Abstract
Background
Recently, it has been found that nitrogen (N) deposition strongly affects the coverage of biocrusts. However, we know little about the response of exopolysaccharides (EPSs), the key cementing material in the formation and stability of biocrusts, to N deposition.
Method
Three N-sources including nitrate, ammonia and urea were added to biocrusts at three rates (2 mg/g, 4 mg/g, 8 mg/g) to evaluate the effect of N additions on the growth of biocrusts and the abundance of EPS.
Results
Our results showed 2 mg/g of nitrate–N had no obvious effect on the cyanobacterial biomass, while 4 and 8 mg/g of nitrate–N inhibited the growth of Microcoleus vaginatus, the dominant cyanobacterium in biocrusts, but promoted other cyanobacteria growth. Ammonia-N and urea-N strongly decreased the cyanobacterial biomass, indicated by chlorophyll-a and 16 s rRNA gene copy-numbers. On the whole, N additions had a positive impact on the α-biodiversity of biocrusts. However, Ammonia-N and urea-N shifted the bacterial communities from more Cyanobacteria to more Proteobacteria and Actinobacteria. Notably, lesser-N (2 mg/g) promoted the excretion of EPSs, while greater-N (8 mg/g) had the opposite effect, and the total proportion of rhamnose and fucose in EPSs decreased in all treatment groups.
Conclusion
N additions (except 2 mg/g of nitrate–N) reduced cyanobacterial biomass and affected the bacterial communities in biocrusts, which would obstruct the development and succession of biocrusts. Meanwhile, the simultaneous reductions of the EPSs contents and proportion of rhamnose and fucose in EPSs may further reduce stability and persistence of cyanobacterial biocrusts, after N additions.
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Data availability
The data sets supporting the results of this article are included within the article and its additional files.
Code availability
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Abbreviations
- N:
-
Nitrogen
- Chl-a:
-
Chlorophyll-a
- nitr2, nitr4, nitr8:
-
Nitrate nitrogen-2 mg/g, 4 mg/g, 8 mg/g
- ammon2, ammon4, ammon8:
-
Ammonia nitrogen-2 mg/g, 4 mg/g, 8 mg/g
- urea2, urea4, urea8:
-
Urea nitrogen-2 mg/g, 4 mg/g, 8 mg/g
- N2, N4, N8:
-
Nitrogen contents-2 mg/g, 4 mg/g, 8 mg/g
- M. vaginatus :
-
Microcoleus vaginatus
- EPS:
-
Exopolysaccharides
- RPS:
-
Released exopolysaccharides
- CPS:
-
Capsule exopolysaccharides
References
Belnap J (2003) The world at your feet: desert biological soil crusts. Front Ecol Environ 1:181–189
Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178. https://doi.org/10.1002/hyp.6325
Benvenutto-Vargas VP, Ochoa-Hueso R (2020) Effects of nitrogen deposition on the spatial pattern of biocrusts and soil microbial activity in a semi-arid Mediterranean shrubland. Funct Ecol 34:923–937. https://doi.org/10.1111/1365-2435.13512
Bobbink R, Hicks K, Gallesseray J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, 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. https://doi.org/10.1890/08-1140.1
Brull LP, Huang ZB, Thomas-Oates JE, Paulsen BS, Cohen EH, Michaelsen TE (2000) Studies of polysaccharides from three edible species of Nostoc (cyanobacteria) with different colony morphologies: Structural characterization and effect on the complement system of polysaccharides from Nostoc commune. J Phycol 36:871–881. https://doi.org/10.1046/j.1529-8817.2000.00038.x
Burton SAQ, Prosser JI (2001) Autotrophic ammonia oxidation at lesser pH through urea hydrolysis. Appl Environ Microbiol 67:2952–2957. https://doi.org/10.1128/aem.67.7.2952-2957.2001
Castillo-Monroy AP, Maestre FT, Delgado-Baquerizo M, Gallardo A (2010) Biological soil crusts modulate nitrogen availability in semi-arid ecosystems: insights from a Mediterranean grassland. Plant Soil 333:21–34. https://doi.org/10.1007/s11104-009-0276-7
