Plant roots alter microbial functional genes supporting root litter decomposition
Abstract
Decomposition of soil organic carbon is central to the global carbon cycle and profoundly affected by plant roots. While root “priming” of decomposition has been extensively investigated, it is not known how plants alter the molecular ecology of soil microbial decomposers. We disentangled the effects of Avena fatua, a common annual grass, on 13C-labeled root litter decomposition and quantified multiple genetic characteristics of soil bacterial and fungal communities. In our study, plants consistently suppressed rates of root litter decomposition. Microbes from planted soils had relatively more genes coding for low molecular weight compound degradation enzymes, while those from unplanted had more macromolecule degradation genes. Higher abundances of “water stress” genes in planted soils suggested that microbes experienced plant-induced water stress. We developed a conceptual model based on Mantel analyses of our extensive data set. This model indicates that plant root effects on the multiple soil environmental and microbial mechanisms involved in root litter decomposition act through changing the functional gene profiles of microbial decomposers living near plant roots.
- Authors:
-
- Univ. of California, Berkeley, CA (United States); Univ. of Oklahoma, Norman, OK (United States)
- Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of Oklahoma, Norman, OK (United States)
- Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
- Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Tsinghua Univ., Beijing (China)
- Publication Date:
- Research Org.:
- Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA)
- OSTI Identifier:
- 1526178
- Alternate Identifier(s):
- OSTI ID: 1636111
- Report Number(s):
- LLNL-JRNL-671996
Journal ID: ISSN 0038-0717; 794212
- Grant/Contract Number:
- AC52-07NA27344; SC0004730; SC0010570; 00008322; SCW1060; SCW142
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Soil Biology and Biochemistry
- Additional Journal Information:
- Journal Volume: 127; Journal Issue: C; Journal ID: ISSN 0038-0717
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Shi, Shengjing, Herman, Donald J., He, Zhili, Pett-Ridge, Jennifer, Wu, Liyou, Zhou, Jizhong, and Firestone, Mary K. Plant roots alter microbial functional genes supporting root litter decomposition. United States: N. p., 2018.
Web. doi:10.1016/j.soilbio.2018.09.013.
Shi, Shengjing, Herman, Donald J., He, Zhili, Pett-Ridge, Jennifer, Wu, Liyou, Zhou, Jizhong, & Firestone, Mary K. Plant roots alter microbial functional genes supporting root litter decomposition. United States. https://doi.org/10.1016/j.soilbio.2018.09.013
Shi, Shengjing, Herman, Donald J., He, Zhili, Pett-Ridge, Jennifer, Wu, Liyou, Zhou, Jizhong, and Firestone, Mary K. Tue .
"Plant roots alter microbial functional genes supporting root litter decomposition". United States. https://doi.org/10.1016/j.soilbio.2018.09.013. https://www.osti.gov/servlets/purl/1526178.
@article{osti_1526178,
title = {Plant roots alter microbial functional genes supporting root litter decomposition},
author = {Shi, Shengjing and Herman, Donald J. and He, Zhili and Pett-Ridge, Jennifer and Wu, Liyou and Zhou, Jizhong and Firestone, Mary K.},
abstractNote = {Decomposition of soil organic carbon is central to the global carbon cycle and profoundly affected by plant roots. While root “priming” of decomposition has been extensively investigated, it is not known how plants alter the molecular ecology of soil microbial decomposers. We disentangled the effects of Avena fatua, a common annual grass, on 13C-labeled root litter decomposition and quantified multiple genetic characteristics of soil bacterial and fungal communities. In our study, plants consistently suppressed rates of root litter decomposition. Microbes from planted soils had relatively more genes coding for low molecular weight compound degradation enzymes, while those from unplanted had more macromolecule degradation genes. Higher abundances of “water stress” genes in planted soils suggested that microbes experienced plant-induced water stress. We developed a conceptual model based on Mantel analyses of our extensive data set. This model indicates that plant root effects on the multiple soil environmental and microbial mechanisms involved in root litter decomposition act through changing the functional gene profiles of microbial decomposers living near plant roots.},
doi = {10.1016/j.soilbio.2018.09.013},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 127,
place = {United States},
year = {Tue Sep 18 00:00:00 EDT 2018},
month = {Tue Sep 18 00:00:00 EDT 2018}
}
Web of Science
Figures / Tables:
Works referenced in this record:
A trait-based approach for modelling microbial litter decomposition
journal, May 2012
- Allison, S. D.
