Large Blooms of Bacillales (Firmicutes) Underlie the Response to Wetting of Cyanobacterial Biocrusts at Various Stages of Maturity

Karaoz, Ulas; Couradeau, Estelle; da Rocha, Ulisses Nunes; Lim, Hsiao -Chien; Northen, Trent; Garcia-Pichel, Ferran; Brodie, Eoin L.; Bailey, Mark J.

doi:10.1128/mBio.01366-16

Title: Large Blooms of Bacillales (Firmicutes) Underlie the Response to Wetting of Cyanobacterial Biocrusts at Various Stages of Maturity

Journal Article · Tue Mar 06 00:00:00 EST 2018 · mBio (Online)

DOI:https://doi.org/10.1128/mBio.01366-16· OSTI ID:1465433

^[1]; Couradeau, Estelle ^[2]; da Rocha, Ulisses Nunes ^[3]; Lim, Hsiao -Chien ^[1]; Northen, Trent ^[1]; Garcia-Pichel, Ferran ^[4]; Brodie, Eoin L. ^[5]; Bailey, Mark J. ^[6]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Arizona State Univ., Tempe, AZ (United States); Univ. de Bourgogne, Dijon (France)
Helmholtz Centre for Environmental Research-UFZ, Leipzig (Germany)
Arizona State Univ., Tempe, AZ (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
CEH-Oxford

Biological soil crusts (biocrusts) account for a substantial portion of primary production in dryland ecosystems. They successionally mature to deliver a suite of ecosystem services, such as carbon sequestration, water retention and nutrient cycling, and climate regulation. Biocrust assemblages are extremely well adapted to survive desiccation and to rapidly take advantage of the periodic precipitation events typical of arid ecosystems. Here we focus on the wetting response of incipient cyanobacterial crusts as they mature from “light” to “dark.” We sampled a cyanobacterial biocrust chronosequence before (dry) and temporally following a controlled wetting event and used high-throughput 16S rRNA and rRNA gene sequencing to monitor the dynamics of microbial response. Overall, shorter-term changes in phylogenetic beta diversity attributable to periodic wetting were as large as those attributable to biocrust successional stage. Notably, more mature crusts showed significantly higher resistance to precipitation disturbance. A large bloom of a few taxa within the Firmicutes, primarily in the order Bacillales, emerged 18 h after wetting, while filamentous crust-forming cyanobacteria showed variable responses to wet-up across the successional gradient, with populations collapsing in less-developed light crusts but increasing in later-successional-stage dark crusts. Overall, the consistent Bacillales bloom accompanied by the variable collapse of pioneer cyanobacteria of the Oscillatoriales order across the successional gradient suggests that the strong response of few organisms to a hydration pulse with the mortality of the autotroph might have important implications for carbon (C) balance in semiarid ecosystems. IMPORTANCE Desert biological soil crusts are terrestrial topsoil microbial communities common to arid regions that comprise 40% of Earth’s terrestrial surface. They successionally develop over years to decades to deliver a suite of ecosystem services of local and global significance. Ecosystem succession toward maturity has been associated with both resistance and resilience to disturbance. Recent work has shown that the impacts of both climate change and physical disturbance on biocrusts increase the potential for successional resetting. A larger proportion of biocrusts are expected to be at an early developmental stage, hence increasing susceptibility to changes in precipitation frequencies. Therefore, it is essential to characterize how biocrusts respond to wetting across early developmental stages. In this study, we document the wetting response of microbial communities from a biocrust chronosequence. Overall, our results suggest that the cumulative effects of altered precipitation frequencies on the stability of biocrusts will depend on biocrust maturity.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1465433

Journal Information:: mBio (Online), Vol. 9, Issue 2; Related Information: © 2018 Karaoz et al.; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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References (92)

Microenvironments and Microscale Productivity of Cyanobacterial Desert Crusts1 Garcia-Pichel, Ferran; Belnap, Jayne Journal of Phycology, Vol. 32, Issue 5 https://doi.org/10.1111/j.0022-3646.1996.00774.x	journal	October 1996
Phylogenetic Resolution and Quantifying the Phylogenetic Diversity and Dispersion of Communities Swenson, Nathan G. PLoS ONE, Vol. 4, Issue 2 https://doi.org/10.1371/journal.pone.0004390	journal	February 2009
Microbial interactions: from networks to models Faust, Karoline; Raes, Jeroen Nature Reviews Microbiology, Vol. 10, Issue 8 https://doi.org/10.1038/nrmicro2832	journal	July 2012
UCHIME improves sensitivity and speed of chimera detection Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C. Bioinformatics, Vol. 27, Issue 16 https://doi.org/10.1093/bioinformatics/btr381	journal	June 2011
rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development Stoddard, Steven F.; Smith, Byron J.; Hein, Robert Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1201	journal	November 2014
Nitrogen Cycling Mediated by Biological soil Crusts and Arbuscular Mycorrhizal Fungi Hawkes, Christine V. Ecology, Vol. 84, Issue 6 https://doi.org/10.1890/0012-9658(2003)084[1553:NCMBBS]2.0.CO;2	journal	June 2003
Mineral and Bacterial Diversities of Desert Sand Grains from South-East Morocco Gommeaux, Maxime; Barakat, Mohamed; Montagnac, Gilles Geomicrobiology Journal, Vol. 27, Issue 1 https://doi.org/10.1080/01490450903393066	journal	January 2010
The Variability of the 16S rRNA Gene in Bacterial Genomes and Its Consequences for Bacterial Community Analyses Větrovský, Tomáš; Baldrian, Petr PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0057923	journal	February 2013
Revision of the genus Massilia La Scola et al. 2000, with an emended description of the genus and inclusion of all species of the genus Naxibacter as new combinations, and proposal of Massilia consociata sp. nov. Kampfer, P.; Lodders, N.; Martin, K. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 7 https://doi.org/10.1099/ijs.0.025585-0	journal	July 2010
Bacteria increase arid-land soil surface temperature through the production of sunscreens Couradeau, Estelle; Karaoz, Ulas; Lim, Hsiao Chien Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10373	journal	January 2016
Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture Curiel Yuste, J.; Baldocchi, D. D.; Gershenson, A. Global Change Biology, Vol. 13, Issue 9 https://doi.org/10.1111/j.1365-2486.2007.01415.x	journal	September 2007
Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils Steven, Blaire; Gallegos-Graves, La Verne; Yeager, Chris Soil Biology and Biochemistry, Vol. 69 https://doi.org/10.1016/j.soilbio.2013.11.008	journal	February 2014
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
Disturbance of biological soil crusts: impacts on potential wind erodibility of sandy desert soils in southeastern Utah Belnap, J.; Gillette, D. A. Land Degradation & Development, Vol. 8, Issue 4 https://doi.org/10.1002/(SICI)1099-145X(199712)8:4<355::AID-LDR266>3.0.CO;2-H	journal	December 1997
Phylogenetic and Morphological Diversity of Cyanobacteria in Soil Desert Crusts from the Colorado Plateau Garcia-Pichel, F.; Lopez-Cortes, A.; Nubel, U. Applied and Environmental Microbiology, Vol. 67, Issue 4 https://doi.org/10.1128/AEM.67.4.1902-1910.2001	journal	April 2001
Precipitation pulse size effects on Sonoran Desert soil microbial crusts Cable, Jessica M.; Huxman, Travis E. Oecologia, Vol. 141, Issue 2 https://doi.org/10.1007/s00442-003-1461-7	journal	December 2003
Taxonomic relatedness shapes bacterial assembly in activated sludge of globally distributed wastewater treatment plants: Taxonomic relatedness shapes AS bacterial assembly Ju, Feng; Xia, Yu; Guo, Feng Environmental Microbiology, Vol. 16, Issue 8 https://doi.org/10.1111/1462-2920.12355	journal	January 2014
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.104	journal	July 2013
Active and total microbial communities in forest soil are largely different and highly stratified during decomposition Baldrian, Petr; Kolařík, Miroslav; Štursová, Martina The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.95	journal	July 2011
Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem Johnson, Shannon L.; Kuske, Cheryl R.; Carney, Travis D. Global Change Biology, Vol. 18, Issue 8 https://doi.org/10.1111/j.1365-2486.2012.02709.x	journal	May 2012
Bacillus koreensis sp. nov., a spore-forming bacterium, isolated from the rhizosphere of willow roots in Korea Lim, J. -M. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 1 https://doi.org/10.1099/ijs.0.63701-0	journal	January 2006
Correlation detection strategies in microbial data sets vary widely in sensitivity and precision Weiss, Sophie; Van Treuren, Will; Lozupone, Catherine The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.235	journal	February 2016
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups Placella, S. A.; Brodie, E. L.; Firestone, M. K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1204306109	journal	June 2012
Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests Kembel, Steven W. Ecology Letters, Vol. 12, Issue 9 https://doi.org/10.1111/j.1461-0248.2009.01354.x	journal	September 2009
The ecological coherence of high bacterial taxonomic ranks Philippot, Laurent; Andersson, Siv G. E.; Battin, Tom J. Nature Reviews Microbiology, Vol. 8, Issue 7 https://doi.org/10.1038/nrmicro2367	journal	June 2010
Diversity and structure of soil bacterial communities associated with vultures in an African savanna Ganz, Holly H.; Karaoz, Ulas; Getz, Wayne M. Ecosphere, Vol. 3, Issue 6 https://doi.org/10.1890/ES11-00333.1	journal	June 2012
Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition Griffiths, R. I.; Whiteley, A. S.; O'Donnell, A. G. Applied and Environmental Microbiology, Vol. 66, Issue 12 https://doi.org/10.1128/AEM.66.12.5488-5491.2000	journal	December 2000
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Inferring Correlation Networks from Genomic Survey Data Friedman, Jonathan; Alm, Eric J. PLoS Computational Biology, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pcbi.1002687	journal	September 2012
UniFrac: an effective distance metric for microbial community comparison Lozupone, Catherine; Lladser, Manuel E.; Knights, Dan The ISME Journal, Vol. 5, Issue 2 https://doi.org/10.1038/ismej.2010.133	journal	September 2010
Phylogenies and Community Ecology Webb, Campbell O.; Ackerly, David D.; McPeek, Mark A. Annual Review of Ecology and Systematics, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.ecolsys.33.010802.150448	journal	November 2002
Testing the spatial phylogenetic structure of local communities: statistical performances of different null models and test statistics on a locally neutral community: Testing spatial community phylogenetic structure Hardy, Olivier J. Journal of Ecology, Vol. 96, Issue 5 https://doi.org/10.1111/j.1365-2745.2008.01421.x	journal	August 2008
Pyrosequencing enumerates and contrasts soil microbial diversity Roesch, Luiz F. W.; Fulthorpe, Roberta R.; Riva, Alberto The ISME Journal, Vol. 1, Issue 4 https://doi.org/10.1038/ismej.2007.53	journal	July 2007
Pattern pluralism and the Tree of Life hypothesis Doolittle, W. F.; Bapteste, E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 7 https://doi.org/10.1073/pnas.0610699104	journal	January 2007
Mapping the niche space of soil microorganisms using taxonomy and traits Lennon, Jay T.; Aanderud, Zachary T.; Lehmkuhl, B. K. Ecology, Vol. 93, Issue 8 https://doi.org/10.1890/11-1745.1	journal	August 2012
Temperature Drives the Continental-Scale Distribution of Key Microbes in Topsoil Communities Garcia-Pichel, Ferran; Loza, Virginia; Marusenko, Yevgeniy Science, Vol. 340, Issue 6140 https://doi.org/10.1126/science.1236404	journal	June 2013
Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust Rajeev, Lara; da Rocha, Ulisses Nunes; Klitgord, Niels The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.83	journal	June 2013
Microbial communities acclimate to recurring changes in soil redox potential status: Fluctuating redox microbial communities DeAngelis, Kristen M.; Silver, Whendee L.; Thompson, Andrew W. Environmental Microbiology, Vol. 12, Issue 12 https://doi.org/10.1111/j.1462-2920.2010.02286.x	journal	December 2010
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Patton's Tracks in the Mojave Desert, USA: An Ecological Legacy Belnap, Jayne; Warren, Steven D. Arid Land Research and Management, Vol. 16, Issue 3 https://doi.org/10.1080/153249802760284793	journal	January 2002
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
An examination of the bacteriophages and bacteria of the Namib desert Prestel, Eric; Salamitou, Sylvie; DuBow, Michael S. The Journal of Microbiology, Vol. 46, Issue 4 https://doi.org/10.1007/s12275-008-0007-4	journal	August 2008
Cross-biome metagenomic analyses of soil microbial communities and their functional attributes Fierer, N.; Leff, J. W.; Adams, B. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 52 https://doi.org/10.1073/pnas.1215210110	journal	December 2012
Exometabolite niche partitioning among sympatric soil bacteria Baran, Richard; Brodie, Eoin L.; Mayberry-Lewis, Jazmine Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9289	journal	September 2015
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Small-Scale Vertical Distribution of Bacterial Biomass and Diversity in Biological Soil Crusts from Arid Lands in the Colorado Plateau Garcia-Pichel, F.; Johnson, S. L.; Youngkin, D. Microbial Ecology, Vol. 46, Issue 3 https://doi.org/10.1007/s00248-003-1004-0	journal	November 2003
A global network of coexisting microbes from environmental and whole-genome sequence data Chaffron, S.; Rehrauer, H.; Pernthaler, J. Genome Research, Vol. 20, Issue 7 https://doi.org/10.1101/gr.104521.109	journal	May 2010
High Bacterial Diversity of Biological Soil Crusts in Water Tracks over Permafrost in the High Arctic Polar Desert Steven, Blaire; Lionard, Marie; Kuske, Cheryl R. PLoS ONE, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pone.0071489	journal	August 2013
Telluria mixta (Pseudomonas mixta Bowman, Sly, and Hayward 1988) gen. nov., comb. nov., and Telluria chitinolytica sp. nov., Soil-Dwelling Organisms Which Actively Degrade Polysaccharides Bowman, J. P.; Sly, L. I.; Hayward, A. C. International Journal of Systematic Bacteriology, Vol. 43, Issue 1 https://doi.org/10.1099/00207713-43-1-120	journal	January 1993
Exploring the Phylogenetic Structure of Ecological Communities: An Example for Rain Forest Trees Webb, Campbell O. The American Naturalist, Vol. 156, Issue 2 https://doi.org/10.1086/303378	journal	August 2000
Export of nitrogenous compounds due to incomplete cycling within biological soil crusts of arid lands Johnson, Shannon L.; Neuer, Susanne; Garcia-Pichel, Ferran Environmental Microbiology, Vol. 9, Issue 3 https://doi.org/10.1111/j.1462-2920.2006.01187.x	journal	March 2007
Bacillus beringensis sp. nov., a psychrotolerant bacterium isolated from the Bering Sea Yu, Yong; Li, Hui-Rong; Zeng, Yin-Xin Antonie van Leeuwenhoek, Vol. 99, Issue 3 https://doi.org/10.1007/s10482-010-9523-4	journal	October 2010
EFFECT OF WATER POTENTIAL ON A MICROCOLEUS (CYANOPHYCEAE) FROM A DESERT CRUST ¹ Brock, Thomas D. Journal of Phycology, Vol. 11, Issue 3 https://doi.org/10.1111/j.1529-8817.1975.tb02786.x	journal	September 1975
The vertical microdistribution of cyanobacteria and green algae within desert crusts and the development of the algal crusts Hu, Chunxiang; Zhang, Delu; Huang, Zebo Plant and Soil, Vol. 257, Issue 1 https://doi.org/10.1023/A:1026253307432	journal	November 2003
Bacillus korlensis sp. nov., a moderately halotolerant bacterium isolated from a sand soil sample in China Zhang, L.; Wang, Y.; Dai, J. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 7 https://doi.org/10.1099/ijs.0.004879-0	journal	June 2009
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities Schloss, P. D.; Westcott, S. L.; Ryabin, T. Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541 https://doi.org/10.1128/AEM.01541-09	journal	October 2009
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Deciphering microbial interactions and detecting keystone species with co-occurrence networks Berry, David; Widder, Stefanie Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00219	journal	May 2014
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Effect of biological soil crusts on soil elemental concentrations: implications for biogeochemistry and as traceable biosignatures of ancient life on land Beraldi-Campesi, H.; Hartnett, H. E.; Anbar, A. Geobiology, Vol. 7, Issue 3 https://doi.org/10.1111/j.1472-4669.2009.00204.x	journal	June 2009
Estimates of global cyanobacterial biomass and its distribution Garcia-Pichel, Ferran; Belnap, Jayne; Neuer, Susanne Algological Studies, Vol. 109, Issue 1 https://doi.org/10.1127/1864-1318/2003/0109-0213	journal	August 2003
Microbial seed banks: the ecological and evolutionary implications of dormancy Lennon, Jay T.; Jones, Stuart E. Nature Reviews Microbiology, Vol. 9, Issue 2 https://doi.org/10.1038/nrmicro2504	journal	January 2011
Interactions between Bacillus anthracis and Plants May Promote Anthrax Transmission Ganz, Holly H.; Turner, Wendy C.; Brodie, Eoin L. PLoS Neglected Tropical Diseases, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pntd.0002903	journal	June 2014
Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material Steven, Blaire; Gallegos-Graves, La Verne; Belnap, Jayne FEMS Microbiology Ecology, Vol. 86, Issue 1 https://doi.org/10.1111/1574-6941.12143	journal	May 2013
Tumebacillus ginsengisoli sp. nov., isolated from soil of a ginseng field Baek, S. -H.; Cui, Y.; Kim, S. -C. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 7 https://doi.org/10.1099/ijs.0.023358-0	journal	August 2010
Phylogenetic structure of angiosperm communities during tropical forest succession Letcher, Susan G. Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1678 https://doi.org/10.1098/rspb.2009.0865	journal	October 2009
The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria Chanal, Angelique; Chapon, Virginie; Benzerara, Karim Environmental Microbiology, Vol. 8, Issue 3 https://doi.org/10.1111/j.1462-2920.2005.00921.x	journal	March 2006
Massilia kyonggiensis sp. nov., isolated from forest soil in Korea Kim, Jaisoo Journal of Microbiology, Vol. 52, Issue 5 https://doi.org/10.1007/s12275-014-4010-7	journal	May 2014
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
ggplot2: Elegant Graphics for Data Analysis: Book Reviews Ginestet, Cedric Journal of the Royal Statistical Society: Series A (Statistics in Society), Vol. 174, Issue 1 https://doi.org/10.1111/j.1467-985X.2010.00676_9.x	journal	January 2011
The Evolution of a Capacity to Build Supra-Cellular Ropes Enabled Filamentous Cyanobacteria to Colonize Highly Erodible Substrates Garcia-Pichel, Ferran; Wojciechowski, Martin F. PLoS ONE, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pone.0007801	journal	November 2009
Elucidating the microbial resuscitation cascade in biological soil crusts following a simulated rain event: Microbial resuscitation in biological soil crusts Angel, Roey; Conrad, Ralf Environmental Microbiology https://doi.org/10.1111/1462-2920.12140	journal	May 2013
Niche partitioning of bacterial communities in biological crusts and soils under grasses, shrubs and trees in the Kalahari Elliott, David R.; Thomas, Andrew D.; Hoon, Stephen R. Biodiversity and Conservation, Vol. 23, Issue 7 https://doi.org/10.1007/s10531-014-0684-8	journal	April 2014
Picante: R tools for integrating phylogenies and ecology Kembel, S. W.; Cowan, P. D.; Helmus, M. R. Bioinformatics, Vol. 26, Issue 11 https://doi.org/10.1093/bioinformatics/btq166	journal	April 2010
Contribution of cryptogamic covers to the global cycles of carbon and nitrogen Elbert, Wolfgang; Weber, Bettina; Burrows, Susannah Nature Geoscience, Vol. 5, Issue 7 https://doi.org/10.1038/ngeo1486	journal	June 2012
Precipitation pulses and soil CO ₂ flux in a Sonoran Desert ecosystem Sponseller, Ryan A. Global Change Biology, Vol. 13, Issue 2 https://doi.org/10.1111/j.1365-2486.2006.01307.x	journal	February 2007
Biological soil crusts accelerate the nitrogen cycle through large NO and HONO emissions in drylands Weber, Bettina; Wu, Dianming; Tamm, Alexandra Proceedings of the National Academy of Sciences, Vol. 112, Issue 50 https://doi.org/10.1073/pnas.1515818112	journal	November 2015
Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons Haas, B. J.; Gevers, D.; Earl, A. M. Genome Research, Vol. 21, Issue 3 https://doi.org/10.1101/gr.112730.110	journal	January 2011
Toward a Census of Bacteria in Soil Schloss, Patrick D.; Handelsman, Jo PLoS Computational Biology, Vol. 2, Issue 7 https://doi.org/10.1371/journal.pcbi.0020092	journal	January 2006
Biogeographical patterns and mechanisms of microbial community assembly that underlie successional biocrusts across northern China Li, Yuanlong; Hu, Chunxiang npj Biofilms and Microbiomes, Vol. 7, Issue 1 https://doi.org/10.1038/s41522-021-00188-6	journal	February 2021
Microbial community structure and functional properties in permanently and seasonally flooded areas in Poyang Lake Liu, Yang; Ren, Ze; Qu, Xiaodong Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-61569-z	journal	March 2020
Database resources of the National Center for Biotechnology Information Wheeler, D. L. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj158	journal	January 2006
Systems Analysis of Gut Microbiome Influence on Metabolic Disease in HIV-Positive and High-Risk Populations Armstrong, Abigail J. S.; Quinn, Kevin; Fouquier, Jennifer mSystems, Vol. 6, Issue 3 https://doi.org/10.1128/msystems.01178-20	journal	June 2021
Succession of endophytic fungi and arbuscular mycorrhizal fungi associated with the growth of plant and their correlation with secondary metabolites in the roots of plants Dang, Hanli; Zhang, Tao; Wang, Zhongke BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-021-02942-6	journal	April 2021
Toward a census of bacteria in soil Schloss, Patrick David; Handelsman, Jo PLoS Computational Biology, Vol. preprint, Issue 2006 https://doi.org/10.1371/journal.pcbi.0020092.eor	journal	January 2005
Database resources of the National Center for Biotechnology Information Sayers, Eric W.; Beck, Jeffrey; Bolton, Evan E. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa892	journal	October 2020
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
Database resources of the National Center for Biotechnology Information Wheeler, D. L.; Barrett, T.; Benson, D. A. Nucleic Acids Research, Vol. 36, Issue Database https://doi.org/10.1093/nar/gkm1000	journal	December 2007
ggplot2: Elegant Graphics for Data Analysis Valero-Mora, Pedro M. Journal of Statistical Software, Vol. 35, Issue Book Review 1 https://doi.org/10.18637/jss.v035.b01	journal	January 2010
A global network of coexisting microbes from environmental and whole-genome sequence data Chaffron, S.; Rehrauer, H.; Pernthaler, J. Cold Spring Harbor Laboratory Press https://doi.org/10.5167/uzh-34788	text	January 2010
Database resources of the National Center for Biotechnology Information Sayers, Eric W.; Agarwala, Richa; Bolton, Evan E. Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1069	journal	November 2018

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59 BASIC BIOLOGICAL SCIENCES
Firmicutes
biological soil crust
carbon loss
ecological succession
ecosystem services
pulsed-activity event
resistance
stability

Title: Large Blooms of Bacillales (Firmicutes) Underlie the Response to Wetting of Cyanobacterial Biocrusts at Various Stages of Maturity

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