Response of Biological Soil Crust Diazotrophs to Season, Altered Summer Precipitation, and Year-Round Increased Temperature in an Arid Grassland of the Colorado Plateau, USA

Yeager, Chris M.; Kuske, Cheryl R.; Carney, Travis D.; Johnson, Shannon L.; Ticknor, Lawrence O.; Belnap, Jayne

doi:10.3389/fmicb.2012.00358

Response of Biological Soil Crust Diazotrophs to Season, Altered Summer Precipitation, and Year-Round Increased Temperature in an Arid Grassland of the Colorado Plateau, USA

Journal Article · Sun Jan 01 00:00:00 EST 2012 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2012.00358· OSTI ID:1396109

Yeager, Chris M. ^[1]; Kuske, Cheryl R. ^[1]; Carney, Travis D. ^[1]; Johnson, Shannon L. ^[1]; Ticknor, Lawrence O. ^[1]; Belnap, Jayne ^[2]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
U.S. Geological Survey, Moab, UT (United States). Southwest Biological Science Center

Biological soil crusts (biocrusts), which supply significant amounts of fixed nitrogen into terrestrial ecosystems worldwide (~33 Tg y^-1), are likely to respond to changes in temperature and precipitation associated with climate change. Using nifH gene-based surveys, we explored variation in the diazotrophic community of biocrusts of the Colorado Plateau, USA in response to season (autumn vs. spring), as well as field manipulations that increased the frequency of small volume precipitation events and year-round soil temperature. Abundance of nifH genes in biocrusts ranged from 3 × 10⁶ to 1 × 108 g^-1 soil, and nifH from heterocystous cyanobacteria closely related to Scytonema hyalinum, Spirirestis rafaelensis, and Nostoc commune comprised >98% of the total. Although there was no apparent seasonal effect on total nifH gene abundance in the biocrusts, T-RFLP analysis revealed a strong seasonal pattern in nifH composition. Spirirestis nifH abundance was estimated to oscillate 1 to >2 orders of magnitude between autumn (low) and spring (high). A year-round increase of soil temperature (2–3°C) had little effect on the diazotroph community structure over 2 years. Altered summer precipitation had little impact on diazotroph community structure over the first 1.5 years of the study, when natural background patterns across years and seasons superseded any treatment effects. However, after the second summer of treatments, nifH abundance was 2.6-fold lower in biocrusts receiving altered precipitation. Heterocystous cyanobacteria were apparently more resilient to altered precipitation than other cyanobacteria. The results demonstrate that diazotrophic community composition of biocrusts in this semi-arid grassland undergoes strong seasonal shifts and that the abundance of its dominant members decreased in response to more frequent, small volume precipitation events.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1396109

Report Number(s):: LA--UR-12-22741

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 3; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (50)

Nitrogen loss from deserts in the southwestern United States Peterjohn, WilliamT.; Schlesinger, WilliamH. Biogeochemistry, Vol. 10, Issue 1 https://doi.org/10.1007/bf00000893	journal	May 1990
Survival of diazotrophic cyanobacteria in soil Tomaselli, L.; Giovannetti, L. World Journal of Microbiology & Biotechnology, Vol. 9, Issue 1 https://doi.org/10.1007/bf00656530	journal	January 1993
Temporal Variation in Community Composition, Pigmentation, and Fv/Fm of Desert Cyanobacterial Soil Crusts Bowker, M. A.; Reed, S. C.; Belnap, J. Microbial Ecology, Vol. 43, Issue 1 https://doi.org/10.1007/s00248-001-1013-9	journal	February 2002
Nitrogen Fixation and Leaching of Biological Soil Crust Communities in Mesic Temperate Soils Veluci, Roberta M.; Neher, Deborah A.; Weicht, Thomas R. Microbial Ecology, Vol. 51, Issue 2 https://doi.org/10.1007/s00248-005-0121-3	journal	February 2006
Distribution of Extensive nifH Gene Diversity Across Physical Soil Microenvironments Izquierdo, Javier A.; Nüsslein, Klaus Microbial Ecology, Vol. 51, Issue 4 https://doi.org/10.1007/s00248-006-9044-x	journal	April 2006
Hypolithic Cyanobacteria Supported Mainly by Fog in the Coastal Range of the Atacama Desert Azúa-Bustos, Armando; González-Silva, Carlos; Mancilla, Rodrigo A. Microbial Ecology, Vol. 61, Issue 3 https://doi.org/10.1007/s00248-010-9784-5	journal	December 2010
Small-Scale Vertical Distribution of Algae and Structure of Lichen Soil Crusts Wu, Li; Lan, Shubin; Zhang, Delu Microbial Ecology, Vol. 62, Issue 3 https://doi.org/10.1007/s00248-011-9828-5	journal	March 2011
Nitrogen fixation in biological soil crusts from southeast Utah, USA Belnap, Jayne Biology and Fertility of Soils, Vol. 35, Issue 2 https://doi.org/10.1007/s00374-002-0452-x	journal	April 2002
Response of desert biological soil crusts to alterations in precipitation frequency Belnap, Jayne; Phillips, Susan L.; Miller, Mark E. Oecologia, Vol. 141, Issue 2 https://doi.org/10.1007/s00442-003-1438-6	journal	December 2003
Above- and belowground responses to nitrogen addition in a Chihuahuan Desert grassland Ladwig, Laura M.; Collins, Scott L.; Swann, Amaris L. Oecologia, Vol. 169, Issue 1 https://doi.org/10.1007/s00442-011-2173-z	journal	November 2011
Cyanobacteria and chloroflexi-dominated hypolithic colonization of quartz at the hyper-arid core of the Atacama Desert, Chile Lacap, Donnabella C.; Warren-Rhodes, Kimberley A.; McKay, Christopher P. Extremophiles, Vol. 15, Issue 1 https://doi.org/10.1007/s00792-010-0334-3	journal	November 2010
Warming and increased precipitation frequency on the Colorado Plateau: implications for biological soil crusts and soil processes Zelikova, Tamara J.; Housman, David C.; Grote, Ed E. Plant and Soil, Vol. 355, Issue 1-2 https://doi.org/10.1007/s11104-011-1097-z	journal	January 2012
Biogeography of diazotrophic bacteria in soils Roesch, Luiz Fernando Wurdig; Fulthorpe, Roberta R.; Jaccques, Rodrigo Josemar Seminoti World Journal of Microbiology and Biotechnology, Vol. 26, Issue 8 https://doi.org/10.1007/s11274-010-0326-6	journal	February 2010
Biological dinitrogen fixation by selected soil cyanobacteria as affected by strain origin, morphotype, and light conditions Hrčková, K.; Šimek, M.; Hrouzek, P. Folia Microbiologica, Vol. 55, Issue 5 https://doi.org/10.1007/s12223-010-0078-6	journal	September 2010
Acetylene reduction by cryptogamic crusts from a blackbrush community as related to resaturation and dehydration Jeffries, D. L.; Klopatek, J. M.; Link, S. O. Soil Biology and Biochemistry, Vol. 24, Issue 11 https://doi.org/10.1016/0038-0717(92)90059-7	journal	November 1992
Effects of desiccation duration on the community structure and nutrient retention of short and long-hydroperiod Everglades periphyton mats Gottlieb, Andrew; Richards, Jennifer; Gaiser, Evelyn Aquatic Botany, Vol. 82, Issue 2 https://doi.org/10.1016/j.aquabot.2005.02.012	journal	June 2005
Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan Desert Housman, D. C.; Powers, H. H.; Collins, A. D. Journal of Arid Environments, Vol. 66, Issue 4 https://doi.org/10.1016/j.jaridenv.2005.11.014	journal	September 2006
Nitrogen limitation in arid-subhumid ecosystems: A meta-analysis of fertilization studies Yahdjian, L.; Gherardi, L.; Sala, O. E. Journal of Arid Environments, Vol. 75, Issue 8 https://doi.org/10.1016/j.jaridenv.2011.03.003	journal	August 2011
Carotenoids and Mycosporine-like Amino Acid Compounds in Members of the Genus Microcoleus (Cyanobacteria): A Chemosystematic Study Karsten, Ulf; Garcia-Pichel, Ferran Systematic and Applied Microbiology, Vol. 19, Issue 3 https://doi.org/10.1016/s0723-2020(96)80054-3	journal	October 1996
Cyanobacteria track water in desert soils Garcia-Pichel, Ferran; Pringault, Olivier Nature, Vol. 413, Issue 6854 https://doi.org/10.1038/35096640	journal	September 2001
Evidence for the functional significance of diazotroph community structure in soil Hsu, Shi-Fang; Buckley, Daniel H. The ISME Journal, Vol. 3, Issue 1 https://doi.org/10.1038/ismej.2008.82	journal	September 2008
Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland Cruz-Martínez, Karelyn; Suttle, K. Blake; Brodie, Eoin L. The ISME Journal, Vol. 3, Issue 6 https://doi.org/10.1038/ismej.2009.16	journal	March 2009
Exposure of phototrophs to 548 days in low Earth orbit: microbial selection pressures in outer space and on early earth Cockell, Charles S.; Rettberg, Petra; Rabbow, Elke The ISME Journal, Vol. 5, Issue 10 https://doi.org/10.1038/ismej.2011.46	journal	May 2011
Changes to dryland rainfall result in rapid moss mortality and altered soil fertility Reed, Sasha C.; Coe, Kirsten K.; Sparks, Jed P. Nature Climate Change, Vol. 2, Issue 10 https://doi.org/10.1038/nclimate1596	journal	July 2012
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
Photosynthesis of the cyanobacterial soil-crust lichen Collema tenax from arid lands in southern Utah, USA: role of water content on light and temperature responses of CO2 exchange Lange, O. L.; Belnap, J.; Reichenberger, H. Functional Ecology, Vol. 12, Issue 2 https://doi.org/10.1046/j.1365-2435.1998.00192.x	journal	April 1998
Nitrogenase gene diversity and microbial community structure: a cross-system comparison Zehr, Jonathan P.; Jenkins, Bethany D.; Short, Steven M. Environmental Microbiology, Vol. 5, Issue 7 https://doi.org/10.1046/j.1462-2920.2003.00451.x	journal	July 2003
Future dryness in the southwest US and the hydrology of the early 21st century drought Cayan, D. R.; Das, T.; Pierce, D. W. Proceedings of the National Academy of Sciences, Vol. 107, Issue 50 https://doi.org/10.1073/pnas.0912391107	journal	December 2010
Damage Escape and Repair in Dried Chroococcidiopsis spp. from Hot and Cold Deserts Exposed to Simulated Space and Martian Conditions Billi, Daniela; Viaggiu, Emanuela; Cockell, Charles S. Astrobiology, Vol. 11, Issue 1 https://doi.org/10.1089/ast.2009.0430	journal	January 2011
Phenotypic variability and phylogenetic relationships of the genera Tolypothrix and Calothrix (Nostocales, Cyanobacteria) from running water Berrendero, E.; Perona, E.; Mateo, P. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 12 https://doi.org/10.1099/ijs.0.027581-0	journal	February 2011
Characterization and Biological Implications of Scytonemin, a Cyanobacterial Sheath Pigment1 Garcia-Pichel, Ferran; Castenholz, Richard W. Journal of Phycology, Vol. 27, Issue 3 https://doi.org/10.1111/j.0022-3646.1991.00395.x	journal	June 1991
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
Carbon exchange in biological soil crust communities under differential temperatures and soil water contents: implications for global change: GAS EXCHANGE IN BIOLOGICAL SOIL CRUSTS Grote, Edmund E.; Belnap, Jayne; Housman, David C. Global Change Biology, Vol. 16, Issue 10 https://doi.org/10.1111/j.1365-2486.2010.02201.x	journal	August 2010
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
Relevance of ammonium oxidation within biological soil crust communities Johnson, Shannon L.; Budinoff, Charles R.; Belnap, Jayne Environmental Microbiology, Vol. 7, Issue 1 https://doi.org/10.1111/j.1462-2920.2004.00649.x	journal	January 2005
Hypolithic community shifts occur as a result of liquid water availability along environmental gradients in China's hot and cold hyperarid deserts Pointing, Stephen B.; Warren-Rhodes, Kimberley A.; Lacap, Donnabella C. Environmental Microbiology, Vol. 9, Issue 2 https://doi.org/10.1111/j.1462-2920.2006.01153.x	journal	February 2007
A global census of nitrogenase diversity: nifH gene diversity Gaby, John Christian; Buckley, Daniel H. Environmental Microbiology, Vol. 13, Issue 7 https://doi.org/10.1111/j.1462-2920.2011.02488.x	journal	April 2011
CO ₂ fluxes of cryptogamic crusts Jeffries, D. L.; Link, S. O.; Klopatek, J. M. New Phytologist, Vol. 125, Issue 1 https://doi.org/10.1111/j.1469-8137.1993.tb03874.x	journal	September 1993
Three distinct clades of cultured heterocystous cyanobacteria constitute the dominant N2-fixing members of biological soil crusts of the Colorado Plateau, USA: N2-fixing cyanobacteria in soil crusts Yeager, Chris M.; Kornosky, Jennifer L.; Morgan, Rachael E. FEMS Microbiology Ecology, Vol. 60, Issue 1 https://doi.org/10.1111/j.1574-6941.2006.00265.x	journal	April 2007
Effect of primer mismatch, annealing temperature and PCR cycle number on 16S rRNA gene-targetting bacterial community analysis: PCR parameters influencing quantitative bias Sipos, Rita; SzÃ©kely, Anna J.; Palatinszky, MÃ¡rton FEMS Microbiology Ecology, Vol. 60, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00283.x	journal	May 2007
Spirirestis rafaelensis gen. et sp. nov. (Cyanophyceae), a new cyanobacterial genus from arid soils Flechtner, Valerie R.; Boyer, Sarah L.; Johansen, Jeffrey R. Nova Hedwigia, Vol. 74, Issue 1-2 https://doi.org/10.1127/0029-5035/2002/0074-0001	journal	February 2002
Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Suzuki, M. T.; Giovannoni, S. J. Applied and environmental microbiology, Vol. 62, Issue 2 https://doi.org/10.1128/aem.62.2.625-630.1996	journal	January 1996
Expression of nifH Genes in Natural Microbial Assemblages in Lake George, New York, Detected by Reverse Transcriptase PCR Zani, Sabino; Mellon, Mark T.; Collier, Jackie L. Applied and Environmental Microbiology, Vol. 66, Issue 7 https://doi.org/10.1128/aem.66.7.3119-3124.2000	journal	July 2000
Diazotrophic Community Structure and Function in Two Successional Stages of Biological Soil Crusts from the Colorado Plateau and Chihuahuan Desert Yeager, C. M.; Kornosky, J. L.; Housman, D. C. Applied and Environmental Microbiology, Vol. 70, Issue 2 https://doi.org/10.1128/aem.70.2.973-983.2004	journal	February 2004
Remarkable N2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. Ueda, T.; Suga, Y.; Yahiro, N. Journal of Bacteriology, Vol. 177, Issue 5 https://doi.org/10.1128/jb.177.5.1414-1417.1995	journal	March 1995
Effects of nitrogen deposition and empirical nitrogen critical loads for ecoregions of the United States Pardo, Linda H.; Fenn, Mark E.; Goodale, Christine L. Ecological Applications, Vol. 21, Issue 8 https://doi.org/10.1890/10-2341.1	journal	December 2011
Photosynthesis and Water Relations of Lichen Soil Crusts: Field Measurements in the Coastal Fog Zone of the Namib Desert Lange, O. L.; Meyer, A.; Zellner, H. Functional Ecology, Vol. 8, Issue 2 https://doi.org/10.2307/2389909	journal	April 1994
Erratum to: Central European Journal of Biology, Volume 6, Issue 5 Péli, Evelin; Lei, Nie; Pócs, Tamás Open Life Sciences, Vol. 6, Issue 6 https://doi.org/10.2478/s11535-011-0075-z	journal	November 2011
Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria Lücking, Robert; Lawrey, James D.; Sikaroodi, Masoumeh American Journal of Botany, Vol. 96, Issue 8 https://doi.org/10.3732/ajb.0800258	journal	August 2009
Effects of nitrogen deposition and empirical nitrogen critical loads for ecoregions of the United States Pardo, Linda H.; Fenn, Mark E.; Goodale, Christine L. Figshare https://doi.org/10.6084/m9.figshare.c.3295196.v1	collection	January 2016

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