- Ecology Letters, Vol. 15, Issue 9
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
Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil
journal, April 2011
- Bird, Jeffrey A.; Herman, Donald J.; Firestone, Mary K.
- Soil Biology and Biochemistry, Vol. 43, Issue 4
Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review
journal, October 2008
- Blagodatskaya, Е.; Kuzyakov, Y.
- Biology and Fertility of Soils, Vol. 45, Issue 2
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012
- Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
- The ISME Journal, Vol. 6, Issue 8
The effects of heating, rhizosphere, and depth on root litter decomposition are mediated by soil moisture
journal, December 2017
- Castanha, Cristina; Zhu, Biao; Hicks Pries, Caitlin E.
- Biogeochemistry, Vol. 137, Issue 1-2
Synthesis and modeling perspectives of rhizosphere priming
journal, August 2013
- Cheng, Weixin; Parton, William J.; Gonzalez-Meler, Miquel A.
- New Phytologist, Vol. 201, Issue 1
The addition of labile carbon alters litter fungal communities and decreases litter decomposition rates
journal, July 2009
- Chigineva, N. I.; Aleksandrova, A. V.; Tiunov, A. V.
- Applied Soil Ecology, Vol. 42, Issue 3
Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest
journal, March 2013
- Clemmensen, K. E.; Bahr, A.; Ovaskainen, O.
- Science, Vol. 339, Issue 6127
Selective progressive response of soil microbial community to wild oat roots
journal, November 2008
- DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z.
- The ISME Journal, Vol. 3, Issue 2
The ade4 Package: Implementing the Duality Diagram for Ecologists
journal, January 2007
- Dray, Stéphane; Dufour, Anne-Béatrice
- Journal of Statistical Software, Vol. 22, Issue 4
Responses of Grassland Production to Single and Multiple Global Environmental Changes
journal, August 2005
- Dukes, Jeffrey S.; Chiariello, Nona R.; Cleland, Elsa E.
- PLoS Biology, Vol. 3, Issue 10
Identification of active bacteria involved in decomposition of complex maize and soybean residues in a tropical Vertisol using 15N-DNA stable isotope probing
journal, May 2011
- España, Mingrelia; Rasche, Frank; Kandeler, Ellen
- Pedobiologia, Vol. 54, Issue 3
Assessment of Soil Microbial Community Structure by Use of Taxon-Specific Quantitative PCR Assays
journal, July 2005
- Fierer, N.; Jackson, J. A.; Vilgalys, R.
- Applied and Environmental Microbiology, Vol. 71, Issue 7
Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles
journal, January 2015
- Finzi, Adrien C.; Abramoff, Rose Z.; Spiller, Kimberly S.
- Global Change Biology, Vol. 21, Issue 5
Carbon input to soil may decrease soil carbon content: Carbon input in soil carbon sequestration
journal, March 2004
- Fontaine, Sébastien; Bardoux, Gérard; Abbadie, Luc
- Ecology Letters, Vol. 7, Issue 4
Networking our science to characterize the state, vulnerabilities, and management opportunities of soil organic matter
journal, September 2017
- Harden, Jennifer W.; Hugelius, Gustaf; Ahlström, Anders
- Global Change Biology, Vol. 24, Issue 2
Continuous flow isotope ratio mass spectrometry of carbon dioxide trapped as strontium carbonate
journal, May 1997
- Harris, D.; Porter, L. K.; Paul, E. A.
