Bacteria increase arid-land soil surface temperature through the production of sunscreens
Abstract
Soil surface temperature, an important driver of terrestrial biogeochemical processes, depends strongly on soil albedo, which can be significantly modified by factors such as plant cover. In sparsely vegetated lands, the soil surface can be colonized by photosynthetic microbes that build biocrust communities. Here we use concurrent physical, biochemical and microbiological analyses to show that mature biocrusts can increase surface soil temperature by as much as 10 °C through the accumulation of large quantities of a secondary metabolite, the microbial sunscreen scytonemin, produced by a group of late-successional cyanobacteria. Scytonemin accumulation decreases soil albedo significantly. Such localized warming has apparent and immediate consequences for the soil microbiome, inducing the replacement of thermosensitive bacterial species with more thermotolerant forms. These results reveal that not only vegetation but also microorganisms are a factor in modifying terrestrial albedo, potentially impacting biosphere feedbacks on past and future climate, and call for a direct assessment of such effects at larger scales.
- Authors:
-
- Arizona State Univ., Tempe, AZ (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
- Arizona State Univ., Tempe, AZ (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1255544
- Alternate Identifier(s):
- OSTI ID: 1379041
- Grant/Contract Number:
- AC02- 05CH11231; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 7; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Couradeau, Estelle, Karaoz, Ulas, Lim, Hsiao Chien, Nunes da Rocha, Ulisses, Northen, Trent, Brodie, Eoin, and Garcia-Pichel, Ferran. Bacteria increase arid-land soil surface temperature through the production of sunscreens. United States: N. p., 2016.
Web. doi:10.1038/ncomms10373.
Couradeau, Estelle, Karaoz, Ulas, Lim, Hsiao Chien, Nunes da Rocha, Ulisses, Northen, Trent, Brodie, Eoin, & Garcia-Pichel, Ferran. Bacteria increase arid-land soil surface temperature through the production of sunscreens. United States. doi:10.1038/ncomms10373.
Couradeau, Estelle, Karaoz, Ulas, Lim, Hsiao Chien, Nunes da Rocha, Ulisses, Northen, Trent, Brodie, Eoin, and Garcia-Pichel, Ferran. Wed .
"Bacteria increase arid-land soil surface temperature through the production of sunscreens". United States. doi:10.1038/ncomms10373. https://www.osti.gov/servlets/purl/1255544.
@article{osti_1255544,
title = {Bacteria increase arid-land soil surface temperature through the production of sunscreens},
author = {Couradeau, Estelle and Karaoz, Ulas and Lim, Hsiao Chien and Nunes da Rocha, Ulisses and Northen, Trent and Brodie, Eoin and Garcia-Pichel, Ferran},
abstractNote = {Soil surface temperature, an important driver of terrestrial biogeochemical processes, depends strongly on soil albedo, which can be significantly modified by factors such as plant cover. In sparsely vegetated lands, the soil surface can be colonized by photosynthetic microbes that build biocrust communities. Here we use concurrent physical, biochemical and microbiological analyses to show that mature biocrusts can increase surface soil temperature by as much as 10 °C through the accumulation of large quantities of a secondary metabolite, the microbial sunscreen scytonemin, produced by a group of late-successional cyanobacteria. Scytonemin accumulation decreases soil albedo significantly. Such localized warming has apparent and immediate consequences for the soil microbiome, inducing the replacement of thermosensitive bacterial species with more thermotolerant forms. These results reveal that not only vegetation but also microorganisms are a factor in modifying terrestrial albedo, potentially impacting biosphere feedbacks on past and future climate, and call for a direct assessment of such effects at larger scales.},
doi = {10.1038/ncomms10373},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {1}
}
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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
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
Surface disturbances: Their role in accelerating desertification
journal, January 1995
- Belnap, Jayne
- Environmental Monitoring and Assessment, Vol. 37, Issue 1-3
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
Quality control and preprocessing of metagenomic datasets
journal, January 2011
- Schmieder, R.; Edwards, R.
- Bioinformatics, Vol. 27, Issue 6
The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts
journal, October 1996
- Mazor, Gideon; Kidron, Giora J.; Vonshak, Ahuva
- FEMS Microbiology Ecology, Vol. 21, Issue 2
Remote sensing of biological soil crust under simulated climate change manipulations in the Mojave Desert
journal, February 2009
- Ustin, Susan L.; Valko, Phillip G.; Kefauver, Shawn C.
