Abstract
Background and aims
Nitrogen (N) deposition and climate change are a threat to the structure and function of drylands, where biocrust-dominated communities are prevalent. We aimed at evaluating the influence of N deposition, climate and edaphic properties of semiarid areas of Spain on soil microbial communities and N cycling.
Methods
We quantified soil bacteria, fungi, ammonium oxidizing bacteria and archaea, estimated the abundance of autotrophic organisms (soil pigment content) and measured a wide array of variables related to the N cycle.
Results
Local climatic conditions and soil fertility were main drivers of soil microbial communities and N cycling. In particular, cyanobacteria were favored in colder sites with lower soil fertility. Higher precipitation at high-fertility sites favored green algae. Soil N availability was negatively related to MAT. Increased N deposition (4.3–7.3 kg N ha−1 yr.−1) reduced the abundance of soil bacteria and fungi, a response partially attributed to N-driven soil acidification, whereas it favored green-algae and increased available N in soil, contributing to a net ecosystem eutrophication.
Conclusions
Changes in soil microbial community structure and nutrient cycling in response to N deposition and climate change will affect the overall functioning of semiarid Mediterranean ecosystems, which may have important implications in terms of long-term soil C sequestration.
Similar content being viewed by others
References
Allen EB, Temple PJ, Bytnerowicz A, Arbaugh MJ, Sirulnik AG, Rao LE (2007) Patterns of understory biodiversity in mixed coniferous forests of southern California impacted by air pollution. Sci World J 7:247–263
Aranibar JN, Otter L, Macko SA, Feral CJW, Epstein HE, Dowty PR, Eckhardt F, Shutgart HH, Swap RJ (2003) Nitrogen cycling in the soil-plant system along a precipitation gradient in the Kalahari sands. Glob Chang Biol 10:359–373
Austin AT, Sala OE (2002) Carbon and nitrogen dynamics across a natural precipitation gradient in Patagonia, Argentina. J Veg Sci 13:351–360
Belnap J (2002) Nitrogen fixation in biological soil crust from southeast Utah, USA. Biol Fert Soils 35:128–135
Belnap J, Phillips SL, Flint S, Money J, Caldwell M (2008) Global change and biological soil crusts: effects of ultraviolet augmentation under altered precipitation regimes and nitrogen additions. Glob Chang Biol 14:670–686
Berkeley A, Thomas AD, Dougill AJ (2005) Cyanobacterial soil crusts and woody shrub canopies in Kalahari rangelands. Afr J Ecol 43:137–145
Biudes MS, Vourlitis GL (2012) Carbon and nitrogen mineralization of a semiarid shrubland exposed to experimental nitrogen deposition. Soil Sci Soc Am J 76:2068–2073
Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-W, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59
Bonanomi G, Caporaso S, Allegrezza M (2006) Short-term effects of nitrogen enrichment litter removal and cutting on a Mediterranean grassland. Acta Oecol 30:419–425
Bowker MA, Reed SC, Belnap J, Phillips SL (2002) Temporal variation in community composition, pigmentation, and Fv/Fm of desert cyanobacterial soil crusts. Microb Ecol 43:13–25
Bowker MA, Mau RL, Maestre FT, Escolar C, Castillo-Monroy AP (2011) Functional profiles reveal unique ecological roles of various biological soil crust organisms. Funct Ecol 25:787–795
Bowker MA, Maestre FT, Eldridge D, Belnap J, Castillo-Monroy A, Escolar C, Soliveres S (2014) Biological soil crusts (biocrusts) as a model system in community, landscape and ecosystem ecology. Biodivers Conserv 23:1619–1637
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretical approach. Springer, New York
Castillo-Monroy AP, Maestre FT, Delgado-Baquerizo M, Gallardo A (2010) Biological soil crusts modulate nitrogen availability in semiarid ecosystems: insights from a Mediterranean grassland. Plant Soil 333:21–34
Chantigny MH, Angers DA, Kaiser K, Kalbitz K (2006) Extraction and characterization of dissolved organic matter. In: Carter MR, Gregorich EG (Eds.), Soil sampling and methods of analysis, second edition, Canadian Society of Soil Science, pp 617–635
Cox RD, Allen EB (2008) Composition of soil seed banks in southern California coastal sage scrub and adjacent exotic grassland. Plant Ecol 198:37–46
Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92:621–632
DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2005) Atmospheric nitrate deposition and enhanced dissolved organic carbon leaching: test of a potential mechanism. Soil Sci Soc Am J 69:1233–1237
Delgado-Baquerizo M, Covelo F, Gallardo A (2011) Dissolved organic nitrogen in Mediterranean ecosystems. Pedosphere 21:302–308
Delgado-Baquerizo M, Maestre FT, Gallardo A (2013) Biological soil crusts increase the resistance of soil nitrogen dynamics to changes in temperatures in a semi-arid ecosystem. Plant Soil 366:35–47
Delgado-Baquerizo M, Maestre FT, Escolar C, Gallardo A, Ochoa V, Gozalo B, Prado-Comesaña A (2014) Direct and indirect impacts of climate change on microbial and biocrust communities alter the resistance of the N cycle in a semiarid grassland. J Ecol 102:1592–1605
DeLuca TH, Zackrisson O, Gentili F, Sellstedt A, Nilsson M-C (2007) Ecosystem control son nitrogen fixation in boreal feather moss communities. Oecologia 152:121–130
Demoling F, Nilsson LO, Bååth E (2008) Bacterial and fungal response to nitrogen fertilization in three coniferous forest soils. Soil Biol Biochem 40:370–379
Dominati E, Patterson M, Mackay A (2010) A framework for classifying and quantifying the natural capital and ecosystem services of soils. Ecol Econ 69:1858–1868
Dougill AJ, Thomas AD (2004) Kalahari sand soils: spatial heterogeneity, biological soil crusts and land degradation. Land Degrad Dev 15:233–242
Eisenlord SD, Zak DR (2010) Simulated atmospheric nitrogen deposition alters actinobacterial community composition in forest soils. Soil Sci Soc Am J 74:1157–1166
Evans SE, Wallenstein MD (2011) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101–116
Fang Y, Zhu W, Gundersen P, Mo J, Zhou G, Yoh M (2009) Large loss of dissolved organic nitrogen from nitrogen-saturated forests in subtropical China. Ecosystems 12:33–45
Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102:14683–14688
Gao XJ, Giorgi F (2008) Increased aridity in the Mediterranean region under greenhouse gas forcing estimated from high resolution simulations with a regional climate model. Glob Planet Chang 62:195–209
García-Gómez H, Garrido JL, Vivanco MG, Lassaletta L, Rabago I, Avila A, Tsyro T, Sanchez G, Gonzales-Ortiz A, Gonzalez-Fernandez I, Alonso R (2014) Nitrogen deposition in Spain: modeled patterns and threatened habitats within the Natura 2000 network. Sci Total Environ 485:450–460
Gaudnik C, Corcket E, Clément B, Delmas CEL, Gombert-Courvoisier S, Muller S, Stevens CJ, Alard D (2011) Detecting the footprint of changing atmospheric nitrogen deposition loads on acid grasslands in the context of climate change. Glob Chang Biol 17:3351–3365
Griffiths RP, Madtritch MD, Swanson AK (2009) The effects of topography on forest soil characteristics in the Oregon Cascade Mountains USA: implications for the effects of climate change on soil properties. For Ecol Manag 257:1–7
Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296
Hawkes CV (2003) Nitrogen cycling mediated by biological soil crusts and arbuscular mycorrhizal fungi. Ecology 84:1553–1562
Hessen DO, Andersen T, Larsen S, Skjelkvåle BL, de Wit HA (2009) Nitrogen deposition, catchment productivity, and climate as determinants of lake stoichiometry. Limnol Oceanogr 54:2520–2528
Horswill P, O’Sullivan O, Phoenix GK, Lee JA, Leake JR (2008) Base cation depletion, eutrophication and acidification of species-rich grasslands in response to long-term simulated nitrogen deposition. Environ Pollut 155:336–349
Hueso S, García C, Hernández T (2012) Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils. Soil Biol Biochem 50:167–173
Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen DON and dissolved organic carbon DOC in soil. Soil Biol Biochem 38:991–999
Li XR, Zhang P, Su YG, Jia RL (2012) Carbon fixation by biological soil crusts following revegetation of sand dunes in arid desert regions of China: a four year field study. Catena 97:119–126
Limpens J, Granath G, Gunnarsson U, Aerts R, Bayley S, Bragazza L, Bubier J, Buttler A, van den Berg LJL, Francez A-J, Grosvernier P, Heijmans MMPD, Hoosbeek MR, Hotes S, Ilomets M, Leith I, Mitchell EAD, Moore T, Nilsson MB, Nordbakken J-F, Rocheford L, Rydin H, Sheppard LJ, Thormann M, Wiedermann MM, Williams BL, Xu B (2011) Climatic modifiers of the response to nitrogen deposition in peat-forming sphagnum mosses: a meta-analysis. New Phytol 191:496–507
Maaroufi NI, Nordin A, Hasselquist NJ, Bach LH, Palmqvist K, Gundale M (2015) Anthropogenic nitrogen deposition enhances carbon sequestration in boreal soils. Glob Chang Biol 21:3169–3180
Maestre FT, Bowker MA, Cantón Y, Castillo-Monroy AP, Cortina J, Escolar C, Escudero A, Lázaro R, Martínez I (2011) Ecology and functional roles of biological soil crusts in semi-arid ecosystems of Spain. J Arid Environ 75:1282–1291
Maestre FT, Salguero-Gómez R, Quero JL (2012) It is getting hotter in here: determining and projecting the impacts of global environmental change on drylands. Philos Trans R Soc B 367:3062–3075
Martínez-Ferri E, Balaguer L, Valladares F, Chico JM, Manrique E (2000) Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiol 20:131–138
McCulley RL, Burke IC, Laurenroth WK (2009) Conservation of nitrogen increases with precipitation across a major grassland in the Central Great Plains of North America. Oecologia 159:571–581
Miranda JD, Armas C, Padilla FM, Pugnaire FI (2011) Climatic change and rainfall patterns: effects on semi-arid plant communities of the Iberian southeast. J Arid Environ 75:1302–1309
Nordin A, Hogberg P, Nasholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–132
Ochoa-Hueso R, Manrique E (2010) Nitrogen fertilization and water supply affect germination and plant establishment of the soil seed bank present in a semi-arid Mediterranean scrubland. Plant Ecol 210:263–273
Ochoa-Hueso R, Allen EB, Branquinho C, Cruz C, Dias T, Fenn ME, Manrique E, Pérez-Corona ME, Sheppard LJ, Stock WD (2011a) Nitrogen deposition effects on Mediterranean-type ecosystems: an ecological assessment. Environ Pollut 159:2265–2279
Ochoa-Hueso R, Hernandez RR, Pueyo JJ, Manrique E (2011b) Spatial distribution of biological soil crusts from semi-arid central Spain are related to soil chemistry and shrub cover. Soil Biol Biochem 43:1894–1901
Ochoa-Hueso R, Maestre FT, de los Ríos A, Valea S, Theobald MR, Vivanco MG, Manrique E, Bowker MA (2013a) Nitrogen deposition alters nitrogen cycling and reduces soil carbon content in low-productivity semiarid Mediterranean ecosystems. Environ Pollut 179:185–193
Ochoa-Hueso R, Pérez-Corona ME, Manrique E (2013b) Impacts of simulated N deposition on plants and mycorrhizae from Spanish semiarid Mediterranean shrublands. Ecosystems 16:838–851
Ochoa-Hueso R, Stevens CJ, Ortiz-Llorente MJ, Manrique E (2013c) Soil chemistry and fertility alterations in response to N application in a semiarid Mediterranean shrubland. Sci Total Environ 452-453:78–86
Ochoa-Hueso R, Arróniz-Crespo M, Bowker MA, Maestre FT, Pérez-Corona ME, Theobald MR, Vivanco MG, Manrique E (2014) Biogeochemical indicators of elevated nitrogen deposition in semiarid Mediterranean ecosystems. Environ Monit Assess 186:5831–5842
Phoenix GK, Hicks WK, Cinderby S, Kuylenstierna JCI, Stock WD, Dentener FJ, Giller KE, Austin AT, Lefroy RDB, Gimeno BS, Ashmore MS, Ineson P (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Chang Biol 12:470–476
Phoenix GK, Emmett BA, Britton AJ, Caporn SJM, Dise NB, Helliwell R, Jones L, Leake JR, Leith ID, Sheppard LJ, Sowerby A, Pilkington MG, Rowe EC, Ashmore MR, Power SA (2012) Impacts of atmospheric nitrogen deposition: responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments. Glob Chang Biol 18:1197–1215
Poikolainen J, Lippo H, Hongisto M, Kubin E, Mikkola K, Lindgren M (1998) On the abundance of epiphytic green algae in relation to the nitrogen concentrations of biomonitors and nitrogen deposition in Finland. Environ Pollut 102:85–92
Pregitzer KS, Zak DR, Burton AJ, Ashby JA, MacDonald NW (2004) Chronic nitrate additions dramatically increase the export of carbon and nitrogen from northern hardwood ecosystems. Biogeochemistry 68:179–197
Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927
Rao LE, Steers RJ, Allen EB (2011) Effects of natural and anthropogenic gradients on native and exotic winter annuals in a southern California desert. Plant Ecol 212:1079–1089
Reed SC, Coe KK, Sparks JP, Housman DC, Zelikova TJ, Belnap J (2012) Changes to dryland rainfall result in rapid moss mortality and altered soil fertility. Nat Clim Chang 2:752–755
Robertson GP, Groffman PM (2007) Nitrogen transformations. In: Soil microbiology, ecology, and biochemistry, pp. 341–364
Rodà F, Ávila A, Rodrigo A (2002) Nitrogen deposition in Mediterranean forests. Environ Pollut 118:205–213
Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712
Sala OE, Chapin III FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774
Schimel JP, Bennett J (2004) Nitrogen mineralization, challenges of a changing paradigm. Ecology 85:591–602
Sinsabaugh RL, Belnap J, Rudgers J, Kuske CR, Martinez N, Sandquist D (2015) Soil microbial responses to nitrogen addition in arid ecosystems. Front Microbiol 6:819
Stevens CJ, Dise NB, Gowing D (2009) Regional trends in soil acidification and exchangeable metal concentrations in relation to acid deposition rates. Environ Pollut 157:313–319
Stevens CJ, Manning P, van den Berg LJL, de Graaf MCC, Wamelink GWW, Boxman AW, Bleeker A, Vergeer P, Arroniz-Crespo M, Limpens J, Lamers LPM, Bobbink R, Dorland E (2011) Ecosystem responses to reduced and oxidized nitrogen inputs in European terrestrial habitats. Environ Pollut 159:665–676
Tian XF, Hu HW, Ding Q, Song MH, Xu XL, Zheng Y, Guo LD (2014) Influence of nitrogen fertilization on soil ammonia oxidizer and denitrifier abundance, microbial biomass, and enzyme activities in an alpine meadow. Biol Fertil Soils 50:703–713
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120
Val J, Monge E, Baker NR (1994) An improved HPLC method for rapid analysis of the xanthophylls cycle pigments. J Chromatogr Sci 32:286–289
van Diepen LTA, Lilleskov ER, Pregitzer KS, Miller RM (2010) Simulated nitrogen deposition causes a decline of intra- and extraradical abundance of arbuscular mycorrhizal fungi and changes in microbial community structure in northern hardwood forests. Ecosystems 13:683–695
van Diepen LTA, Lilleskov ER, Pregitzer KS (2011) Simulated nitrogen deposition affects community structure of arbuscular mycorrhizal fungi in northern hardwood forests. Mol Ecol 20:799–811
Vivanco MG, Palomino I, Vautard R, Bessagnet B, Martín F, Menut L, Jiménez S (2009) Multi-year assessment of photochemical air quality simulation Spain. Environ Model Softw 24:63–73
Waldrop MP, Zak DR (2006) Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems 9:921–933
Warren CR (2009) Does nitrogen concentration affect relative uptake rates of nitrate, ammonium, and glycine? J Plant Nutr Soil Sci 172:224–229
Wei C, Yu Q, Bai E, Lü X, Li Q, Xia J, Kardol P, Liang W, Wang Z, Han X (2013) Nitrogen deposition weakens plant–microbe interactions in grassland ecosystems. Glob Chang Biol 19:3688–3697
Yeomans J, Bremmer JM (1989) A rapid and precise method for routine determination of organic carbon in soil. Commun Soil Sci Plant Anal 19:1467–1476
Yun S-I, Ro H-M, Choi W-J, Han G-H (2011) Interpreting the temperature-induced response of ammonia oxidizing microorganisms in soil using nitrogen isotope fractionation. J Soils Sediments 11:1253–1261
Zak DR, Pregitzer KS, Burton AJ, Edwards IP, Kellner H (2011) Microbial responses to a changing environment: implications for the future functioning of terrestrial ecosystems. Fungal Ecol 4:386–395
Zechmeister-Boltenstern S, Michel K, Pfeffer M (2011) Soil microbial community structure in European forests in relation to forest type and atmospheric nitrogen deposition. Plant Soil 343:37–50
Zelikova TJ, Housman DC, Grote EE, Neher DA, Belnap J (2012) Warming and increased precipitation on the Colorado Plateau: implications for biological soil crusts and soil processes. Plant Soil 355:265–282
Zhang X, Liu W, Bai Y, Zhang G, Han X (2011) Nitrogen deposition mediates the effects and importance of chance in changing biodiversity. Mol Ecol 20:429–438
Zornoza R, Mataix-Solera J, Guerrero C, Arcenegui V, Mataix-Beneyto J (2009) Storage effects on biochemical properties of air-dried soil samples from southeastern Spain. Arid Land Res Manag 23:213–222
Acknowledgments
This research was supported by the Spanish Ministerio de Economía y Competitividad (CGL-2009-11015; CTM2009-12838-CO4-O3), the Comunidad de Madrid (S-0505/AMB/0335), and the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant agreement no. 242658 (BIOCOM project). FTM, MDB and ROH were supported by the BIOCOM project.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Kees Jan van Groenigen.
Rights and permissions
About this article
Cite this article
Ochoa-Hueso, R., Delgado-Baquerizo, M., Gallardo, A. et al. Climatic conditions, soil fertility and atmospheric nitrogen deposition largely determine the structure and functioning of microbial communities in biocrust-dominated Mediterranean drylands. Plant Soil 399, 271–282 (2016). https://doi.org/10.1007/s11104-015-2695-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-015-2695-y