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Title: 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-CO 2 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:
 [1];  [2];  [3];  [1];  [1];  [1];  [4];  [4];  [5];  [1];  [1]
  1. Univ. Bourgogne Franche-Comte, Dijon (France)
  2. Univ. Bourgogne Franche-Comte, Dijon (France); Iowa State Univ., Ames, IA (United States)
  3. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  4. Swiss Federal Research Institute WSL, Birmensdorf (Switzerland)
  5. Univ. Politecnica de Madrid, Madrid (Spain)
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (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:
Journal Article: 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. 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, and Barnard, Romain L. Fri . "Depth matters: effects of precipitation regime on soil microbial activity upon rewetting of a plant-soil system". United States. doi: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},
issn = {1751-7362},
number = ,
volume = 12,
place = {United States},
year = {2018},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
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Cited by: 7 works
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Figures / Tables:

Fig. 1 Fig. 1: Dynamics of soil water content in the experimental treatments (infrequent and frequent water input, dotted and full curves, respectively) over the duration of the experiment. Lines and shaded polygons around them indicate mean ± standard error (n=5).

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Works referenced in this record:

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Drying and rewetting effects on soil microbial community composition and nutrient leaching
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The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters
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High-resolution isotope measurements resolve rapid ecohydrological dynamics at the soil-plant interface
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Effects of simulated drought and nitrogen fertilizer on plant productivity and nitrous oxide (N2O) emissions of two pastures
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Vertical distribution of fungal communities in tallgrass prairie soil
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Hydration dynamics promote bacterial coexistence on rough surfaces
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Forest understory plant and soil microbial response to an experimentally induced drought and heat-pulse event: the importance of maintaining the continuum
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Development of a Prokaryotic Universal Primer for Simultaneous Analysis of Bacteria and Archaea Using Next-Generation Sequencing
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Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils
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Dynamics of 18O Incorporation from H 2 18O into Soil Microbial DNA
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Summer drought alters carbon allocation to roots and root respiration in mountain grassland
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Basic Local Alignment Search Tool
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Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
journal, December 2011

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    Works referencing / citing this record:

    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
    • DOI: 10.1002/rcm.5287

    Drying–Rewetting Cycles Affect Fungal and Bacterial Growth Differently in an Arable Soil
    journal, July 2010


    Shifts in Microbial Biomass and the Bacteria: Fungi Ratio Occur Under Field Conditions Within 3 h After Rainfall
    journal, March 2011


    Dynamics of 18O Incorporation from H 2 18O into Soil Microbial DNA
    journal, March 2011


    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
    • DOI: 10.1007/s00248-016-0835-4

    Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter?
    journal, September 2011


    Effects of simulated drought and nitrogen fertilizer on plant productivity and nitrous oxide (N2O) emissions of two pastures
    journal, May 2012


    An extraction method for measuring soil microbial biomass C
    journal, January 1987


    Living in a fungal world: impact of fungi on soil bacterial niche development
    journal, September 2005


    Tallgrass prairie soil fungal communities are resilient to climate change
    journal, August 2014


    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
    • DOI: 10.1016/j.ppees.2011.12.001

    Drying and rewetting effects on soil microbial community composition and nutrient leaching
    journal, February 2008


    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


    Responses of soil heterotrophic respiration to moisture availability: An exploration of processes and models
    journal, April 2013


    Prolonged summer droughts retard soil N processing and stabilization in organo-mineral fractions
    journal, January 2014


    Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling
    journal, February 2015


    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
    • DOI: 10.1038/ismej.2009.16

    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
    • DOI: 10.1038/ismej.2011.139

    Hydration dynamics promote bacterial coexistence on rough surfaces
    journal, October 2012


    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
    • DOI: 10.1038/ismej.2013.104

    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
    • DOI: 10.1038/ismej.2014.192

    Phylogenetic organization of bacterial activity
    journal, March 2016

    • Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
    • The ISME Journal, Vol. 10, Issue 9
    • DOI: 10.1038/ismej.2016.28

    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
    • DOI: 10.1038/nclimate1368

    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
    • DOI: 10.1038/nmeth.f.303

    Bacterial flagellar motility on hydrated rough surfaces controlled by aqueous film thickness and connectedness
    journal, January 2016


    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
    • DOI: 10.1073/pnas.1008392107

    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
    • DOI: 10.1073/pnas.1204306109

    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
    • DOI: 10.1086/303378

    PyNAST: a flexible tool for aligning sequences to a template alignment
    journal, November 2009


    Picante: R tools for integrating phylogenies and ecology
    journal, April 2010


    Search and clustering orders of magnitude faster than BLAST
    journal, August 2010


    PEAR: a fast and accurate Illumina Paired-End reAd mergeR
    journal, October 2013


    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
    • DOI: 10.1093/femsec/fiv044

    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
    • DOI: 10.1093/molbev/msp077

    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
    • DOI: 10.1111/1365-2745.12593

    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
    • DOI: 10.1111/1574-6941.12155

    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
    • DOI: 10.1111/gcb.12789

    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
    • DOI: 10.1111/gcb.13270

    The sensitivity of annual grassland carbon cycling to the quantity and timing of rainfall
    journal, June 2008


    Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils
    journal, October 2008


    Drought effects on allocation of recent carbon: from beech leaves to soil CO2 efflux
    journal, October 2009


    The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters
    journal, March 2010


    Prediction of soil water retention properties after stratification by combining texture, bulk density and the type of horizon
    journal, December 2008


    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
    • DOI: 10.1111/nph.13146

    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
    • DOI: 10.1111/nph.13868

    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
    • DOI: 10.1111/plb.12486

    Phylogenies and Community Ecology
    journal, November 2002


    Development of a Prokaryotic Universal Primer for Simultaneous Analysis of Bacteria and Archaea Using Next-Generation Sequencing
    journal, August 2014


    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
    • DOI: 10.1890/12-2018.1

    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
    • DOI: 10.2136/sssaj2014.10.0431

    Controls on soil microbial community stability under climate change
    journal, January 2013


    Vertical distribution of fungal communities in tallgrass prairie soil
    journal, September 2010

    • Jumpponen, Ari; Jones, Kenneth L.; Blair, John
    • Mycologia, Vol. 102, Issue 5
    • DOI: 10.3852/09-316

    VSEARCH: a versatile open source tool for metagenomics
    journal, January 2016


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.