- Remote Sensing of Environment, Vol. 113, Issue 2
Targeted and shotgun metagenomic approaches provide different descriptions of dryland soil microbial communities in a manipulated field study: Sequencing to describe dryland soil communities
journal, February 2012
- Steven, Blaire; Gallegos-Graves, La Verne; Starkenburg, Shawn R.
- Environmental Microbiology Reports, Vol. 4, Issue 2
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
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
MUST, a computer package of Management Utilities for Sequences and Trees
journal, January 1993
- Philippe, Hervé
- Nucleic Acids Research, Vol. 21, Issue 22
Phylogenetic and Morphological Diversity of Cyanobacteria in Soil Desert Crusts from the Colorado Plateau
journal, April 2001
- Garcia-Pichel, F.; Lopez-Cortes, A.; Nubel, U.
- Applied and Environmental Microbiology, Vol. 67, Issue 4
PANDAseq: paired-end assembler for illumina sequences
journal, January 2012
- Masella, Andre P.; Bartram, Andrea K.; Truszkowski, Jakub M.
- BMC Bioinformatics, Vol. 13, Issue 1
Micrometeorological modeling to understand the thermal anomaly in the sand dunes across the Israel–Egypt border
journal, June 2002
- Qin, Zhihao; Berliner, Pedro; Karnieli, Arnon
- Journal of Arid Environments, Vol. 51, Issue 2
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
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
Response and resilience of soil biocrust bacterial communities to chronic physical disturbance in arid shrublands
journal, November 2011
- Kuske, Cheryl R.; Yeager, Chris M.; Johnson, Shannon
- The ISME Journal, Vol. 6, Issue 4
Modern Terrestrial Sedimentary Biostructures and Their Fossil Analogs in Mesoproterozoic Subaerial Deposits
journal, February 2014
- Beraldi-Campesi, H.; Farmer, J. D.; Garcia-Pichel, F.
- PALAIOS, Vol. 29, Issue 2
Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests
journal, June 2008
- Bonan, G. B.
- Science, Vol. 320, Issue 5882
Surface Albedo and Desertification
journal, September 1975
- Jackson, R. D.; Idso, S. B.; Otterman, J.
- Science, Vol. 189, Issue 4207
MAFFT version 5: improvement in accuracy of multiple sequence alignment
journal, January 2005
- Katoh, K.
- Nucleic Acids Research, Vol. 33, Issue 2
Terrestrial Ecosystem Feedbacks to Global Climate Change
journal, November 1997
- Lashof and, Daniel A.; DeAngelo, Benjamin J.; Saleska and, Scott R.
- Annual Review of Energy and the Environment, Vol. 22, Issue 1
Temperature Drives the Continental-Scale Distribution of Key Microbes in Topsoil Communities
journal, June 2013
- Garcia-Pichel, Ferran; Loza, Virginia; Marusenko, Yevgeniy
- Science, Vol. 340, Issue 6140
Examining the global distribution of dominant archaeal populations in soil
journal, November 2010
- Bates, Scott T.; Berg-Lyons, Donna; Caporaso, J. Gregory
- The ISME Journal, Vol. 5, Issue 5
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 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
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
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
Diurnal Relationship Between the Surface Albedo and Surface Temperature in Revegetated Desert Ecosystems, Northwestern China
journal, January 2012
- Zhang, Ya-Feng; Wang, Xin-Ping; Pan, Yan-Xia
- Arid Land Research and Management, Vol. 26, Issue 1
Evaluation of vegetation cover and land-surface albedo in MPI-ESM CMIP5 simulations: VEGETATION AND LAND ALBEDO IN MPI-ESM
journal, February 2013
- Brovkin, V.; Boysen, L.; Raddatz, T.
- Journal of Advances in Modeling Earth Systems, Vol. 5, Issue 1
Surface Roughness Effects on Soil Albedo
journal, January 2000
- Matthias, A. D.; Fimbres, A.; Sano, E. E.
- Soil Science Society of America Journal, Vol. 64, Issue 3
The climatic impact of a Sonoran vegetation discontinuity
journal, August 1988
- Balling, RobertC.