Chamizo S, Adessi A, Mugnai G, Simiani A, De Philippis R (2019) Soil Type and Cyanobacteria Species Influence the Macromolecular and Chemical Characteristics of the Polysaccharidic Matrix in Induced Biocrusts. Microb Ecol 78:482–493. https://doi.org/10.1007/s00248-018-1305-y
Chamizo S, Adessi A, Torzillo G, De Philippis R (2020) Exopolysaccharide Features Influence Growth Success in Biocrust-forming Cyanobacteria, Moving From Liquid Culture to Sand Microcosms. Front Microbiol 11. https://doi.org/10.3389/fmicb.2020.568224
Chen L-Z, Wang G-H, Hong S, Liu A, Li C, Liu Y-D (2009) UV-B-induced Oxidative Damage and Protective Role of Exopolysaccharides in Desert Cyanobacterium Microcoleus vaginatus. J Integr Plant Biol 51:194–200. https://doi.org/10.1111/j.1744-7909.2008.00784.x
Chen L, Rossi F, Deng S, Liu Y, Wang G, Adessi A, De Philippis R (2014) Macromolecular and chemical features of the excreted extracellular polysaccharides in induced biological soil crusts of different ages. Soil Biol Biochem 78:1–9. https://doi.org/10.1016/j.soilbio.2014.07.004
Chen F, Huang GL, Yang ZY, Hou YP (2019) Antioxidant activity of Momordica charantia polysaccharide and its derivatives. Int J Biol Macromol 138:673–680. https://doi.org/10.1016/j.ijbiomac.2019.07.129
Cheng Y, Wang J, Chang SX, Cai Z, Mueller C, Zhang J (2019) Nitrogen deposition affects both net and gross soil nitrogen transformations in forest ecosystems: A review. Environ Pollut 244:608–616. https://doi.org/10.1016/j.envpol.2018.10.054
Cho DH, Chae HJ, Kim EY (2001) Synthesis and characterization of a novel extracellular polysaccharide by Rhodotorula glutinis. Appl Biochem Biotechnol 95:183–193. https://doi.org/10.1385/abab:95:3:183
Chrismas NAM, Barker G, Anesio AM, Sanchez-Baracaldo P (2016) Genomic mechanisms for cold tolerance and production of exopolysaccharides in the Arctic cyanobacterium Phormidesmis priestleyi BC1401. BMC Genomics 17:14. https://doi.org/10.1186/s12864-016-2846-4
Colica G, Li H, Rossi F, De Philippis R, Liu Y (2015) Differentiation of the characteristics of excreted extracellular polysaccharides reveals the heterogeneous primary succession of induced biological soil crusts. J Appl Phycol 27:1935–1944. https://doi.org/10.1007/s10811-015-0532-6
Collos Y, Harrison PJ (2014) Acclimation and toxicity of greater ammonium concentrations to unicellular algae. Mar Pollut Bull 80:8–23. https://doi.org/10.1016/j.marpolbul.2014.01.006
Costa OYA, Raaijmakers JM, Kuramae EE (2018) Microbial Extracellular Polymeric Substances: Ecological Function and Impact on Soil Aggregation. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.01636
Couradeau E, Giraldo-Silva A, De Martini F, Garcia-Pichel F (2019) Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere. Microbiome 7. https://doi.org/10.1186/s40168-019-0661-2
Dai GZ, Qiu BS, Forchhammer K (2014) Ammonium tolerance in the cyanobacterium Synechocystis sp strain PCC 6803 and the role of the psbA multigene family. Plant, Cell Environ 37:840–851. https://doi.org/10.1111/pce.12202
De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22:151–175. https://doi.org/10.1016/S0168-6445(98)00012-6
Delattre C, Pierre G, Laroche C, Michaud P (2016) Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides. Biotechnol Advance 34:1159–1179. https://doi.org/10.1016/j.biotechadv.2016.08.001
Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168:167–167. https://doi.org/10.1038/168167a0
Ehling-Schulz M, Scherer S (1999) UV protection in cyanobacteria. Eur J Phycol 34:329–338. https://doi.org/10.1080/09670269910001736392
Elbert W, Weber B, Burrows S, Steinkamp J, Budel B, Andreae MO, Poschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462. https://doi.org/10.1038/ngeo1486
Evans RD, Belnap J (1999) Long-term consequences of disturbance on nitrogen dynamics in an arid ecosystem. Ecology 80:150–160. https://doi.org/10.1890/0012-9658(1999)080[0150:LTCODO]2.0.CO;2