- Communications in Soil Science and Plant Analysis, Vol. 28, Issue 9-10
GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes
journal, May 2007
- He, Zhili; Gentry, Terry J.; Schadt, Christopher W.
- The ISME Journal, Vol. 1, Issue 1
Nitrogen Dynamics in an Annual Grassland: oak Canopy, Climate, and Microbial Population Effects
journal, June 2003
- Herman, Donald J.; Halverson, Larry J.; Firestone, Mary K.
- Ecological Applications, Vol. 13, Issue 3
Detrended correspondence analysis: An improved ordination technique
journal, October 1980
- Hill, M. O.; Gauch, H. G.
- Vegetatio, Vol. 42, Issue 1-3
Rhizosphere priming effect: A meta-analysis
journal, August 2017
- Huo, Changfu; Luo, Yiqi; Cheng, Weixin
- Soil Biology and Biochemistry, Vol. 111
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities
journal, July 2012
- Ihrmark, Katarina; Bödeker, Inga T. M.; Cruz-Martinez, Karelyn
- FEMS Microbiology Ecology, Vol. 82, Issue 3
The Ecology of Soil Carbon: Pools, Vulnerabilities, and Biotic and Abiotic Controls
journal, November 2017
- Jackson, Robert B.; Lajtha, Kate; Crow, Susan E.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 48, Issue 1
Mineral protection of soil carbon counteracted by root exudates
journal, March 2015
- Keiluweit, Marco; Bougoure, Jeremy J.; Nico, Peter S.
- Nature Climate Change, Vol. 5, Issue 6
Nitrogen Additions and Litter Decomposition: a Meta-Analysis
journal, December 2005
- Knorr, M.; Frey, S. D.; Curtis, P. S.
- Ecology, Vol. 86, Issue 12
Review: Factors affecting rhizosphere priming effects
journal, August 2002
- Kuzyakov, Yakov
- Journal of Plant Nutrition and Soil Science, Vol. 165, Issue 4
Priming effects: Interactions between living and dead organic matter
journal, September 2010
- Kuzyakov, Yakov
- Soil Biology and Biochemistry, Vol. 42, Issue 9
Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature
journal, December 2006
- Kuzyakov, Yakov; Hill, Paul W.; Jones, David L.
- Plant and Soil, Vol. 290, Issue 1-2
The importance of anabolism in microbial control over soil carbon storage
journal, July 2017
- Liang, Chao; Schimel, Joshua P.; Jastrow, Julie D.
- Nature Microbiology, Vol. 2, Issue 8
Function and functional redundancy in microbial systems
journal, April 2018
- Louca, Stilianos; Polz, Martin F.; Mazel, Florent
- Nature Ecology & Evolution, Vol. 2, Issue 6
Seasonal dynamics of leaf- and root-derived C in arctic tundra mesocosms
journal, April 2004
- Loya, Wendy M.; Johnson, Loretta C.; Nadelhoffer, Knute J.
- Soil Biology and Biochemistry, Vol. 36, Issue 4
Toward more realistic projections of soil carbon dynamics by Earth system models: SOIL CARBON MODELING
journal, January 2016
- Luo, Yiqi; Ahlström, Anders; Allison, Steven D.
- Global Biogeochemical Cycles, Vol. 30, Issue 1
Drying and rewetting of a loamy sand soil did not increase the turnover of native organic matter, but retarded the decomposition of added 14C-labelled plant material
journal, April 1999
- Magid, J.; Kjærgaard, C.; Gorissen, A.