- Climatic Change, Vol. 13, Issue 1
Works referencing / citing this record:
Warming reduces the cover, richness and evenness of lichen-dominated biocrusts but promotes moss growth: insights from an 8 yr experiment
journal, January 2018
- Ladrón de Guevara, Mónica; Gozalo, Beatriz; Raggio, José
- New Phytologist, Vol. 220, Issue 3
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
Exposure to predicted precipitation patterns decreases population size and alters community structure of cyanobacteria in biological soil crusts from the Chihuahuan Desert: Changing rainfall effects on soil cyanobacteria
journal, December 2017
- Fernandes, Vanessa M. C.; Machado de Lima, Náthali Maria; Roush, Daniel
- Environmental Microbiology, Vol. 20, Issue 1
Characterization of maximum land surface temperatures in 16 years from MODIS in Iran
journal, June 2018
- Khandan, Reza; Gholamnia, Mehdi; Duan, Si-Bo
- Environmental Earth Sciences, Vol. 77, Issue 12
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
Spectral Response Analysis: An Indirect and Non-Destructive Methodology for the Chlorophyll Quantification of Biocrusts
journal, June 2019
- Román, José Raúl; Rodríguez-Caballero, Emilio; Rodríguez-Lozano, Borja
- Remote Sensing, Vol. 11, Issue 11
Diversity and mineral substrate preference in endolithic microbial communities from marine intertidal outcrops (Isla de Mona, Puerto Rico)
journal, January 2017
- Couradeau, Estelle; Roush, Daniel; Guida, Brandon Scott
- Biogeosciences, Vol. 14, Issue 2
Biological soil crusts: diminutive communities of potential global importance
journal, March 2017
- Ferrenberg, Scott; Tucker, Colin L.; Reed, Sasha C.
- Frontiers in Ecology and the Environment, Vol. 15, Issue 3
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
Characterization of maximum land surface temperatures in 16 years from MODIS in Iran
journal, June 2018
- Khandan, Reza; Gholamnia, Mehdi; Duan, Si-Bo
- Environmental Earth Sciences, Vol. 77, Issue 12
Exposure to predicted precipitation patterns decreases population size and alters community structure of cyanobacteria in biological soil crusts from the Chihuahuan Desert: Changing rainfall effects on soil cyanobacteria
journal, December 2017
- Fernandes, Vanessa M. C.; Machado de Lima, Náthali Maria; Roush, Daniel
- Environmental Microbiology, Vol. 20, Issue 1
Warming reduces the cover, richness and evenness of lichen-dominated biocrusts but promotes moss growth: insights from an 8 yr experiment
journal, January 2018
- Ladrón de Guevara, Mónica; Gozalo, Beatriz; Raggio, José
- New Phytologist, Vol. 220, Issue 3
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
Spectral Response Analysis: An Indirect and Non-Destructive Methodology for the Chlorophyll Quantification of Biocrusts
journal, June 2019
- Román, José Raúl; Rodríguez-Caballero, Emilio; Rodríguez-Lozano, Borja
- Remote Sensing, Vol. 11, Issue 11
Diversity and mineral substrate preference in endolithic microbial communities from marine intertidal outcrops (Isla de Mona, Puerto Rico)
journal, January 2017
- Couradeau, Estelle; Roush, Daniel; Guida, Brandon Scott
- Biogeosciences, Vol. 14, Issue 2
Microbial communities from arid environments on a global scale. A systematic review
journal, July 2020
- Vásquez-Dean, Javiera; Maza, Felipe; Morel, Isidora
- Biological Research, Vol. 53, Issue 1
A predictive model for the spectral “bioalbedo” of snow: Bioalbedo of Snow
journal, January 2017
- Cook, J. M.; Hodson, A. J.; Taggart, A. J.
- Journal of Geophysical Research: Earth Surface, Vol. 122, Issue 1
Simulated climate change affects how biocrusts modulate water gains and desiccation dynamics after rainfall events
journal, January 2018
- Lafuente, Angela; Berdugo, Miguel; Ladrón de Guevara, Mónica
- Ecohydrology, Vol. 11, Issue 6
Biocrusts and their disturbance mediate the recruitment of native and exotic grasses from a hot desert ecosystem
journal, July 2018
- Havrilla, Caroline A.; Barger, Nichole N.
- Ecosphere, Vol. 9, Issue 7
Restoring soil functions by means of cyanobacteria inoculation: Importance of soil conditions and species selection
journal, July 2018
- Román, José Raúl; Roncero-Ramos, Beatriz; Chamizo, Sonia
- Land Degradation & Development, Vol. 29, Issue 9
Grazing pressure interacts with aridity to determine the development and diversity of biological soil crusts in Patagonian rangelands
journal, December 2019
- Velasco Ayuso, Sergio; Oñatibia, Gastón R.; Maestre, Fernando T.
- Land Degradation & Development, Vol. 31, Issue 4
Biocrust morphology is linked to marked differences in microbial community composition
journal, October 2017
- Chilton, Angela M.; Neilan, Brett A.; Eldridge, David J.