Ferree MA, Shannon RD (2001) Evaluation of a second derivative UV/visible spectroscopy technique for nitrate and total nitrogen analysis of wastewater samples. Water Res 35:327–332. https://doi.org/10.1016/s0043-1354(00)00222-0
Fischer SE, Miguel MJ, Mori GB (2003) Effect of root exudates on the exopolysaccharide composition and the lipopolysaccharide profile of Azospirillum brasilense Cd under saline stress. FEMS Microbiol Lett 219:53–62. https://doi.org/10.1016/s0378-1097(02)01194-1
Flores E, Picossi S, Valladares A, Herrero A (2019) Transcriptional regulation of development in heterocyst-forming cyanobacteria. Biochimica Et Biophysica Acta-Gene Regulatory Mechanisms 1862:673–684. https://doi.org/10.1016/j.bbagrm.2018.04.006
Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Gallesseray JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos Trans R Soc Lond B Biol Sci 368:13. https://doi.org/10.1098/rstb.2013.0164
Freedman ZB, Romanowicz KJ, Upchurch RA, Zak DR (2015) Differential responses of total and active soil microbial communities to long-term experimental N deposition. Soil Biol Biochem 90:275–282. https://doi.org/10.1016/j.soilbio.2015.08.014
Frosler J, Panitz C, Wingender J, Flemming HC, Rettberg P (2017) Survival of Deinococcus geothermalis in Biofilms under Desiccation and Simulated Space and Martian Conditions. Astrobiology 17:431–447. https://doi.org/10.1089/ast.2015.1431
Ge H, Zhang J, Zhou X, Xia L, Hu C (2014) Effects of light intensity on components and topographical structures of extracellular polymeric substances from Microcoleus vaginatus (Cyanophyceae). Phycologia 53:167–173. https://doi.org/10.2216/13-163.1
Gupta V, Germida JJ (2015) Soil aggregation: Influence on microbial biomass and implications for biological processes. Soil Biol Biochem 80:A3–A9. https://doi.org/10.1016/j.soilbio.2014.09.002
Han PP, Yao SY, Guo RJ, Shen SG, Yan RR, Tan ZL, Jia SR (2017) The relationship between monosaccharide composition of extracellular polysaccharide and activities of related enzymes in Nostoc flagelliforme under different culture conditions. Carbohyd Polym 174:111–119. https://doi.org/10.1016/j.carbpol.2017.05.093
Holland EA, Braswell BH, Sulzman J, Lamarque JF (2005) Nitrogen deposition onto the United States and western Europe: Synthesis of observations and models. Ecol Appl 15:38–57. https://doi.org/10.1890/03-5162
Hu CX, Liu YD, Paulsen BS, Petersen D, Klaveness B (2003) Extracellular carbohydrate polymers from five desert soil algae with different cohesion in the stabilization of fine sand grain. Carbohyd Polym 54:33–42. https://doi.org/10.1016/s0144-8617(03)00135-8
Karray F, Gargouri M, Chebaane A, Mhiri N, Mliki A, Sayadi S (2020) Climatic Aridity Gradient Modulates the Diversity of the Rhizosphere and Endosphere Bacterial Microbiomes ofOpuntia ficus-indica. Front Microbiol 11:15. https://doi.org/10.3389/fmicb.2020.01622
Kielak AM, Castellane TCL, Campanharo JC, Colnago LA, Costa OYA, da Silva MLC, van Veen JA, Lemos EGM, Kuramae EE (2017) Characterization of novel Acidobacteria exopolysaccharides with potential industrial and ecological applications. Sci Rep 7. https://doi.org/10.1038/srep41193
Knowles VL, Plaxton WC (2003) From genome to enzyme: analysis of key glycolytic and oxidative pentose-phosphate pathway enzymes in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 44:758–763. https://doi.org/10.1093/pcp/pcg086
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 65:77–88. https://doi.org/10.1007/s12665-011-1066-0
Lan S, Zhang Q, Wu L, Liu Y, Zhang D, Hu C (2014) Artificially Accelerating the Reversal of Desertification: Cyanobacterial Inoculation Facilitates the Succession of Vegetation Communities. Environ Sci Technol 48:307–315. https://doi.org/10.1021/es403785j
Lan S, Wub L, Zhang D, Hu C (2015) Effects of light and temperature on open cultivation of desert cyanobacterium Microcoleus vaginatus. Biores Technol 182:144–150. https://doi.org/10.1016/j.biortech.2015.02.002
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. https://doi.org/10.1890/06-2057.1
Leung PH, Wu JY (2007) Effects of ammonium feeding on the production of bioactive metabolites (cordycepin and exopolysaccharides) in mycelial culture of a Cordyceps sinensis fungus. J Appl Microbiol 103:1942–1949. https://doi.org/10.1111/j.1365-2672.2007.03451.x
Ling N, Chen D, Guo H, Wei J, Bai Y, Shen Q, Hu S (2017) Differential responses of soil bacterial communities to long-term N and P inputs in a semi-arid steppe. Geoderma 292:25–33. https://doi.org/10.1016/j.geoderma.2017.01.013
Liu XJ, Duan L, Mo JM, Du EZ, Shen JL, Lu XK, Zhang Y, Zhou XB, He CN, Zhang FS (2011) Nitrogen deposition and its ecological impact in China: An overview. Environ Pollut 159:2251–2264. https://doi.org/10.1016/j.envpol.2010.08.002
Liu XR, Eusterhues K, Thieme J, Ciobota V, Hoschen C, Mueller CW, Kusel K, Kogel-Knabner I, Rosch P, Popp J, Totsche KU (2013) STXM and NanoSIMS Investigations on EPS Fractions before and after Adsorption to Goethite. Environ Sci Technol 47:3158–3166. https://doi.org/10.1021/es3039505
Liu XC, Zhu ZY, Tang YL, Wang MF, Wang Z, Liu AJ, Zhang YM (2016) Structural properties of polysaccharides from cultivated fruit bodies and mycelium of Cordyceps militaris. Carbohyd Polym 142:63–72. https://doi.org/10.1016/j.carbpol.2016.01.040
Liu J, Liu W, Long X-E, Chen Y, Huang T, Huo J, Duan L, Wang X (2020) Effects of nitrogen addition on C:N:P stoichiometry in moss crust-soil continuum in the N-limited Gurbantunggut Desert, Northwest China. Eur J Soil Biol 98. https://doi.org/10.1016/j.ejsobi.2020.103174
Mager D, Thomas A (2011) Extracellular polysaccharides from cyanobacterial soil crusts: a review of their role in dryland soil processes. J Arid Environ 75:91–97
Marsh KL, Sims GK, Mulvaney RL (2005) Availability of urea to autotrophic ammonia-oxidizing bacteria as related to the fate of C-14- and N-15-labeled urea added to soil. Biol Fertil Soils 42:137–145. https://doi.org/10.1007/s00374-005-0004-2
Merino-Martin L, Stokes A, Gweon HS, Moragues-Saitua L, Staunton S, Plassard C, Oliver A, Le Bissonnais Y, Griffiths RI (2021) Interacting effects of land use type, microbes and plant traits on soil aggregate stability. Soil Biol Biochem 154. https://doi.org/10.1016/j.soilbio.2020.108072
Miralles I, Lazaro R, Sanchez-Maranon M, Soriano M, Ortega R (2020) Biocrust cover and successional stages influence soil bacterial composition and diversity in semiarid ecosystems. Sci Total Environ 709. https://doi.org/10.1016/j.scitotenv.2019.134654
Nelson C, Garcia-Pichel F (2021) Beneficial Cyanosphere Heterotrophs Accelerate Establishment of Cyanobacterial Biocrust. Appl Environ Microbiol 87:e0123621. https://doi.org/10.1128/AEM.01236-21
Nelson C, Giraldo-Silva A, Garcia-Pichel F (2021) A symbiotic nutrient exchange within the cyanosphere microbiome of the biocrust cyanobacterium, Microcoleus vaginatus. ISME J 15:282–292. https://doi.org/10.1038/s41396-020-00781-1
Patterson GM, Bolis CM (1995) Regulation of scytophycin accumulation in cultures of Scytonema ocellatum. II Nutrient Requirements. Appl Microbiol Biotechnol 43:692–700
Pereira S, Zille A, Micheletti E, Moradas-Ferreira P, De Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol Rev 33:917–941. https://doi.org/10.1111/j.1574-6976.2009.00183.x
Qian L, Ye X, Xiao J, Lin S, Wang H, Liu Z, Ma Y, Yang L, Zhang Z, Wu L (2021) Nitrogen concentration acting as an environmental signal regulates cyanobacterial EPS excretion. Chemosphere: 132878–132878. https://doi.org/10.1016/j.chemosphere.2021.132878
Rath KM, Fierer N, Murphy DV, Rousk J (2019) Linking bacterial community composition to soil salinity along environmental gradients. ISME J 13:836–846. https://doi.org/10.1038/s41396-018-0313-8
Redfield E, Barns SM, Belnap J, Daane LL, Kuske CR (2002) Comparative diversity and composition of cyanobacteria in three predominant soil crusts of the Colorado Plateau. FEMS Microbiol Ecol 40:55–63. https://doi.org/10.1111/j.1574-6941.2002.tb00936.x
Rodriguez-Caballero E, Belnap J, Budel B, Crutzen PJ, Andreae MO, Poschl U, Weber B (2018) Dryland photoautotrophic soil surface communities endangered by global change. Nat Geosci 11: 185-+. https://doi.org/10.1038/s41561-018-0072-1
Rong XY, Zhou XB, Li XZ, Yao MJ, Lu YX, Xu P, Yin BF, Li YG, Aanderud ZT, Zhang YM (2022) Biocrust diazotrophs and bacteria rather than fungi are sensitive to chronic lesser N deposition. Environ Microbiol. https://doi.org/10.1111/1462-2920.16095
Rossi F, De Philippis R (2015) Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats. Life (basel, Switzerland) 5:1218–1238. https://doi.org/10.3390/life5021218
Rossi F, Micheletti E, Bruno L, Adhikary SP, Albertano P, De Philippis R (2012a) Characteristics and role of the exocellular polysaccharides produced by five cyanobacteria isolated from phototrophic biofilms growing on stone monuments. Biofouling 28:215–224. https://doi.org/10.1080/08927014.2012.663751
Rossi F, Potrafka RM, Pichel FG, Philippis RD (2012b) The role of the exopolysaccharides in enhancing hydraulic conductivity of biological soil crusts. Soil Biol Biochem 46:33–40
Rossi F, Mugnai G, De Philippis R (2018) Complex role of the polymeric matrix in biological soil crusts. Plant Soil 429:19–34. https://doi.org/10.1007/s11104-017-3441-4
Smith KS, Ferry JG (2000) Prokaryotic Carbonic Anhydrases. Fems Microbiol Rev 24:335–366. https://doi.org/10.1111/j.1574-6976.2000.tb00546.x
Solórzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801. https://doi.org/10.4319/lo.1969.14.5.0799
Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria1Publication 2274 of the Centre of Estuarine and Coastal Ecology, Yerseke, The Netherlands. 1. FEMS Microbiol Rev 21:179–211. https://doi.org/10.1016/S0168-6445(97)00056-9
Stuart RK, Mayali X, Lee JZ, Craig Everroad R, Hwang M, Bebout BM, Weber PK, Pett-Ridge J, Thelen MP (2016) Cyanobacterial reuse of extracellular organic carbon in microbial mats. ISME J 10:1240–1251
Su YG, Li XR, Zheng JG, Huang G (2009) The effect of biological soil crusts of different successional stages and conditions on the germination of seeds of three desert plants. J Arid Environ 73:931–936. https://doi.org/10.1016/j.jaridenv.2009.04.010
Veluci RM, Neher DA, Weicht TR (2006) Nitrogen fixation and leaching of biological soil crust communities in mesic temperate soils. Microb Ecol 51:189–196. https://doi.org/10.1007/s00248-005-0121-3
Victor DG (2011) Climate change and world order: implications for the UN, industry, diplomacy, and the great powers. In: DG Victor (ed) Global Warming Gridlock: Creating More Effective Strategies for Protecting the Planet. Cambridge University Press, Cambridge
Wang J, Bao J, Su J, Li X, Chen G, Ma X (2015) Impact of inorganic nitrogen additions on microbes in biological soil crusts. Soil Biol Biochem 88:303–313. https://doi.org/10.1016/j.soilbio.2015.06.004
Wang JC, Xue C, Song Y, Wang L, Huang QW, Shen QR (2016) Wheat and Rice Growth Stages and Fertilization Regimes Alter Soil Bacterial Community Structure, But Not Diversity. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.01207
Warren SD, St Clair LL, Stark LR, Lewis LA, Pombubpa N, Kurbessoian T, Stajich JE, Aanderud ZT (2019) Reproduction and Dispersal of Biological Soil Crust Organisms. Front Ecol Evol 7:17. https://doi.org/10.3389/fevo.2019.00344
Xia JY, Wan SQ (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179:428–439. https://doi.org/10.1111/j.1469-8137.2008.02488.x
Ye CR, Tao Y, Zhang YR, Cao J, Ke T, Wei SJ, De Philippis R, Chen LZ (2020) Monosaccharide composition of primary cell wall polysaccharides as a developmental level indicator of biological soil crusts. CATENA 195:8. https://doi.org/10.1016/j.catena.2020.104782
Yu GR, Jia YL, He NP, Zhu JX, Chen Z, Wang QF, Piao SL, Liu XJ, He HL, Guo XB, Wen Z, Li P, Ding GA, Goulding K (2019) Stabilization of atmospheric nitrogen deposition in China over the past decade. Nat Geosci 12: 424-+. https://doi.org/10.1038/s41561-019-0352-4
Yuan HZ, Ge TD, Zhou P, Liu SL, Roberts P, Zhu HH, Zou ZY, Tong CL, Wu JS (2013) Soil microbial biomass and bacterial and fungal community structures responses to long-term fertilization in paddy soils. J Soils Sediments 13:877–886. https://doi.org/10.1007/s11368-013-0664-8
Zaady E, Kuhn U, Wilske B, Sandoval-Soto L, Kesselmeier J (2000) Patterns of CO2 exchange in biological soil crusts of successional age. Soil Biol Biochem 32:959–966
Zeng J, Liu XJ, Song L, Lin XG, Zhang HY, Shen CC, Chu HY (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49. https://doi.org/10.1016/j.soilbio.2015.09.018
Zha SH, Zhao QS, Chen JJ, Wang LW, Zhang GF, Zhang H, Zhao B (2014) Extraction, purification and antioxidant activities of the polysaccharides from maca (Lepidium meyenii). Carbohyd Polym 111:584–587. https://doi.org/10.1016/j.carbpol.2014.05.017
Zhai ZY, Chen A, Zhou HM, Zhang DY, Du XH, Liu Q, Wu XY, Cheng JE, Chen LJ, Hu F, Liu Y, Su P (2021) Structural characterization and functional activity of an exopolysaccharide secreted by Rhodopseudomonas palustris GJ-22. Int J Biol Macromol 167:160–168. https://doi.org/10.1016/j.ijbiomac.2020.11.165
Zhang M, Zhang X, Zhang L, Zeng L, Liu Y, Wang X, He P, Li S, Liang G, Zhou W, Ai C (2021) The stronger impact of inorganic nitrogen fertilization on soil bacterial community than organic fertilization in short-term condition. Geoderma 382. https://doi.org/10.1016/j.geoderma.2020.114752.
Zhong YQ, Yan WM, Zhouping SG (2015) Impact of long-term N additions upon coupling between soil microbial community structure and activity, and nutrient-use efficiencies. Soil Biol Biochem 91:151–159. https://doi.org/10.1016/j.soilbio.2015.08.030
Zhou Z, Wang C, Zheng M, Jiang L, Luo Y (2017) Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115:433–441. https://doi.org/10.1016/j.soilbio.2017.09.015
Zhou X, Tao Y, Yin B, Tucker C, Zhang Y (2020) Nitrogen pools in soil covered by biological soil crusts of different successional stages in a temperate desert in Central Asia. Geoderma 366. https://doi.org/10.1016/j.geoderma.2019.114166.
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This study was kindly supported by the National Natural Science Foundation of China (U1703120; U2003120; 32061123009).
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Long Qian: Conceptualization, Data curation, Visualization, Writing-original draft. Jingshang Xiao: Methodology, Data curation, Validation. Ling Xia: Conceptualization, Resource, Writing-review & editing. Shaoxian Song: Formal analysis, Project administration, Investigation. María E. Farías: Writing-review & editing, Methodology. Rosa María Torres: Formal analysis, Project administration, Investigation. Lie Yang: Supervision, Oversight and leadership responsibility for the research activity planning and execution, including mentorship external to the core team. Zulin Zhang: Project administration, Mannoseagement and coordination responsibility for the research activity planning and execution. Li Wu: Acquisition of the financial support for the project leading to this publication. Review & Editing, Preparabinosetion, creation and/or presentation of the published work by those from the original research group, specifically critical review, commentary or revision – including pre-or postpublication stages.
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Qian, L., Xiao, J., Zhang, Z. et al. Impact of different nitrogen additions on microbes and exopolysaccharides excretion in cyanobacterial biocrusts. Plant Soil 487, 229–247 (2023). https://doi.org/10.1007/s11104-023-05920-z
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DOI: https://doi.org/10.1007/s11104-023-05920-z