Abstract
Aims
This study aimed at assessing whether patch type (i.e., under-shrub soil patch and inter-shrub soil patch) has an effect on soil microbes and how different shrub species altered the soil microbes through understanding soil microbial activity, biomass, and community structure.
Methods
We characterized the soil microbes in under-shrub and inter-shrub soil patches in three shrublands (Artemisia ordosica, Salix psammophila, and Caragana microphylla), respectively, in the Mu Us Desert, China, using microbial activity indicators, chloroform fumigation-extraction analysis, and high-throughput 16S rRNA gene sequencing.
Results
Members of the phyla Proteobacteria, Actinobacteria, Acidobacteria, Planctomycetes, Bacteroidetes, Chloroflexi, Firmicutes, and Gemmatimonadetes were dominant. Inter-shrub soil patch differed from under-shrub soil patch in soil bacterial composition, microbial enzyme activity, and biomass, but not in diversity. Soil collected in A. ordosica shrubland exhibited the highest microbial enzyme activity, biomass, and diversity. Shrub species had significant effects on community structure, primarily the relative abundance of Proteobacteria, Actinobacteria, and Bacteroidetes.
Conclusions
The results indicated that both shrub species and patch type had effects on soil microbial communities. In shrub-dominated desert ecosystems, spatial heterogeneity of soil nutrients and moisture might not be the main factors underlying variations in bacterial diversity. The different compositions of microbial communities in various shrublands provide a foundation for further research into the mechanisms of soil organic carbon accumulation.
Similar content being viewed by others
References
Acosta-Martinez V, Dowd SE, Sun Y, Wester D, Allen V (2010) Pyrosequencing analysis for characterization of soil bacterial populations as affected by an integrated livestock-cotton production system. Appl Soil Ecol 45:13–25. doi:10.1016/j.apsoil.2010.01.005
Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256. doi:10.1016/j.soilbio.2006.04.011
Bachar A, Soares MIM, Gillor O (2012) The effect of resource islands on abundance and diversity of bacteria in arid soils. Microbial Ecol 63:694–700. doi:10.1007/s00248-011-9957-x
Bai YF, Wu JG, Xing Q, Pan QM, Huang JH, Yang DL, Han XG (2008) Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology 89:2140–2153. doi:10.1890/07-0992.1
Ben-David EA, Zaady E, Sher Y, Nejidat A (2011) Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses. FEMS Microbiol Ecol 76:492–503. doi:10.1111/j.1574-6941.2011.01075.x
Brockett BFT, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44:9–20. doi:10.1016/j.soilbio.2011.09.003
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. doi:10.1016/0038-0717(85)90144-0
Černohlávková J, Jarkovský J, Nešporová M, Hofman J (2009) Variability of soil microbial properties: effects of sampling, handling and storage. Ecotoxicol Environ Saf 72:2102–2108. doi:10.1016/j.ecoenv.2009.04.023
Cheng M, Xue ZJ, Xiang Y, Darboux F, An SS (2015) Soil organic carbon sequestration in relation to revegetation on the Loess Plateau, China. Plant Soil 397:31–42. doi:10.1007/s11104-015-2486-5
Clark JS, Campbell JH, Grizzle H, Acosta-Martìnez V, Zak JC (2009) Soil microbial community response to drought and precipitation variability in the Chihuahuan Desert. Microbial Ecol 57:248–260. doi:10.1007/s00248-008-9475-7
Diedhiou-Sall S, Dossa EL, Diedhiou I, Badiane AN, Assigbetsé KB, Samba SAN, Khoumag M, Sèneh M, Dick RP (2013) Microbiology and macrofaunal activity in soil beneath shrub canopies during residue decomposition in agroecosystems of the Sahel. Soil Sci Soc Am J 77:501–511. doi:10.2136/sssaj2012.0284
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381
Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903. doi:10.1016/j.soilbio.2010.02.003
Eisenhauer N, Beßler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch S, Sabais ACW, Scherber C, Steinbeiss S, Weigelt A, Weisser WW, Scheu S (2010) Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91:485–496. doi:10.1890/08-2338.1
Evenari M, Shanan L, Tadmor N (1982) The Negev: the challenge of a desert. Harvard University Press, Cambridge
Ewing SA, Southard RJ, Macalady JL, Hartshorn AS, Johnson MJ (2007) Soil microbial fingerprints, carbon, and nitrogen in a Mojave Desert creosote-bush ecosystem. Soil Sci Soc Am J 71:469–475. doi:10.2136/sssaj2005.0283