- Plant and Soil, Vol. 429, Issue 1-2
Establishing rates of lateral expansion of cyanobacterial biological soil crusts for optimal restoration
journal, June 2018
- Sorochkina, Kira; Velasco Ayuso, Sergio; Garcia-Pichel, Ferran
- Plant and Soil, Vol. 429, Issue 1-2
Soil surface disturbance alters cyanobacterial biocrusts and soil properties in dry grassland and shrubland ecosystems
journal, June 2019
- Chung, Y. Anny; Thornton, Bradly; Dettweiler-Robinson, Eva
- Plant and Soil, Vol. 441, Issue 1-2
Assessing the influence of soil abiotic and biotic factors on Nostoc commune inoculation success
journal, August 2019
- Roncero-Ramos, B.; Román, J. R.; Rodríguez-Caballero, E.
- Plant and Soil, Vol. 444, Issue 1-2
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
Albedo feedbacks to future climate via climate change impacts on dryland biocrusts
journal, March 2017
- Rutherford, William A.; Painter, Thomas H.; Ferrenberg, Scott
- Scientific Reports, Vol. 7, Issue 1
Cyanobacterial diversity of western European biological soil crusts along a latitudinal gradient
journal, July 2016
- Williams, Laura; Loewen-Schneider, Katharina; Maier, Stefanie
- FEMS Microbiology Ecology, Vol. 92, Issue 10
Biophysical processes supporting the diversity of microbial life in soil
journal, August 2017
- Tecon, Robin; Or, Dani
- FEMS Microbiology Reviews, Vol. 41, Issue 5
Genomic and transcriptomic insights into the survival of the subaerial cyanobacterium Nostoc flagelliforme in arid and exposed habitats: Cyanobacteria in arid and exposed habitats
journal, January 2019
- Shang, Jin-Long; Chen, Min; Hou, Shengwei
- Environmental Microbiology, Vol. 21, Issue 2
Factors influencing pigment production by halophilic bacteria and its effect on brine evaporation rates
journal, October 2018
- Silva-Castro, Gloria Andrea; Moyo, Anesu Conrad; Khumalo, Londiwe
- Microbial Biotechnology, Vol. 12, Issue 2
Altering biocrusts for an altered climate
journal, February 2016
- Young, Kristina E.; Grover, Henry S.; Bowker, Matthew A.
- New Phytologist, Vol. 210, Issue 1
Matworld - the biogeochemical effects of early life on land
journal, November 2016
- Lenton, Timothy M.; Daines, Stuart J.
- New Phytologist, Vol. 215, Issue 2
Cyanobacterial biocrust diversity in Mediterranean ecosystems along a latitudinal and climatic gradient
journal, July 2018
- Muñoz-Martín, M. Ángeles; Becerra-Absalón, Itzel; Perona, Elvira
- New Phytologist, Vol. 221, Issue 1
Nursing biocrusts: isolation, cultivation, and fitness test of indigenous cyanobacteria: Nursing biocrust cyanobacteria
journal, January 2019
- Giraldo-Silva, Ana; Nelson, Corey; Barger, Nichole N.
- Restoration Ecology, Vol. 27, Issue 4
Effect of preconditioning to the soil environment on the performance of 20 cyanobacterial strains used as inoculum for biocrust restoration
journal, November 2019
- Giraldo‐Silva, Ana; Nelson, Corey; Penfold, Cory
- Restoration Ecology, Vol. 28, Issue S2
Microbial Nursery Production of High-Quality Biological Soil Crust Biomass for Restoration of Degraded Dryland Soils
journal, November 2016
- Velasco Ayuso, Sergio; Giraldo Silva, Ana; Nelson, Corey
- Applied and Environmental Microbiology, Vol. 83, Issue 3
Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
journal, May 2019
- Garcia-Pichel, Ferran; Lombard, Jonathan; Soule, Tanya
- mBio, Vol. 10, Issue 3
Large Blooms of Bacillales ( Firmicutes ) Underlie the Response to Wetting of Cyanobacterial Biocrusts at Various Stages of Maturity
journal, March 2018
- Karaoz, Ulas; Couradeau, Estelle; da Rocha, Ulisses Nunes
- mBio, Vol. 9, Issue 2
The Compositionally Distinct Cyanobacterial Biocrusts From Brazilian Savanna and Their Environmental Drivers of Community Diversity
journal, December 2019
- Machado-de-Lima, Náthali Maria; Fernandes, Vanessa Moreira Câmara; Roush, Daniel
- Frontiers in Microbiology, Vol. 10