- Soil Biology and Biochemistry, Vol. 31, Issue 4
Responses of soil microbial communities to water stress: results from a meta-analysis
journal, April 2012
- Manzoni, Stefano; Schimel, Joshua P.; Porporato, Amilcare
- Ecology, Vol. 93, Issue 4
“Non-metabolizable” glucose analogue shines new light on priming mechanisms: Triggering of microbial metabolism
journal, April 2017
- Mason-Jones, Kyle; Kuzyakov, Yakov
- Soil Biology and Biochemistry, Vol. 107
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
Soil Mineralogy Affects Conifer Forest Soil Carbon Source Utilization and Microbial Priming
journal, January 2007
- Rasmussen, Craig; Southard, Randal J.; Horwath, William R.
- Soil Science Society of America Journal, Vol. 71, Issue 4
Legume presence reduces the decomposition rate of non-legume roots
journal, March 2016
- Saar, Sirgi; Semchenko, Marina; Barel, Janna M.
- Soil Biology and Biochemistry, Vol. 94
Microbial control over carbon cycling in soil
journal, January 2012
- Schimel, Joshua P.; Schaeffer, Sean M.
- Frontiers in Microbiology, Vol. 3
The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model
journal, April 2003
- Schimel, J.
- Soil Biology and Biochemistry, Vol. 35, Issue 4
Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga
journal, June 1999
- Schimel, Joshua P.; Gulledge, Jay M.; Clein-Curley, Joy S.
- Soil Biology and Biochemistry, Vol. 31, Issue 6
The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
journal, June 2016
- Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.
- Ecology Letters, Vol. 19, Issue 8
Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
journal, August 2015
- Shi, Shengjing; Nuccio, Erin; Herman, Donald J.
- mBio, Vol. 6, Issue 4
Stoichiometry of soil enzyme activity at global scale: Stoichiometry of soil enzyme activity
journal, September 2008
- Sinsabaugh, Robert L.; Lauber, Christian L.; Weintraub, Michael N.
- Ecology Letters, Vol. 11, Issue 11
Taxon-specific responses of soil microbial communities to different soil priming effects induced by addition of plant residues and their biochars
journal, August 2015
- Su, Peng; Lou, Jun; Brookes, Philip C.
- Journal of Soils and Sediments, Vol. 17, Issue 3
The effect of living plants on root decomposition of four grass species
journal, January 2002
- Van Der Krift, Tanja A. J.; Kuikman, Peter J.; Berendse, Frank
- Oikos, Vol. 96, Issue 1
Dinner in the dark: Illuminating drivers of soil organic matter decomposition
journal, February 2017
- van der Wal, Annemieke; de Boer, Wietse
- Soil Biology and Biochemistry, Vol. 105
Functional Gene Differences in Soil Microbial Communities from Conventional, Low-Input, and Organic Farmlands
journal, December 2012
- Xue, Kai; Wu, Liyou; Deng, Ye
- Applied and Environmental Microbiology, Vol. 79, Issue 4
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018
- Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao
- Nature Microbiology, Vol. 3, Issue 4
Impacts of drying–wetting cycles on rhizosphere respiration and soil organic matter decomposition
journal, August 2013
- Zhu, Biao; Cheng, Weixin
- Soil Biology and Biochemistry, Vol. 63
Works referencing / citing this record:
Massively parallel screening of synthetic microbial communities
journal, June 2019
- Kehe, Jared; Kulesa, Anthony; Ortiz, Anthony
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 26
Simulating metagenomic stable isotope probing datasets with MetaSIPSim
journal, January 2020
- Barnett, Samuel E.; Buckley, Daniel H.
- BMC Bioinformatics, Vol. 21, Issue 1
Plant presence reduces root and shoot litter decomposition rates of crops and wild relatives
journal, March 2019
- Barel, Janna M.; Kuyper, Thomas W.; de Boer, Wietse
- Plant and Soil, Vol. 438, Issue 1-2
Simulating metagenomic stable isotope probing datasets with MetaSIPSim
journal, January 2020
- Barnett, Samuel E.; Buckley, Daniel H.
- BMC Bioinformatics, Vol. 21, Issue 1
Figures / Tables found in this record: