Microhydrological Niches in Soils: How Mucilage and EPS Alter the Biophysical Properties of the Rhizosphere and Other Biological Hotspots
Abstract
Core Ideas Plant mucilage and bacterial extracellular polymeric substances (EPS) prevent the breakup of the soil liquid phase. Formation of continuous structures buffers soil hydraulic properties. The release of viscous polymeric substances represents a universal strategy. Plant roots and bacteria are capable of buffering erratic fluctuations of water content in their local soil environment by releasing a diverse, highly polymeric blend of substances (e.g. extracellular polymeric substances [EPS] and mucilage). Although this concept is well accepted, the physical mechanisms by which EPS and mucilage interact with the soil matrix and determine the soil water dynamics remain unclear. High‐resolution X‐ray computed tomography revealed that upon drying in porous media, mucilage (from maize [ Zea mays L.] roots) and EPS (from intact biocrusts) form filaments and two‐dimensional interconnected structures spanning across multiple pores. Unlike water, these mucilage and EPS structures connecting soil particles did not break up upon drying, which is explained by the high viscosity and low surface tension of EPS and mucilage. Measurements of water retention and evaporation with soils mixed with seed mucilage show how these one‐ and two‐dimensional pore‐scale structures affect macroscopic hydraulic properties (i.e., they enhance water retention, preserve the continuity of the liquid phase in dryingmore »
- Authors:
-
- Faculty for Biology, Chemistry, and Earth Sciences, Chair of Soil Physics Univ. of Bayreuth Universitätsstraße 30, 95447 Bayreuth Bavaria Germany, Faculty of Agricultural Sciences, Group of Soil Hydrology Univ. of Göttingen Büsgenweg 2, 37077 Göttingen Lower Saxony Germany
- Faculty for Biology, Chemistry, and Earth Sciences, Chair of Soil Physics Univ. of Bayreuth Universitätsstraße 30, 95447 Bayreuth Bavaria Germany
- Institute for Environmental Sciences Group of Environmental and Soil Chemistry Univ. Koblenz‐Landau Fortstraße 7, 76829 Landau Rhineland‐Palatinate Germany
- Paul Scherrer Institute Swiss Light Source Forschungsstrasse 111 5232 Villigen Switzerland
- Arizona State Univ. School of Life Sciences 427 E. Tyler Mall Tempe AZ85281, Lawrence Berkeley National Lab. Environmental Genomics and Systems Biology 1 Cyclotron Rd. Berkeley CA 94720
- Dep. of Soil Science Univ. of Kassel Mönchebergstraße 19 34125 Witzenhausen Hesse Germany
- Paul Scherrer Institute Lab. for Neutron Scattering and Imaging Forschungsstrasse 111 5232 Villigen Switzerland
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1602291
- Alternate Identifier(s):
- OSTI ID: 1604258
- Resource Type:
- Published Article
- Journal Name:
- Vadose Zone Journal
- Additional Journal Information:
- Journal Name: Vadose Zone Journal Journal Volume: 18 Journal Issue: 1; Journal ID: ISSN 1539-1663
- Publisher:
- Wiley Blackwell (John Wiley & Sons)
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Benard, Pascal, Zarebanadkouki, Mohsen, Brax, Mathilde, Kaltenbach, Robin, Jerjen, Iwan, Marone, Federica, Couradeau, Estelle, Felde, Vincent J. M. N. L., Kaestner, Anders, and Carminati, Andrea. Microhydrological Niches in Soils: How Mucilage and EPS Alter the Biophysical Properties of the Rhizosphere and Other Biological Hotspots. United States: N. p., 2019.
Web. doi:10.2136/vzj2018.12.0211.
Benard, Pascal, Zarebanadkouki, Mohsen, Brax, Mathilde, Kaltenbach, Robin, Jerjen, Iwan, Marone, Federica, Couradeau, Estelle, Felde, Vincent J. M. N. L., Kaestner, Anders, & Carminati, Andrea. Microhydrological Niches in Soils: How Mucilage and EPS Alter the Biophysical Properties of the Rhizosphere and Other Biological Hotspots. United States. https://doi.org/10.2136/vzj2018.12.0211
Benard, Pascal, Zarebanadkouki, Mohsen, Brax, Mathilde, Kaltenbach, Robin, Jerjen, Iwan, Marone, Federica, Couradeau, Estelle, Felde, Vincent J. M. N. L., Kaestner, Anders, and Carminati, Andrea. Thu .
"Microhydrological Niches in Soils: How Mucilage and EPS Alter the Biophysical Properties of the Rhizosphere and Other Biological Hotspots". United States. https://doi.org/10.2136/vzj2018.12.0211.
@article{osti_1602291,
title = {Microhydrological Niches in Soils: How Mucilage and EPS Alter the Biophysical Properties of the Rhizosphere and Other Biological Hotspots},
author = {Benard, Pascal and Zarebanadkouki, Mohsen and Brax, Mathilde and Kaltenbach, Robin and Jerjen, Iwan and Marone, Federica and Couradeau, Estelle and Felde, Vincent J. M. N. L. and Kaestner, Anders and Carminati, Andrea},
abstractNote = {Core Ideas Plant mucilage and bacterial extracellular polymeric substances (EPS) prevent the breakup of the soil liquid phase. Formation of continuous structures buffers soil hydraulic properties. The release of viscous polymeric substances represents a universal strategy. Plant roots and bacteria are capable of buffering erratic fluctuations of water content in their local soil environment by releasing a diverse, highly polymeric blend of substances (e.g. extracellular polymeric substances [EPS] and mucilage). Although this concept is well accepted, the physical mechanisms by which EPS and mucilage interact with the soil matrix and determine the soil water dynamics remain unclear. High‐resolution X‐ray computed tomography revealed that upon drying in porous media, mucilage (from maize [ Zea mays L.] roots) and EPS (from intact biocrusts) form filaments and two‐dimensional interconnected structures spanning across multiple pores. Unlike water, these mucilage and EPS structures connecting soil particles did not break up upon drying, which is explained by the high viscosity and low surface tension of EPS and mucilage. Measurements of water retention and evaporation with soils mixed with seed mucilage show how these one‐ and two‐dimensional pore‐scale structures affect macroscopic hydraulic properties (i.e., they enhance water retention, preserve the continuity of the liquid phase in drying soils, and decrease vapor diffusivity and local drying rates). In conclusion, we propose that the release of viscous polymeric substances and the consequent creation of a network bridging the soil pore space represent a universal strategy of plants and bacteria to engineer their own soil microhydrological niches where stable conditions for life are preserved.},
doi = {10.2136/vzj2018.12.0211},
journal = {Vadose Zone Journal},
number = 1,
volume = 18,
place = {United States},
year = {2019},
month = {6}
}
https://doi.org/10.2136/vzj2018.12.0211
Web of Science
Works referenced in this record:
Commonality of Elastic Relaxation Times in Biofilms
journal, August 2004
- Shaw, T.; Winston, M.; Rupp, C. J.
- Physical Review Letters, Vol. 93, Issue 9
Rheological properties of viscoelastic biofilm extracellular polymeric substances and comparison to the behavior of calcium alginate gels
journal, January 2004
- Wloka, M.; Rehage, H.; Flemming, H. -C.
- Colloid and Polymer Science, Vol. 282, Issue 10
Microbial extracellular polymeric substances improve water retention in dryland biological soil crusts
journal, January 2018
- Adessi, Alessandra; Cruz de Carvalho, Ricardo; De Philippis, Roberto
- Soil Biology and Biochemistry, Vol. 116
Dynamics of soil water content in the rhizosphere
journal, January 2010
- Carminati, Andrea; Moradi, Ahmad B.; Vetterlein, Doris
- Plant and Soil, Vol. 332, Issue 1-2
Clay- or sand-polysaccharide associations as models for the interface between micro-organisms and soil: water related properties and microstructure
journal, March 1993
- Chenu, Claire
- Geoderma, Vol. 56, Issue 1-4
Dryland photoautotrophic soil surface communities endangered by global change
journal, February 2018
- Rodriguez-Caballero, Emilio; Belnap, Jayne; Büdel, Burkhard
- Nature Geoscience, Vol. 11, Issue 3
An efficient method for the collection of root mucilage from different plant species-A case study on the effect of mucilage on soil water repellency
journal, February 2016
- Zickenrott, Ina-Maria; Woche, Susanne K.; Bachmann, Jörg
- Journal of Plant Nutrition and Soil Science, Vol. 179, Issue 2
Nonequilibrium water dynamics in the rhizosphere: How mucilage affects water flow in soils
journal, August 2014
- Kroener, Eva; Zarebanadkouki, Mohsen; Kaestner, Anders
- Water Resources Research, Vol. 50, Issue 8
Relationship between Desiccation and Exopolysaccharide Production in a Soil Pseudomonas sp
journal, January 1992
- Roberson, Emily B.; Firestone, Mary K.
- Applied and Environmental Microbiology, Vol. 58, Issue 4
Mechanical robustness of Pseudomonasaeruginosa biofilms
journal, January 2011
- Lieleg, Oliver; Caldara, Marina; Baumgärtel, Regina
- Soft Matter, Vol. 7, Issue 7
Synergistic effects of soil microstructure and bacterial EPS on drying rate in emulated soil micromodels
journal, April 2015
- Deng, Jinzi; Orner, Erika P.; Chau, Jessica Furrer
- Soil Biology and Biochemistry, Vol. 83
Towards on-the-fly data post-processing for real-time tomographic imaging at TOMCAT
journal, January 2017
- Marone, Federica; Studer, Alain; Billich, Heiner
- Advanced Structural and Chemical Imaging, Vol. 3, Issue 1
Liquid bridges at the root-soil interface
journal, April 2017
- Carminati, Andrea; Benard, P.; Ahmed, M. A.
- Plant and Soil, Vol. 417, Issue 1-2
Biofilm effect on soil hydraulic properties: Experimental investigation using soil-grown real biofilm: HYDRAULIC PROPERTIES OF BIOFILM AMENDED SOIL
journal, August 2016
- Volk, Elazar; Iden, Sascha C.; Furman, Alex
- Water Resources Research, Vol. 52, Issue 8
Chemical and Functional Properties of Chia Seed ( Salvia hispanica L.) Gum
journal, January 2014
- Segura-Campos, Maira Rubi; Ciau-Solís, Norma; Rosado-Rubio, Gabriel
- International Journal of Food Science, Vol. 2014
Biofilm material properties as related to shear-induced deformation and detachment phenomena
journal, December 2002
- Stoodley, P.; Cargo, R.; Rupp, C. J.
- Journal of Industrial Microbiology and Biotechnology, Vol. 29, Issue 6
Natural functions of lipopeptides from Bacillus and Pseudomonas : more than surfactants and antibiotics
journal, November 2010
- Raaijmakers, Jos M.; De Bruijn, Irene; Nybroe, Ole
- FEMS Microbiology Reviews, Vol. 34, Issue 6
Characteristic lengths affecting evaporative drying of porous media
journal, May 2008
- Lehmann, Peter; Assouline, Shmuel; Or, Dani
- Physical Review E, Vol. 77, Issue 5
Trends in synchrotron-based tomographic imaging: the SLS experience
conference, August 2006
- Stampanoni, M.; Groso, A.; Isenegger, A.
- SPIE Optics + Photonics, SPIE Proceedings
Complex role of the polymeric matrix in biological soil crusts
journal, October 2017
- Rossi, Federico; Mugnai, Gianmarco; De Philippis, Roberto
- Plant and Soil, Vol. 429, Issue 1-2
Surface tension and viscosity of axenic maize and lupin root mucilages
journal, December 1997
- Read, D. B.; Gregory, P. J.
- New Phytologist, Vol. 137, Issue 4
Neutron imaging at PSI: a promising tool in materials science and technology
journal, March 2010
- Lehmann, Eberhard H.; Wagner, Werner
- Applied Physics A, Vol. 99, Issue 3
In Situ X-Ray Tomography Imaging of Soil Water and Cyanobacteria From Biological Soil Crusts Undergoing Desiccation
journal, June 2018
- Couradeau, Estelle; Felde, Vincent J. M. N. L.; Parkinson, Dilworth
- Frontiers in Environmental Science, Vol. 6
Influence of calcium ions on the mechanical properties of a model biofilm of mucoid Pseudomonas aeruginosa
journal, March 2001
- Körstgens, V.; Flemming, H. -C.; Wingender, J.
- Water Science and Technology, Vol. 43, Issue 6
Microbial hotspots and hot moments in soil: Concept & review
journal, April 2015
- Kuzyakov, Yakov; Blagodatskaya, Evgenia
- Soil Biology and Biochemistry, Vol. 83
Plant exudates may stabilize or weaken soil depending on species, origin and time: Effect of plant exudates on rhizosphere formation
journal, October 2017
- Naveed, M.; Brown, L. K.; Raffan, A. C.
- European Journal of Soil Science, Vol. 68, Issue 6
Interplay between soil drying and root exudation in rhizosheath development
journal, October 2013
- Albalasmeh, Ammar A.; Ghezzehei, Teamrat A.
- Plant and Soil, Vol. 374, Issue 1-2
Pore-Scale Distribution of Mucilage Affecting Water Repellency in the Rhizosphere
journal, September 2017
- Benard, P.; Zarebanadkouki, M.; Hedwig, C.
- Vadose Zone Journal, Vol. 17, Issue 1
Extracellular Polymeric Substances Affecting Pore-Scale Hydrologic Conditions for Bacterial Activity in Unsaturated Soils
journal, January 2007
- Or, Dani; Phutane, Sachin; Dechesne, Arnaud
- Vadose Zone Journal, Vol. 6, Issue 2
Plant Growth‐Promoting Rhizobacteria (PGPR) Reduce Evaporation and Increase Soil Water Retention
journal, May 2018
- Zheng, Wenjuan; Zeng, Saiqi; Bais, Harsh
- Water Resources Research, Vol. 54, Issue 5
The biofilm matrix
journal, August 2010
- Flemming, Hans-Curt; Wingender, Jost
- Nature Reviews Microbiology, Vol. 8, Issue 9
Going back to the roots: the microbial ecology of the rhizosphere
journal, September 2013
- Philippot, Laurent; Raaijmakers, Jos M.; Lemanceau, Philippe
- Nature Reviews Microbiology, Vol. 11, Issue 11
Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object
journal, April 2002
- Paganin, D.; Mayo, S. C.; Gureyev, T. E.
- Journal of Microscopy, Vol. 206, Issue 1
Water Retention Curves of Biofilm-Affected Soils using Xanthan as an Analogue
journal, January 2012
- Rosenzweig, Ravid; Shavit, Uri; Furman, Alex
- Soil Science Society of America Journal, Vol. 76, Issue 1
The final stages of capillary break-up of polymer solutions
journal, February 2012
- Sattler, R.; Gier, S.; Eggers, J.
- Physics of Fluids, Vol. 24, Issue 2
Relevance of microbial extracellular polymeric substances (EPSs) - Part I: Structural and ecological aspects
journal, March 2001
- Flemming, H. -C.; Wingender, J.
- Water Science and Technology, Vol. 43, Issue 6
Three-dimensional visualization and quantification of water content in the rhizosphere
journal, August 2011
- Moradi, Ahmad B.; Carminati, Andrea; Vetterlein, Doris
- New Phytologist, Vol. 192, Issue 3
Microstructural changes in bacterial exopolysaccharides during desiccation
journal, September 1993
- Roberson, E. B.; Chenu, C.; Firestone, M. K.
- Soil Biology and Biochemistry, Vol. 25, Issue 9
A mass conservative numerical solution for two-phase flow in porous media with application to unsaturated flow
journal, October 1992
- Celia, Michael A.; Binning, Philip
- Water Resources Research, Vol. 28, Issue 10
Effects of Mucilage on Rhizosphere Hydraulic Functions Depend on Soil Particle Size
journal, January 2018
- Kroener, Eva; Holz, Maire; Zarebanadkouki, Mohsen
- Vadose Zone Journal, Vol. 17, Issue 1
Revisiting the simplified evaporation method: Identification of hydraulic functions considering vapor, film and corner flow
journal, August 2015
- Peters, Andre; Iden, Sascha C.; Durner, Wolfgang
- Journal of Hydrology, Vol. 527
Biocrusts positively affect the soil water balance in semiarid ecosystems: The Role of Biocrusts in the Local Water Balance
journal, January 2016
- Chamizo, Sonia; Cantón, Yolanda; Rodríguez-Caballero, Emilio
- Ecohydrology, Vol. 9, Issue 7
Plant roots release phospholipid surfactants that modify the physical and chemical properties of soil
journal, January 2003
- Read, D. B.; Bengough, A. G.; Gregory, P. J.
- New Phytologist, Vol. 157, Issue 2
The perfect slime
journal, September 2011
- Flemming, Hans-Curt
- Colloids and Surfaces B: Biointerfaces, Vol. 86, Issue 2
A Role for Exopolysaccharides in the Protection of Microorganisms from Desiccation
journal, January 1994
- Ophir, Tslil; Gutnick, David L.
- Applied and Environmental Microbiology, Vol. 60, Issue 2
Rhizosphere-Scale Quantification of Hydraulic and Mechanical Properties of Soil Impacted by Root and Seed Exudates
journal, January 2018
- Naveed, M.; Brown, L. K.; Raffan, A. C.
- Vadose Zone Journal, Vol. 17, Issue 1
Biofilms: an emergent form of bacterial life
journal, August 2016
- Flemming, Hans-Curt; Wingender, Jost; Szewzyk, Ulrich
- Nature Reviews Microbiology, Vol. 14, Issue 9
Breakup of Liquid Filaments
journal, February 2012
- Castrejón-Pita, Alfonso A.; Castrejón-Pita, J. R.; Hutchings, I. M.
- Physical Review Letters, Vol. 108, Issue 7
Contribution of cryptogamic covers to the global cycles of carbon and nitrogen
journal, June 2012
- Elbert, Wolfgang; Weber, Bettina; Burrows, Susannah
- Nature Geoscience, Vol. 5, Issue 7
Die Bildung von Tropfen an Düsen und die Auflösung flüssiger Strahlen
journal, January 1936
- Ohnesorge, Wolfgang V.
- ZAMM - Journal of Applied Mathematics and Mechanics / Zeitschrift für Angewandte Mathematik und Mechanik, Vol. 16, Issue 6
Evaporation Method for Measuring Unsaturated Hydraulic Properties of Soils: Extending the Measurement Range
journal, July 2010
- Schindler, U.; Durner, W.; von Unold, G.
- Soil Science Society of America Journal, Vol. 74, Issue 4
The expansion of maize root-cap mucilage during hydration. 3. Changes in water potential and water content
journal, January 1997
- McCully, M. E.; Boyer, J. S.
- Physiologia Plantarum, Vol. 99, Issue 1