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Journal of Arid Land  2021, Vol. 13 Issue (3): 239-256    DOI: 10.1007/s40333-021-0061-x
Research article     
Snowpack shifts cyanobacterial community in biological soil crusts
ZHANG Bingchang1,2, ZHANG Yongqing1, ZHOU Xiaobing2, LI Xiangzhen3,*(), ZHANG Yuanming2,*()
1Geographical Science College, Shanxi Normal University, Linfen 041004, China
2State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
3Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China
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Winter snowpack is an important source of moisture that influences the development of biological soil crusts (BSCs) in desert ecosystems. Cyanobacteria are important photosynthetic organisms in BSCs. However, the responses of the cyanobacterial community in BSCs to snowpack, snow depth and melting snow are still unknown. In this study, we investigated the cyanobacterial community composition and diversity in BSCs under different snow treatments (doubled snow, ambient snow and removed snow) and three snow stages (stage 1, snowpack; stage 2, melting snow; and stage 3, melted snow) in the Gurbantunggut Desert in China. In stages 1 and 2, Cyanobacteria were the dominant phylum in the bacterial community in the removed snow treatment, whereas Proteobacteria and Bacteroidetes were abundant in the bacterial communities in the ambient snow and doubled snow treatments. The relative abundances of Proteobacteria and Bacteroidetes increased with increasing snow depth. The relative abundances of Cyanobacteria and other bacterial taxa were affected mainly by soil temperature and irradiance. In stages 2 and 3, the relative abundance of Cyanobacteria increased quickly due to the suitable soil moisture and irradiance conditions. Oscillatoriales, Chroococcales, Nostocales, Synechococcales and unclassified Cyanobacteria were detected in all the snow treatments, and the most dominant taxa were Oscillatoriales and Chroococcales. Various cyanobacterial taxa showed different responses to snowpack. Soil moisture and irradiance were the two critical factors shaping the cyanobacterial community structure. The snowpack depth and duration altered the soil surface irradiance, soil moisture and other soil properties, which consequently were selected for different cyanobacterial communities. Thus, local microenvironmental filtering (niche selection) caused by snow conditions may be a dominant process driving shifts in the cyanobacterial community in BSCs.

Key wordscyanobacterial diversity      community structure      biological soil crusts      snowpack      niche selection     
Published: 10 March 2021
Corresponding Authors: LI Xiangzhen,ZHANG Yuanming     E-mail:;
About author: ZHANG Yuanming (E-mail:
* LI Xiangzhen (E-mail:;
Cite this article:

ZHANG Bingchang, ZHANG Yongqing, ZHOU Xiaobing, LI Xiangzhen, ZHANG Yuanming. Snowpack shifts cyanobacterial community in biological soil crusts. Journal of Arid Land, 2021, 13(3): 239-256.

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Fig. 1 Location of the study area in the Gurbantunggut Desert (a) and demonstration of the experimental design (b). DS, double snow; AS, ambient snow; RS, removed snow.
Environmental property Fsnow treatments
Fsnow stages
Fsnow treatments×snow stages (df=4) Environmental property Fsnow treatments
Fsnow stage
Fsnow treatments×snow stages (df=4)
SOC 4.489* 5.995** 3.256* pH 10.381** 2.117 0.445
Total N 5.219* 5.266* 4.849** EC 0.947 13.675** 2.307
Total P 0.580 0.217 0.187 Total salts 3.468 0.667 1.031
Total K 1.041 2.261 0.525 Soil moisture 19.179** 129.255** 5.565**
Available N 3.290 0.580 1.979 Soil temperature 1685.724** 37.588** 409.824**
Available P 0.783 1.288 5.078** Irradiance 3999.179** 793.259** 409.196
Available K 6.858** 0.315 0.612
Table 1 Repeated-measures ANOVA results for the effects of snow treatments, snow stages and their interactions on the environmental properties of biological soil crusts (BSCs)
Table 2 Soil physicochemical properties of BSCs in different snow treatments and stages
Fig. 2 Effects of snow depth and stages on (a) cyanobacterial OTUs (operational taxonomic units; richness) and (b) relative abundance in the total bacterial community. Stage 1, snowpack; Stage 2, melting snow; Stage 3, melted snow; DS, double snow; AS, ambient snow; RS, removed snow. Bars mean standard deviations. The different lowercase letters indicate significant differences at the P<0.05 level among different snow treatments in the same stage (LSD). The different uppercase letters indicate significant differences at the P<0.05 level (LSD) in different stages of the same snow treatment.
