems, Vol. 4, Issue 5
Rapid Shifts in Bacterial Community Assembly under Static and Dynamic Hydration Conditions in Porous Media
text, January 2020
- Kleyer, Hannah; Tecon, Robin; Or, Dani
- ETH Zurich
Improved soil biological health increases corn grain yield in N fertilized systems across the Corn Belt
journal, March 2020
- Wade, Jordon; Culman, Steve W.; Logan, Jessica A. R.
- Scientific Reports, Vol. 10, Issue 1
Rapid Shifts in Bacterial Community Assembly under Static and Dynamic Hydration Conditions in Porous Media
journal, October 2019
- Kleyer, Hannah; Tecon, Robin; Or, Dani
- Applied and Environmental Microbiology, Vol. 86, Issue 1
Seasonal Dynamics of Soil Fungal and Bacterial Communities in Cool-Temperate Montane Forests
journal, August 2019
- Shigyo, Nobuhiko; Umeki, Kiyoshi; Hirao, Toshihide
- Frontiers in Microbiology, Vol. 10
Figures / Tables found in this record: