A novel method to evaluate nutrient retention by biological soil crust exopolymeric matrix
Abstract
Biological soil crusts (biocrusts) are microbial communities commonly found in the upper layer of arid soils. These microorganisms release exopolysaccharides (EPS), which form the exopolymeric matrix (EPM), allowing them to bond soil particles together and survive long periods of dryness. The aim of this paper is to develop methods for measuring metabolite retention by biocrust EPM and EPS. We report new methods for the investigation of metabolite sorption on biocrusts compared to the underlying unconsolidated subcrust fraction. A 13C–labeled bacterial lysate metabolite mixture was incubated with biocrust, subcrust and biocrust-extracted EPS. Non-sorbed metabolites were extracted and analyzed by liquid chromatography/mass spectrometry. This simple and rapid approach enabled the comparison of metabolite sorption on the biocrust EPM or EPS versus mineral sorption on the underlying soils. Our results suggest that the biocrust (and its extracted EPS) sorb more metabolites, especially amino acids and organic acids, than the underlying subcrust. This study demonstrates a useful method to highlight the essential role of biocrust (especially the EPM), which acts as a passive nutrient filter, sequestering metabolites released by microbes during wetting events. Finally, this may facilitate recovery of the community upon wetting and further enhance biocrust survival and nutrient retention.
- Authors:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
- Univ. of Florence (Italy). Dept. of Agrifood Production and Environmental Sciences; CNR Inst. of Ecosystem Study, Sesto Fiorentino (Italy)
- Univ. of Florence (Italy). Dept. of Agrifood Production and Environmental Sciences
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1477354
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Plant and Soil
- Additional Journal Information:
- Journal Volume: 429; Journal Issue: 1-2; Journal ID: ISSN 0032-079X
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; biological soil crusts; exopolymeric matrix; exopolysaccharides; metabolomics; sorption
Citation Formats
Swenson, Tami L., Couradeau, Estelle, Bowen, Benjamin P., De Philippis, Roberto, Rossi, Federico, Mugnai, Gianmarco, and Northen, Trent R. A novel method to evaluate nutrient retention by biological soil crust exopolymeric matrix. United States: N. p., 2017.
Web. doi:10.1007/s11104-017-3537-x.
Swenson, Tami L., Couradeau, Estelle, Bowen, Benjamin P., De Philippis, Roberto, Rossi, Federico, Mugnai, Gianmarco, & Northen, Trent R. A novel method to evaluate nutrient retention by biological soil crust exopolymeric matrix. United States. https://doi.org/10.1007/s11104-017-3537-x
Swenson, Tami L., Couradeau, Estelle, Bowen, Benjamin P., De Philippis, Roberto, Rossi, Federico, Mugnai, Gianmarco, and Northen, Trent R. Fri .
"A novel method to evaluate nutrient retention by biological soil crust exopolymeric matrix". United States. https://doi.org/10.1007/s11104-017-3537-x. https://www.osti.gov/servlets/purl/1477354.
@article{osti_1477354,
title = {A novel method to evaluate nutrient retention by biological soil crust exopolymeric matrix},
author = {Swenson, Tami L. and Couradeau, Estelle and Bowen, Benjamin P. and De Philippis, Roberto and Rossi, Federico and Mugnai, Gianmarco and Northen, Trent R.},
abstractNote = {Biological soil crusts (biocrusts) are microbial communities commonly found in the upper layer of arid soils. These microorganisms release exopolysaccharides (EPS), which form the exopolymeric matrix (EPM), allowing them to bond soil particles together and survive long periods of dryness. The aim of this paper is to develop methods for measuring metabolite retention by biocrust EPM and EPS. We report new methods for the investigation of metabolite sorption on biocrusts compared to the underlying unconsolidated subcrust fraction. A 13C–labeled bacterial lysate metabolite mixture was incubated with biocrust, subcrust and biocrust-extracted EPS. Non-sorbed metabolites were extracted and analyzed by liquid chromatography/mass spectrometry. This simple and rapid approach enabled the comparison of metabolite sorption on the biocrust EPM or EPS versus mineral sorption on the underlying soils. Our results suggest that the biocrust (and its extracted EPS) sorb more metabolites, especially amino acids and organic acids, than the underlying subcrust. This study demonstrates a useful method to highlight the essential role of biocrust (especially the EPM), which acts as a passive nutrient filter, sequestering metabolites released by microbes during wetting events. Finally, this may facilitate recovery of the community upon wetting and further enhance biocrust survival and nutrient retention.},
doi = {10.1007/s11104-017-3537-x},
journal = {Plant and Soil},
number = 1-2,
volume = 429,
place = {United States},
year = {Fri Dec 29 00:00:00 EST 2017},
month = {Fri Dec 29 00:00:00 EST 2017}
}
Web of Science
Figures / Tables:
Works referenced in this record:
The potential roles of biological soil crusts in dryland hydrologic cycles
journal, January 2006
- Belnap, Jayne
- Hydrological Processes, Vol. 20, Issue 15
Microenvironments and Microscale Productivity of Cyanobacterial Desert Crusts1
journal, October 1996
- Garcia-Pichel, Ferran; Belnap, Jayne
- Journal of Phycology, Vol. 32, Issue 5
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?
journal, January 2018
- Sasse, Joelle; Martinoia, Enrico; Northen, Trent
- Trends in Plant Science, Vol. 23, Issue 1
Characterization and Biological Implications of Scytonemin, a Cyanobacterial Sheath Pigment1
journal, June 1991
- Garcia-Pichel, Ferran; Castenholz, Richard W.
- Journal of Phycology, Vol. 27, Issue 3
Development of the polysaccharidic matrix in biocrusts induced by a cyanobacterium inoculated in sand microcosms
journal, September 2017
- Mugnai, Gianmarco; Rossi, Federico; Felde, Vincent John Martin Noah Linus
- Biology and Fertility of Soils, Vol. 54, Issue 1
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases
journal, July 2015
- Yao, Yushu; Sun, Terence; Wang, Tony
- Metabolites, Vol. 5, Issue 3
Competitive sorption of microbial metabolites on an iron oxide mineral
journal, November 2015
- Swenson, Tami L.; Bowen, Benjamin P.; Nico, Peter S.
- Soil Biology and Biochemistry, Vol. 90
Bacteria increase arid-land soil surface temperature through the production of sunscreens
journal, January 2016
- Couradeau, Estelle; Karaoz, Ulas; Lim, Hsiao Chien
- Nature Communications, Vol. 7, Issue 1
Aeolian dust in Colorado Plateau soils: Nutrient inputs and recent change in source
journal, June 2001
- Reynolds, R.; Belnap, J.; Reheis, M.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 13
Production of Pullulan and other Exopolysaccharides by Filamentous Fungi
journal, January 1992
- Seviour, R. J.; Stasinopoulos, S. J.; Auer, D. P. F.
- Critical Reviews in Biotechnology, Vol. 12, Issue 3
Do development stages of biological soil crusts determine activity and functional diversity in a sand-dune ecosystem?
journal, August 2012
- Yu, Jun; Kidron, Giora J.; Pen-Mouratov, Stanislav
- Soil Biology and Biochemistry, Vol. 51
Water repellency and pore clogging at early successional stages of microbiotic crusts on inland dunes, Brandenburg, NE Germany
journal, January 2010
- Fischer, Thomas; Veste, Maik; Wiehe, Wolfgang
- CATENA, Vol. 80, Issue 1
What distinguishes cyanobacteria able to revive after desiccation from those that cannot: the genome aspect: Desiccation Resistance Genes in Cyanobacteria
journal, August 2016
- Murik, Omer; Oren, Nadav; Shotland, Yoram
- Environmental Microbiology, Vol. 19, Issue 2
Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem
journal, May 2012
- Johnson, Shannon L.; Kuske, Cheryl R.; Carney, Travis D.
- Global Change Biology, Vol. 18, Issue 8
Revisiting classic water erosion models in drylands: The strong impact of biological soil crusts
journal, September 2008
- Bowker, Matthew A.; Belnap, Jayne; Bala Chaudhary, V.
- Soil Biology and Biochemistry, Vol. 40, Issue 9
Effects of inoculated Microcoleus vaginatus on the structure and function of biological soil crusts of desert
journal, December 2010
- Zheng, Yunpu; Xu, Ming; Zhao, Jiancheng
- Biology and Fertility of Soils, Vol. 47, Issue 4
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
Microbial Stress-Response Physiology and its Implications for Ecosystem Function
journal, June 2007
- Schimel, Joshua; Balser, Teri C.; Wallenstein, Matthew
- Ecology, Vol. 88, Issue 6
Adsorption of nucleotides onto Fe–Mg–Al rich swelling clays
journal, November 2013
- Feuillie, Cécile; Daniel, Isabelle; Michot, Laurent J.
- Geochimica et Cosmochimica Acta, Vol. 120
Cyanobacterial reuse of extracellular organic carbon in microbial mats
journal, October 2015
- Stuart, Rhona K.; Mayali, Xavier; Lee, Jackson Z.
- The ISME Journal, Vol. 10, Issue 5
Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust
journal, June 2013
- Rajeev, Lara; da Rocha, Ulisses Nunes; Klitgord, Niels
- The ISME Journal, Vol. 7, Issue 11
Changes in biocrust cover drive carbon cycle responses to climate change in drylands
journal, September 2013
- Maestre, Fernando T.; Escolar, Cristina; de Guevara, Mónica Ladrón
- Global Change Biology, Vol. 19, Issue 12
Long-term effects of UV and visible irradiance on natural populations of a scytonemin-containing cyanobacterium (Calothrix sp.)
journal, December 1997
- Brenowitz, Stephan; Castenholz, Richard W.
- FEMS Microbiology Ecology, Vol. 24, Issue 4
Macromolecular and chemical features of the excreted extracellular polysaccharides in induced biological soil crusts of different ages
journal, November 2014
- Chen, Lanzhou; Rossi, Federico; Deng, Songqiang
- Soil Biology and Biochemistry, Vol. 78
The biofilm matrix
journal, August 2010
- Flemming, Hans-Curt; Wingender, Jost
- Nature Reviews Microbiology, Vol. 8, Issue 9
Exometabolite niche partitioning among sympatric soil bacteria
journal, September 2015
- Baran, Richard; Brodie, Eoin L.; Mayberry-Lewis, Jazmine
- Nature Communications, Vol. 6, Issue 1
Small-Scale Vertical Distribution of Bacterial Biomass and Diversity in Biological Soil Crusts from Arid Lands in the Colorado Plateau
journal, November 2003
- Garcia-Pichel, F.; Johnson, S. L.; Youngkin, D.
- Microbial Ecology, Vol. 46, Issue 3
Cytoplasmic Vitrification and Survival of Anhydrobiotic Organisms
journal, July 1997
- Sun, Wendell Q.; Leopold, A. Carl
- Comparative Biochemistry and Physiology Part A: Physiology, Vol. 117, Issue 3
Microbial secreted exopolysaccharides affect the hydrological behavior of induced biological soil crusts in desert sandy soils
journal, January 2014
- Colica, Giovanni; Li, Hua; Rossi, Federico
- Soil Biology and Biochemistry, Vol. 68
Cyanobacteria track water in desert soils
journal, September 2001
- Garcia-Pichel, Ferran; Pringault, Olivier
- Nature, Vol. 413, Issue 6854
The role of the exopolysaccharides in enhancing hydraulic conductivity of biological soil crusts
journal, March 2012
- Rossi, Federico; Potrafka, Ruth M.; Pichel, Ferran Garcia
- Soil Biology and Biochemistry, Vol. 46
The adsorption of short single-stranded DNA oligomers to mineral surfaces
journal, June 2011
- James Cleaves, H.; Crapster-Pregont, Ellen; Jonsson, Caroline M.
- Chemosphere, Vol. 83, Issue 11
Extracellular polysaccharides from cyanobacterial soil crusts: A review of their role in dryland soil processes
journal, February 2011
- Mager, D. M.; Thomas, A. D.
- Journal of Arid Environments, Vol. 75, Issue 2
Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly
journal, September 2009
- Pereira, Sara; Zille, Andrea; Micheletti, Ernesto
- FEMS Microbiology Reviews, Vol. 33, Issue 5
Effect of biological soil crusts on soil elemental concentrations: implications for biogeochemistry and as traceable biosignatures of ancient life on land
journal, June 2009
- Beraldi-Campesi, H.; Hartnett, H. E.; Anbar, A.
- Geobiology, Vol. 7, Issue 3
Response of desert biological soil crusts to alterations in precipitation frequency
journal, December 2003
- Belnap, Jayne; Phillips, Susan L.; Miller, Mark E.
- Oecologia, Vol. 141, Issue 2
Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material
journal, May 2013
- Steven, Blaire; Gallegos-Graves, La Verne; Belnap, Jayne
- FEMS Microbiology Ecology, Vol. 86, Issue 1
Exocellular polysaccharides from cyanobacteria and their possible applications
journal, September 1998
- De Philippis, R.
- FEMS Microbiology Reviews, Vol. 22, Issue 3
A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces
journal, June 2007
- Kleber, M.; Sollins, P.; Sutton, R.
- Biogeochemistry, Vol. 85, Issue 1
The Evolution of a Capacity to Build Supra-Cellular Ropes Enabled Filamentous Cyanobacteria to Colonize Highly Erodible Substrates
journal, November 2009
- Garcia-Pichel, Ferran; Wojciechowski, Martin F.
- PLoS ONE, Vol. 4, Issue 11
The Community and Phylogenetic Diversity of Biological Soil Crusts in the Colorado Plateau Studied by Molecular Fingerprinting and Intensive Cultivation
journal, May 2006
- Gundlapally, Sathyanarayana Reddy; Garcia-Pichel, Ferran
- Microbial Ecology, Vol. 52, Issue 2
Exopolysaccharide-producing cyanobacteria in heavy metal removal from water: molecular basis and practical applicability of the biosorption process
journal, October 2011
- De Philippis, Roberto; Colica, Giovanni; Micheletti, Ernesto
- Applied Microbiology and Biotechnology, Vol. 92, Issue 4
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
Untargeted soil metabolomics methods for analysis of extractable organic matter
journal, January 2015
- Swenson, Tami L.; Jenkins, Stefan; Bowen, Benjamin P.
- Soil Biology and Biochemistry, Vol. 80
Exopolymeric substances of sulfate-reducing bacteria: Interactions with calcium at alkaline pH and implication for formation of carbonate minerals
journal, December 2007
- Braissant, O.; Decho, A. W.; Dupraz, C.
- Geobiology, Vol. 5, Issue 4
Role of Cyanobacterial Exopolysaccharides in Phototrophic Biofilms and in Complex Microbial Mats
journal, April 2015
- Rossi, Federico; De Philippis, Roberto
- Life, Vol. 5, Issue 2
Works referencing / citing this record:
Soil Type and Cyanobacteria Species Influence the Macromolecular and Chemical Characteristics of the Polysaccharidic Matrix in Induced Biocrusts
journal, December 2018
- Chamizo, Sonia; Adessi, Alessandra; Mugnai, Gianmarco
- Microbial Ecology, Vol. 78, Issue 2
Biocrusts: the living skin of the earth
journal, July 2018
- Bowker, Matthew A.; Reed, Sasha C.; Maestre, Fernando T.
- Plant and Soil, Vol. 429, Issue 1-2
A practical guide to measuring functional indicators and traits in biocrusts
journal, July 2019
- Mallen‐Cooper, Max; Bowker, Matthew A.; Antoninka, Anita J.
- Restoration Ecology, Vol. 28, Issue S2
Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere
journal, April 2019
- Couradeau, Estelle; Giraldo-Silva, Ana; De Martini, Francesca
- Microbiome, Vol. 7, Issue 1
Preliminary evidences of the presence of extracellular DNA single stranded forms in soil
journal, January 2020
- Pathan, Shamina Imran; Arfaioli, Paola; Ceccherini, Maria Teresa
- PLOS ONE, Vol. 15, Issue 1
Soil Type and Cyanobacteria Species Influence the Macromolecular and Chemical Characteristics of the Polysaccharidic Matrix in Induced Biocrusts
journal, December 2018
- Chamizo, Sonia; Adessi, Alessandra; Mugnai, Gianmarco
- Microbial Ecology, Vol. 78, Issue 2
Preliminary evidences of the presence of extracellular DNA single stranded forms in soil
journal, January 2020
- Pathan, Shamina Imran; Arfaioli, Paola; Ceccherini, Maria Teresa
- PLOS ONE, Vol. 15, Issue 1
Figures / Tables found in this record: