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Divergence in physiological responses between cyanobacterial and lichen crusts to a gradient of simulated nitrogen deposition

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Abstract

Background and aims

Nitrogen (N) deposition in arid lands is known to be increasing. However, N deposition gradients have unclear effects on physiological characteristics of biocrusts. This study tested if physiological characteristics are stimulated by low levels of N deposition and reduced by high levels of N deposition.

Methods

We simulated N deposition at various rates to plots of cyanobacterial and lichen biocrusts in the Gurbantunggut Desert and measured indicators of growth and stress.

Results

In cyanobacterial crusts, most evidence suggests that biomass and growth are unaffected by lower levels of N but suppressed at the highest level. Biomass and growth of lichen crusts were less sensitive to N addition but, in the case of actual photochemical efficiency, were also suppressed at the highest N addition rate. Most osmotic adjustment substances of cyanobacterial and lichen crusts did not show significant responses after N addition. In the two crusts, minor increase in antioxidative enzyme activity was found in some N addition rates but no similar trends between the crust types were observed.

Conclusions

Physiological performance of cyanobacterial crusts was more sensitive to high levels of N addition than that of lichen crusts. Increasing N deposition might greatly affect cyanobacterial crusts before lichen crusts.

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References

  • Abed RMM, Al Kharusi S, Schramm A, Robinson MD (2010) Bacterial diversity, pigments and nitrogen fixation of biological desert crusts from the Sultanate of Oman. FEMS Microbiol Ecol 72:418–428. doi:10.1111/j.1574-6941.2010.00854.x

    Article  CAS  PubMed  Google Scholar 

  • Alon A, Steinberger Y (1999) Effect of nitrogen amendments on microbial biomass, above-ground biomass and nematode population in the Negev Desert soil. J Arid Environ 41:429–441

    Article  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. doi:10.1146/annurev.arplant.59.032607.092759

    Article  CAS  PubMed  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bauer GA, Bazzaz FA, Minocha R, Long S, Magill A, Aber J, Berntson GM (2004) Effects of chronic N additions on tissue chemistry, photosynthetic capacity, and carbon sequestration potential of a red pine (Pinus resinosa Ait.) stand in the NE United States. For Ecol Manag 196:173–186. doi:10.1016/j.foreco.2004.03.032

    Article  Google Scholar 

  • Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fert Soils 35:128–135. doi:10.1007/s00374-002-0452-x

    Article  CAS  Google Scholar 

  • Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178. doi:10.1002/Hyp.6325

    Article  CAS  Google Scholar 

  • Belnap J, Phillips SL, Miller ME (2004) Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia 141:306–316. doi:10.1007/s00442-003-1438-6

    Article  PubMed  Google Scholar 

  • Belnap J, Phillips SL, Troxler T (2006) Soil lichen and moss cover and species richness can be highly dynamic: the effects of invasion by the annual exotic grass Bromus tectorum, precipitation, and temperature on biological soil crusts in SE Utah. Appl Soil Ecol 32:63–76. doi:10.1016/j.apsoil.2004.12.010

    Article  Google Scholar 

  • 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. Global Change Biol 14:670–686. doi:10.1111/j.1365-2486.2007.01509.x

    Article  Google Scholar 

  • Bignal KL, Ashmore MR, Headley AD (2008) Effects of air pollution from road transport on growth and physiology of six transplanted bryophyte species. Environ Pollut 156:332–340. doi:10.1016/j.envpol.2008.02.011

    Article  CAS  PubMed  Google Scholar 

  • Chen LZ, Li DH, Song LR, Hu CX, Wang GH, Liu YD (2006) Effects of salt stress on carbohydrate metabolism in desert soil alga Microcoleus vaginatus Gom. J Integr Plant Biol 48:914–919. doi:10.1111/j.1744-7909.2006.00291.x

    Article  CAS  Google Scholar 

  • Chen YN, Wang Q, Li WH, Ruan X (2007) Microbiotic crusts and their interrelations with environmental factors in the Gurbantonggut desert, western China. Environ Geol 52:691–700

    Article  Google Scholar 

  • Choudhury S, Panda SK (2005) Toxic effects, oxidative stress and ultrastructural changes in moss Taxithelium nepalense (Schwaegr.) Broth. under chromium and lead phytotoxicity. Water Air Soil Pollut 167:73–90

    Article  CAS  Google Scholar 

  • Curatti L, Giarrocco LE, Cumino AC, Salerno GL (2008) Sucrose synthase is involved in the conversion of sucrose to polysaccharides in filamentous nitrogen-fixing cyanobacteria. Planta 228:617–625. doi:10.1007/s00425-008-0764-7

    Article  CAS  PubMed  Google Scholar 

  • Deslippe JR, Egger KN, Henry GHR (2005) Impacts of warming and fertilization on nitrogen-fixing microbial communities in the Canadian High Arctic. FEMS Microbiol Ecol 53:41–50. doi:10.1016/j.femsec.2004.12.002

    Article  CAS  PubMed  Google Scholar 

  • Enrique AG, Bruno C, Christopher A, Virgile C, Steven C (2008) Effects of nitrogen availability on microbial activities, densities and functional diversities involved in the degradation of a Mediterranean evergreen oak litter (Quercus ilex L.). Soil Biol Biochem 40(7):1654–1661. doi:10.1016/j.soilbio.2008.01.020

    Article  CAS  Google Scholar 

  • Evans RD, Johansen J (1999) Microbiotic crusts and ecosystem processes. Crit Rev Plant Sci 18:183–225. doi:10.1016/s0735-2689(99)00384-6

    Article  Google Scholar 

  • Fenn ME, Haeuber R, Tonnesen GS, Baron JS, Grossman-Clarke S, Hope D, Jaffe DA, Copeland S, Geiser L, Rueth HM, Sickman JO (2003) Nitrogen emissions, deposition, and monitoring in the western United States. Bioscience 53:391–403

    Article  Google Scholar 

  • Funk FA, Loydi A, Peter G (2014) Effects of biological soil crusts and drought on emergence and survival of a Patagonian perennial grass in the Monte of Argentina. J Arid Land 6:735–741

    Article  Google Scholar 

  • Garcia-Pichel F, Belnap J, Neuer S, Schanz F (2003) Estimates of global cyanobacterial biomass and its distribution. Algol Stud 109:213–227. doi:10.1127/1864-1318/ 2003/0109-0213

    Article  Google Scholar 

  • Ge HM, Zhou XP, Xia L, Zhang DL, Hu CX (2014) Effects of light and nitrogen source on the secretion of extracellular polysaccharides from Nostoc sp. Acta Hydrobiol Sinica 38:480–486 (In Chinese with English abstract)

    CAS  Google Scholar 

  • Gonzalez CM, Pignata ML (1994) The influence of air pollution on soluble proteins, chlorophyll degradation, MDA, sulphur and heavy metals in a transplanted lichen. Chem Ecol 9:105–113

    Article  CAS  Google Scholar 

  • Gusewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164(2):243–266. doi:10.1111/j.1469-8137.2004.01192.x

    Article  Google Scholar 

  • Hallbom L, Bergman B (1979) Influence of certain herbicides and a forest fertilizer on the nitrogen-fixation by the lichen Peltigera praetextata. Oecologia 40(1):19–27. doi:10.1007/bf00388807

    Article  Google Scholar 

  • Hashempour A, Ghasemnezhad M, Ghazvini RF, Sohani MM (2014) Olive (Olea europaea L.) freezing tolerance related to antioxidant enzymes activity during cold acclimation and non acclimation. Acta Physiol Plant 36:3231–3241. doi:10.1007/s11738-014-1689-3

    Article  CAS  Google Scholar 

  • Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:605–618. doi:10.1111/j.1365-3040.1995.tb00562.x

    Article  CAS  Google Scholar 

  • Hogan EJ, Minnullina G, Sheppard LJ, Leith ID, Crittenden PD (2010) Response of phosphomonoesterase activity in the lichen Cladonia portentosa to nitrogen and phosphorus enrichment in a field manipulation experiment. New Phytol 186:926–933. doi:10.1111/j.1469-8137.2010.03221.x

    Article  CAS  PubMed  Google Scholar 

  • Hu CX, Liu YD, Song LR, Zhang DK (2002) Effect of desert soil algae on the stabilization of fine sands. J Appl Phycol 14:281–292. doi:10.1023/A:1021128530086

    Article  CAS  Google Scholar 

  • Huang ZA, Jiang DA, Yang Y, Sun JW, Jin SH (2004) Effects of nitrogen deficiency on gas exchange, chlorophyll fluorescence, and antioxidant enzymes in leaves of rice plants. Photosynthetica 42:357–364. doi:10.1023/B:PHOT.0000046153.08935.4c

    Article  CAS  Google Scholar 

  • Hui R, X-r L, R-l J, Zhao X, Y-m L, C-y C (2012) Effects of enhanced UV-B radiation on physiological characteristics of Bryum argenteum. Shengtaixue Zazhi 31:38–43 (In Chinese with English Abstract)

    CAS  Google Scholar 

  • Hui R, Li XR, Jia RL, Liu LC, Zhao RM, Zhao X, Wei YP (2014) Photosynthesis of two moss crusts from the Tengger Desert with contrasting sensitivity to supplementary UV-B radiation. Photosynthetica 52:36–49. doi:10.1007/s11099-014-0003-3

    Article  CAS  Google Scholar 

  • Johansson O, Olofsson J, Giesler R, Palmqvist K (2011) Lichen responses to nitrogen and phosphorus additions can be explained by the different symbiont responses. New Phytol 191:795–805. doi:10.1111/j.1469-8137.2011.03739.x

    Article  CAS  PubMed  Google Scholar 

  • Kidron GJ, Barinova S, Vonshak A (2012) The effects of heavy winter rains and rare summer rains on biological soil crusts in the Negev Desert. Catena 95:6–11

    Article  Google Scholar 

  • Krupa SV (2003) Effects of atmospheric ammonia (NH3) on terrestrial vegetation: a review. Environ Pollut 124:179–221. doi:10.1016/s0269-7491(02)00434-7

    Article  CAS  PubMed  Google Scholar 

  • Lan SB, Wu L, Zhang DL, Hu CX (2012) Successional stages of biological soil crusts and their microstructure variability in Shapotou region (China). Environ Earth Sci 65(1):77–88

    Article  Google Scholar 

  • Lange L, Nobel P, Osmond C, Ziegler H (1981) Responses to the physical environment. In: Physiological plant ecology I, vol 12A. Springer-Verlag, pp 67, 259

  • Lassouane N, Aïd F, Lutts S (2013) Water stress impact on young seedling growth of Acacia arabica. Acta Physiol Plant 35:2157–2169

    Article  CAS  Google Scholar 

  • Li KH, Liu XJ, Song W, Chang YH, Hu YK, Tian CY (2014) Atmospheric nitrogen deposition at two sites in an arid environment of Central Asia. Plos One 9. doi:10.1371/journal.pone.0067018

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Liu LC, Li SZ, Duan ZH, Wang T, Zhang ZS, Li XR (2006) Effects of microbiotic crusts on dew deposition in the restored vegetation area at Shapotou, northwest China. J Hydrol 328:331–337. doi:10.1016/j.jhydrol.2005.12.004

    Article  Google Scholar 

  • Liu H, Han X, Li L, Huang J, Liu H, Li X (2009) Grazing density effects on cover, species composition, and nitrogen fixation of biological soil crust in an inner Mongolia steppe. Rangel Ecol Manag 62:321–327

    Article  Google Scholar 

  • Malapascua JRF, Jerez CG, Sergejevova M, Figueroa FL, Masojidek J (2014) Photosynthesis monitoring to optimize growth of microalgal mass cultures: application of chlorophyll fluorescence techniques. Aquat Biol 22:123–140. doi:10.3354/ab00597

    Article  Google Scholar 

  • Medici LO, Azevedo RA, Smith RJ, Lea PJ (2004) The influence of nitrogen supply on antioxidant enzymes in plant roots. Funct Plant Biol 31:1–9. doi:10.1071/fp03130

    Article  CAS  Google Scholar 

  • Mendoza-Aguilar DO, Cortina J, Pando-Moreno M (2014) Biological soil crust influence on germination and rooting of two key species in a Stipa tenacissima steppe. Plant Soil 375:267–274. doi:10.1007/s11104-013-1958-8

    Article  CAS  Google Scholar 

  • Monreal J, Jiménez E, Remesal E, Morillo-Velarde R, García-Mauriño S, Echevarría C (2007) Proline content of sugar beet storage roots: response to water deficit and nitrogen fertilization at field conditions. Environ Exp Bot 60:257–267

    Article  CAS  Google Scholar 

  • Ochoa-Hueso R, Manrique E (2011) Effects of nitrogen deposition and soil fertility on cover and physiology of Cladonia foliacea (Huds.) Willd., a lichen of biological soil crusts from Mediterranean Spain. Environ Pollut 159:449–457. doi:10.1016/j.envpol.2010.10.021

    Article  CAS  PubMed  Google Scholar 

  • Ochoa-Hueso R, Mejias-Sanz V, Perez-Corona ME, Manrique E (2013) Nitrogen deposition effects on tissue chemistry and phosphatase activity in Cladonia foliacea (Huds.) Willd., a common terricolous lichen of semi-arid Mediterranean shrublands. J Arid Environ 88:78–81. doi:10.1016/j.jaridenv.2012.07.007

    Article  Google Scholar 

  • Ochoa-Hueso R, Arroniz-Crespo M, Bowker MA, Maestre FT, Esther Perez-Corona M, Theobald MR, Vivanco MG, Manrique E (2014) Biogeochemical indicators of elevated nitrogen deposition in semiarid Mediterranean ecosystems. Environ Monit Assess 186(9):5831–5842. doi:10.1007/s10661-014-3822-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pendleton RL, Pendleton BK, Howard GL, Warren SD (2003) Growth and nutrient content of herbaceous seedlings associated with biological soil crusts. Arid Land Res Manag 17:271–281. doi:10.1080/15324980301598

    Article  Google Scholar 

  • Potvin C, Lechowicz MJ, Tardif S (1990) The statistical analysis of ecophysiological response curves obtained from experiments involving repeated measures. Ecology 71:1389–1400. doi:10.2307/1938276

    Article  Google Scholar 

  • 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 Change 2:752–755, http://www.nature.com/nclimate/journal/v2/n10/abs/nclimate1596.html#supplementary-information

    Article  CAS  Google Scholar 

  • Rubio-Wilhelmi MM et al (2011) Effect of cytokinins on oxidative stress in tobacco plants under nitrogen deficiency. Environ Exp Bot 72:167–173. doi:10.1016/j.envexpbot.2011.03.005

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012

  • Singh DV, Tripathi AK, Kumar HD (1987) Is tryptophan a repressor of heterocyst differentiation and nitrogenase activity in the cyanobacterium Anabaena doliolum. Ann Sci Nat Bot Biol Veg 8(1):29–33

    Google Scholar 

  • Stursova M, Crenshaw CL, Sinsabaugh RL (2006) Microbial responses to long-term N deposition in a semiarid grassland. Microbial Ecol 51:90–98

    Article  Google Scholar 

  • Su YG, Zhao X, Li AX, Li XR, Huang G (2011) Nitrogen fixation in biological soil crusts from the Tengger desert, northern China. Eur J Soil Biol 47:182–187

    Article  CAS  Google Scholar 

  • Sun SQ, He M, Cao T, Zhang YC, Han W (2009) Response mechanisms of antioxidants in bryophyte (Hypnum plumaeforme) under the stress of single or combined Pb and/or Ni. Environ Monit Assess 149:291–302

    Article  CAS  PubMed  Google Scholar 

  • Thiet RK, Doshas A, Smith SM (2014) Effects of biocrusts and lichen-moss mats on plant productivity in a US sand dune ecosystem. Plant Soil 377:235–244. doi:10.1007/s11104-013-2002-8

    Article  CAS  Google Scholar 

  • Throop HL (2005) Nitrogen deposition and herbivory affect biomass production and allocation in an annual plant. Oikos 111:91–100

    Article  Google Scholar 

  • Wang XQ, Jiang J, Wang YC, Luo WL, Song CW, Chen JJ (2006) Responses of ephemeral plant germination and growth to water and heat conditions in the southern part of Gurbantunggut Desert. Chin Sci Bull 51:110–116. doi:10.1007/s11434-006-8214-z

    Article  Google Scholar 

  • Watanabe S, Kojima K, Ide Y, Sasaki S (2000) Effects of saline and osmotic stress on proline and sugar accumulation in Populus euphratica in vitro. Plant Cell Tissue Organ 63:199–206

    Article  CAS  Google Scholar 

  • Willams BL, Silcock DJ (1997) Nutrient and microbial changes in the peat profile beneath Sphagnum magellanicum in response to additions of ammonium nitrate. J Appl Ecol 34(4):961–970

    Article  Google Scholar 

  • Wu QS, Zou YN, Xia RX, Wang MY (2007) Five Glomus species affect water relations of Citrus tangerine during drought stress. Bot Stud 48:147–154

    Google Scholar 

  • Wu N, Zhang YM, Downing A (2009) Comparative study of nitrogenase activity in different types of biological soil crusts in the Gurbantunggut Desert, Northwestern China. J Arid Environ 73:828–833. doi:10.1016/j.jaridenv.2009.04.002

    Article  Google Scholar 

  • Wu H, Wu X, Li Z, Duan L, Zhang M (2012a) Physiological evaluation of drought stress tolerance and recovery in cauliflower (Brassica oleracea L.) seedlings treated with methyl jasmonate and coronatine. J Plant Growth Regul 31:113–123

    Article  CAS  Google Scholar 

  • Wu N, Zhang YM, Downing A, Zhang J, Yang CH (2012b) Membrane stability of the desert moss Syntrichia caninervis Mitt. during desiccation and rehydration. J Bryol 34:1–8. doi:10.1179/1743282011y.0000000043

    Article  Google Scholar 

  • Xie Z, Wang Y, Liu Y, Liu Y (2009) Ultraviolet-B exposure induces photo-oxidative damage and subsequent repair strategies in a desert cyanobacterium Microcoleus vaginatus Gom. Eur J Soil Biol 45:377–382. doi:10.1016/j.ejsobi.2009.04.003

    Article  CAS  Google Scholar 

  • Xu ZZ, Zhou GS (2006) Combined effects of water stress and high temperature on photosynthesis, nitrogen metabolism and lipid peroxidation of a perennial grass Leymus chinensis. Planta 224:1080–1090. doi:10.1007/s00425-006-0281-5

    Article  CAS  PubMed  Google Scholar 

  • Zhang YM, Wang HL, Wang XQ, Yang WK, Zhang DY (2006) The microstructure of microbiotic crust and its influence on wind erosion for a sandy soil surface in the Gurbantunggut Desert of Northwestern China. Geoderma 132:441–449. doi:10.1016/j.geoderma.2005.06.008

    Article  Google Scholar 

  • Zhang LX, Li SX, Zhang H, Liang ZS (2007a) Nitrogen rates and water stress effects on production, lipid peroxidation and antioxidative enzyme activities in two maize (Zea mays L.) genotypes. J Agron Crop Sci 193:387–397. doi:10.1111/j.1439-037X.2007.00276.x

    Article  CAS  Google Scholar 

  • Zhang YM, Chen J, Wang L, Wang XQ, Gu ZH (2007b) The spatial distribution patterns of biological soil crusts in the Gurbantunggut Desert, Northern Xinjiang, China. J Arid Environ 68:599–610. doi:10.1016/j.jaridenv.2006.06.012

    Article  Google Scholar 

  • Zhang NL, Wan SQ, Li LH, Bi J, Zhao MM, Ma KP (2008a) Impacts of urea N addition on soil microbial community in a semi-arid temperate steppe in northern China. Plant Soil 311:19–28. doi:10.1007/s11104-008-9650-0

    Article  CAS  Google Scholar 

  • Zhang Y, Zheng LX, Liu XJ, Jickells T, Cape JN, Goulding K, Fangmeier A, Zhang FS (2008b) Evidence for organic N deposition and its anthropogenic sources in China. Atmos Environ 42:1035–1041. doi:10.1016/j.atmosenv.2007.12.015

    Article  CAS  Google Scholar 

  • Zhang YM, Wu N, Zhang BC, Zhang J (2010) Species composition, distribution patterns and ecological functions of biological soil crusts in the Gurbantunggut Desert. J Arid Land 2:180–189

    Article  Google Scholar 

  • Zhang J, Zhang YM, Downing A, Wu N, Zhang BC (2011a) Photosynthetic and cytological recovery on remoistening Syntrichia caninervis Mitt., a desiccation-tolerant moss from Northwestern China. Photosynthetica 49:13–20. doi:10.1007/s11099-011-0002-6

    Article  Google Scholar 

  • Zhang W, Liu X, Hu Y, Li K, Shen J, Luo X, Song W (2011b) Analysis on input of atmospheric nitrogen dry deposition in Urumqi. Arid Zone Res 28:771–716 (in Chinese with English abstract)

    Google Scholar 

  • Zhao YM, Zhu QK, Li P, Zhao LL, Wang LL, Zheng XL, Ma H (2014) Effects of artificially cultivated biological soil crusts on soil nutrients and biological activities in the Loess Plateau. J Arid Land 6:742–752

    Article  Google Scholar 

  • Zhou XB, Zhang YM (2014) Seasonal pattern of soil respiration and gradual changing effects of nitrogen addition in a soil of the Gurbantunggut Desert, northwestern China. Atmos Environ 85:187–194. doi:10.1016/j.atmosenv.2013.12.024

    Article  CAS  Google Scholar 

  • Zhou XB, Zhang YM, Ji XH, Downing A, Serpe M (2011) Combined effects of nitrogen deposition and water stress on growth and physiological responses of two annual desert plants in northwestern China. Environ Exp Bot 74:1–8. doi:10.1016/j.envexpbot.2010.12.005

    Article  CAS  Google Scholar 

  • Zhou XB, Zhang YM, Downing A (2012) Non-linear response of microbial activity across a gradient of nitrogen addition to a soil from the Gurbantunggut Desert, northwestern China. Soil Biol Biochem 47:67–77. doi:10.1016/j.soilbio.2011.05.012

    Article  CAS  Google Scholar 

  • Zhou XB, Zhang YM, Niklas KJ (2014) Sensitivity of growth and biomass allocation patterns to increasing nitrogen: A comparison between ephemerals and annuals in the Gurbantunggut Desert, north-western China. Ann Bot-London 113:501–511. doi:10.1093/aob/mct275

    Article  Google Scholar 

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Acknowledgments

This study was jointly supported by the National Natural Science Foundation of China (41471251), the National Basic Research Program (2014CB954202), the West Light Foundation of The Chinese Academy of Sciences (XBBS-2014-20), and the Youth Innovation Promotion Association CAS (2015356). Comments of four anonymous reviewers improved the manuscript. We thank Lin Wu, Ye Tao, and Guodong Li for their hard work in the field.

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  1. Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Beijing South Road, Urumqi, 830011, China

    Xiaobing B. Zhou, Yuanming M. Zhang & Benfeng F. Yin

  2. State Key Laboratory of Earth Surface Processes and Resource Ecology, College of Life Sciences, Beijing Normal University, Beijing, 100875, China

    Benfeng F. Yin

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  1. Xiaobing B. Zhou
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Correspondence to Yuanming M. Zhang.

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Zhou, X.B., Zhang, Y.M. & Yin, B.F. Divergence in physiological responses between cyanobacterial and lichen crusts to a gradient of simulated nitrogen deposition. Plant Soil 399, 121–134 (2016). https://doi.org/10.1007/s11104-015-2687-y

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