df Nostocales Oscillatoriales Chroococcales Synechococcales Unclassified Cyanobacteria
Fsnow treatments 2 2.364 6.193* 6.674** 4.172* 3.223*
Fsnow stages 2 4.098* 3.798* 3.395 1.231 1.646
Fsnow treatments×snow stages 4 1.630 3.798* 2.656 0.514 2.911*
Table 3 Repeated-measures ANOVA results for the effects of snow treatments, snow stages and their interactions on the relative abundances of cyanobacterial orders in BSCs
Table 4 Dominant cyanobacterial taxa and their relative abundances in the total bacterial community in different treatments and stages
Fig. 3 RDA plots showing the relationships between cyanobacterial OTU compositions and soil physicochemical properties. RDA, canonical redundancy analysis; DS, double snow; AS, ambient snow; RS, removed snow; SOC, soil organic carbon; EC, electrical conductivity.
Fig. S1 Phylogenetic trees based on the 16S rRNA (ribosomal ribonucleic acid) gene representative sequences of cyanobacterial operational taxonomic units (OTUs) from biological soil crusts (BSCs) samples and reference sequences using maximum likelihood method
Fig. S2 Bacterial community compositions in different snow treatments and snow stages. Stage 1, snowpact; Stage 2, melting snow; Stage 3, melted snow; DS, double snow; AS, ambient snow; RS, removed snow. The data in the figure are the mean relative abundance of five replicate samples. The data at top of each bar is the total numbers of bacterial OTUs.
Table S1 Correlation coefficients among soil physicochemical properties of biological soil crusts (BSCs)
Table S2 Affiliations of cyanobacterial operational taxonomic units (OTUs) and their relative abundances in BSCs in different snow treatments and stages
[1]   Aanderud Z T, Jones S E, Schoolmaster D R, et al. 2013. Sensitivity of soil respiration and microbial communities to altered snowfall. Soil Biology and Biochemistry, 57:217-227.
[2]   Ade L J, Hu L, Zi H B, et al. 2018. Effect of snowpack on the soil bacteria of alpine meadows in the Qinghai-Tibetan Plateau of China. Catena, 164:13-22.
[3]   An J X, Liu C, Wang Q, et al. 2019. Soil bacterial community structure in Chinese wetlands. Geoderma, 337:290-299.
[4]   Belnap J, Lange O L. 2003. Biological Soil Crusts: Structure, Function, and Management. Berlin: Springer, 218-260.
[5]   Borcard D, Gillet F, Legendre P. 2011. Numerical Ecology with R. New York: Springer, 137-200.
[6]   Bowker M A, Belnap J. 2004. Predictive modeling of biological soil crusts can be used as a tool for better range management. The Bulletin of the Ecological Society of America Annual Meeting Abstracts, 89:58.
[7]   Brooks P D, Grogan P, Templer P H, et al. 2011. Carbon and nitrogen cycling in snow-covered environments. Geography Compass, 5(9):682-699.
[8]   Büdel B, Dulić T, Darienko T. 2016. Cyanobacteria and algae of biological soil crusts. In: Weber B, Büdel B, Belnap J. Biological Soil Crusts: An Organizing Principle in Drylands. Mainz: Spinger, 55-80.
[9]   Chen Y N, Wang Q, Li W H, et al. 2007. Microbiotic crusts and their interrelations with environmental factors in the Gurbantonggut desert, western China. Environmental Geology, 52:691-700.
[10]   Fernandes V M C, Lima N M M, Roush D, et al. 2018. Exposure to predicted precipitation patterns decreases population size and alters community structure of cyanobacteria in biological soil crusts from the Chihuahuan Desert. Environmental Microbiology, 20(1):259-269.
doi: 10.1111/1462-2920.13983 pmid: 29124873
[11]   Garcia-Pichel F, Belnap J. 1996. Microenvironments and microscale productivity of cyanobacterial desert crusts. Journal of Phycology, 32(5):774-782.
[12]   Garcia-Pichel F, Loza V, Marusenko V, et al. 2013. Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science, 340(6140):1574-1577.
doi: 10.1126/science.1236404 pmid: 23812714
[13]   Ge H M, Zhang J, Zhou X P, et al. 2014. Effects of light intensity on components and topographical structures of extracellular polymeric substances from Microcoleus vaginatus (Cyanophyceae). Phycologia, 53(2):167-173.
[14]   Guo G X, Kong W D, Liu J B, et al. 2015. Diversity and distribution of autotrophic microbial community along environmental gradients in grassland soils on the Tibetan Plateau. Applied Microbiology and Biotechnology, 99(20):8765-8776.
doi: 10.1007/s00253-015-6723-x pmid: 26084890
[15]   Hu C X, Zhang D L, Huang Z B, et al. 2003. The vertical microdistribution of cyanobacteria and green algae within desert crusts and the development of the algal crusts. Plant and Soil, 257(1):97-111.
[16]   IPCC. 2003. Climate Change 2013: The Physical Science Basis. In: Stocker T F, Qin D, Plattner G K, et al. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.
[17]   Kapnick S B, Delworth T L. 2013. Controls of global snow under a changed climate. Journal of Climate, 26(15):5537-5562.
[18]   Kiderová J, Elster J. 2019. Ecophysiology of cyanobacteria in the Polar Regions. In: Mishre A K, Tiwari D N, Rai A N. Cyanobacteria from Basic Science to Applications. London: Academic Press, 277-301.
[19]   Lan S B, Wu L, Zhang D L, et al. 2014. Desiccation provides photosynthetic protection for crust cyanobacteria Microcoleus vaginatus from high temperature. Physiologia Plantarum, 152(2):345-354.
doi: 10.1111/ppl.12176 pmid: 24611508
[20]   Lange O L. 2003. Photosynthesis of soil-crust biota as dependent on environmental factors. In: Belnap J, Lange O L. Biological Soil Crusts: Structure, Function, and Management. Berlin: Springer, 217-240.
[21]   Li P, Sayer E J, Jia Z, et al. 2020. Deepened winter snow cover enhances net ecosystem exchange and stabilizes plant community composition and productivity in a temperate grassland. Global Change Biology, 26(5):3015-3027.
pmid: 32107822
[22]   Li Y, Tao H, Su B D, et al. 2019. Impacts of 1.5°C and 2°C global warming on winter snow depth in Central Asia. Science of The Total Environment, 651:2866-2873.
[23]   Novis P M, Whitehead D, Gregorich E D G, et al. 2007. Annual carbon fixation in terrestrial populations of Nostoc commune (Cyanobacteria) from an Antarctic dry valley is driven by temperature regime. Global Change Biology, 13(6):1224-1237.
[24]   Potts M. 1999. Mechanisms of desiccation tolerance in cyanobacteria. Europe Journal of Phycology, 34(4):319-328.
[25]   Pushkareva E, Pessi I S, Namsaraev Z, et al. 2018. Cyanobacteria inhabiting biological soil crusts of a polar desert: Sør Rondane Mountains, Antarctica. Systematic and Applied Microbiology, 41(1):363-373.
[26]   Qian Y B, Wu Z N, Zhao R F, et al. 2008. Vegetation patterns and species-environment relationships in the Gurbantunggut Desert of China. Journal of Geographical Sciences, 18(4):400-414.
[27]   Rajeev L, da Rocha U N, Klitgord N, et al. 2013. Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust. ISMI Journal, 7(11):2178-2191.
[28]   Redfield E, Barns S M, Belnap J, et al. 2002. Comparative diversity and composition of cyanobacteria in three predominant soil crusts of the Colorado Plateau. FEMS Microbiology Ecology, 40(1):55-63
doi: 10.1111/j.1574-6941.2002.tb00936.x pmid: 19709211
[29]   Ren Y, Zhang L, Yang K, et al. 2020. Short-term effects of snow cover manipulation on soil bacterial diversity and community composition. Science of The Total Environment, 741. doi: 10.1016/j.scitotenv.2020.140454.
[30]   Schmidt S K, Vimercati L. 2019. Growth of cyanobacterial soil crusts during diurnal freez-thaw cycles. Journal of Microbiology, 57(4):243-251.
[31]   Steven B, Gallegos-Graves L V, Belnap J, et al. 2013. Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material. FEMS Microbiology Ecology, 86(1):101-113.
doi: 10.1111/1574-6941.12143 pmid: 23621290
[32]   Strong C L, Bullard J E, Burford M A, et al. 2013. Response of cyanobacterial soil crusts to moisture and nutrient availability. Catena, 109:195-202.
[33]   Su Y G, Huang G, Lin Y J, et al. 2016. No synergistic effects of water and nitrogen addition on soil microbial communities and soil respiration in a temperate desert. Catena, 142:126-133.
[34]   Vincent W F. 2007. Cold tolerance in cyanobacteria and life in the cryosphere. In: Seckbach J. Algae and Cyanobacteria in Extreme Environments (e-book). Netherlands: Springer, 287-301.
[35]   Vries F T D, Griffiths R L. 2018. Impacts of climate change on soil microbial communities and their functioning. Developments in Soil Science, 35:111-129.
[36]   Wang J, Zhang P, Bao J, et al. 2020. Comparison of cyanobacterial communities in temperate deserts: A cue for artificial inoculation of biological soil crusts. Science of The Total Environment, 745, doi: 10.1016/j.scitotenv.2020.140970.
[37]   Wu X D, Xu H Y, Liu G M, et al. 2017. Bacterial communities in the upper soil layers in the permafrost regions on the Qinghai-Tibetan plateau. Applied Soil Ecology, 120:81-88.
[38]   Xu L, Zhu B J, Li C, et al. 2020. Development of biological soil crust prompts convergent succession of prokaryotic communities. Catena, 187:104360.
[39]   Yang L, Jiang M, Zhu W H, et al. 2019. Soil bacterial communities with an indicative function response to nutrients in wetlands of Northeastern China that have undergone natural restoration. Ecological Indicators, 101:562-571.
[40]   Yuan H Z, Ge T D, Chen C Y, et al. 2012. Significant role for microbial autotrophy in the sequestration of soil carbon. Applied and Environmental Microbiology, 78(7):2328-2336.
[41]   Zhang B C, Zhou X B, Zhang Y M. 2015. Responses of microbial activities and soil physical-chemical properties to the successional process of biological soil crusts in the Gurbantunggut Desert, Xinjiang. Journal of Arid Land, 7(1):101-109.
[42]   Zhang Y M, Chen J, Wang X Q, et al. 2007. The spatial distribution patterns of biological soil crusts in the Gurbantunggut Desert, Northern Xinjiang, China. Journal of Arid Environments, 68(4):599-610.
[43]   Zhao R M, Hui R, Wang Z L, et al. 2016. Winter snowfall can have a positive effect on photosynthetic carbon fixation and biomass accumulation of biological soil crusts from the Gurbantunggut Desert, China. Ecological Research, 31(2):251-262.
[44]   Zhao R M, Hui R, Liu L C, et al. 2018. Effects of snowfall depth on soil physical-chemical properties and soil microbial biomass in moss-dominated crusts in the Gurbantunggut Desert, Northern China. Catena, 169:175-182.
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