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. doi:10.1890/05-1839
Fließbach A, Sarig S, Steinberger Y (1994) Effects of water pulses and climatic conditions on microbial biomass kinetics and microbial activity in a Yermosol of the central Negev. Arid Land Res Manag 8:353–362. doi:10.1080/15324989409381409
Geisseler D, Horwath WR, Scow KM (2011) Soil moisture and plant residue addition interact in their effect on extracellular enzyme activity. Pedobiologia 54:71–78. doi:10.1016/j.pedobi.2010.10.001
Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809. doi:10.1128/AEM.69.3.1800-1809.2003
Goberna M, Pascual JA, Garcia C, Sánchez J (2007) Do plant clumps constitute microbial hotspots in semiarid Mediterranean patchy landscapes? Soil Biol Biochem 39:1047–1054. doi:10.1016/j.soilbio.2006.11.015
Guan SY, Zhang DS, Zhang ZM (1991) Methods of soil enzyme activities analysis. Agriculture Press, Beijing, pp 368–386
Herzberger AJ, Meiners SJ, Towey JB, Butts PA, Armstrong DL (2015) Plant–microbe interactions change along a tallgrass prairie restoration chronosequence. Restor Ecol 23:220–227. doi:10.1111/rec.12165
Hortal S, Bastida F, Armas C, Lozano YM, Moreno JL, Garcia C, Pugnaire FI (2013) Soil microbial community under a nurse-plant species changes in composition, biomass and activity as the nurse grows. Soil Biol Biochem 64:139–146. doi:10.1016/j.soilbio.2013.04.018
Hortal S, Bastida F, Moreno JL, Armas C, García C, Pugnaire FI (2015) Benefactor and allelopathic shrub species have different effects on the soil microbial community along an environmental severity gradient. Soil Biol Biochem 88:48–57. doi:10.1016/j.soilbio.2015.05.009
Hu R, Wang XP, Zhang YF, Shi W, Jin YX, Chen N (2016) Insight into the influence of sand-stabilizing shrubs on soil enzyme activity in a temperate desert. Catena 137:526–535. doi:10.1016/j.catena.2015.10.022
Huang L, Zhang ZS (2015) Stable isotopic analysis on water utilization of two xerophytic shrubs in a revegetated desert area: Tengger Desert, China. Water 7:1030–1045. doi:10.3390/w7031030
Jia X, Zha TS, Wu B, Zhang YQ, Gong JN, Qing SG, Chen GP, Qian D, Kellomäki S, Peltola H (2014) Biophysical controls on net ecosystem CO2 exchange over a semiarid shrubland in northwest China. Biogeosciences 11:4679–4693. doi:10.5194/bg-11-4679-2014
Jiang YM, Chen CR, Xu ZH, Liu YQ (2012) Effects of single and mixed species forest ecosystems on diversity and function of soil microbial community in subtropical China. J Soil Sediment 12:228–240. doi:10.1007/s11368-011-0442-4
Kardol P, Wardle DA (2010) How understanding aboveground–belowground linkages can assist restoration ecology. Trends Ecol Evol 25:670–679. doi:10.1016/j.tree.2010.09.001
Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the Proteobacteria. In: Dwarkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes, vol 5. Springer, New York, pp 3–37
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microb 79:5112–5120. doi:10.1128/AEM.01043-13
Ladygina N, Hedlund K (2010) Plant species influence microbial diversity and carbon allocation in the rhizosphere. Soil Biol Biochem 42:162–168. doi:10.1016/j.soilbio.2009.10.009
Lai ZR, Zhang YQ, Liu JB, Wu B, Qin SG, Fa KY (2016) Fine-root distribution, production, decomposition, and effect on soil organic carbon of three revegetation shrub species in northwest China. Forest Ecol Manag 359:381–388. doi:10.1016/j.foreco.2015.04.025
Lamb EG, Kennedy N, Siciliano SD (2011) Effects of plant species richness and evenness on soil microbial community diversity and function. Plant Soil 338:483–495. doi:10.1007/s11104-010-0560-6
Lange M, Habekost M, Eisenhauer N, Roscher C, Bessler H, Engels C, Oelmann Y, Scheu S, Wilcke W, Schulze E-D, Gleixner G (2014) Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland. PLoS One 9(5):e96182. doi:10.1371/journal.pone.0096182
Legay N, Baxendale C, Grigulis K, Krainer U, Kastl E, Schloter M, Bardgett RD, Arnoldi C, Bahn M, Dumont M, Poly F, Pommier T, Clément JC, Lavorel S (2014) Contribution of above- and below-ground plant traits to the structure and function of grassland soil microbial communities. Ann Bot-London 114:1011–1021. doi:10.1093/aob/mcu169
Li JJ, Zhou XM, Yan JX, Li HJ, He JZ (2015) Effects of regenerating vegetation on soil enzyme activity and microbial structure in reclaimed soils on a surface coal mine site. Appl Soil Ecol 87:56–62. doi:10.1016/j.apsoil.2014.11.010
Liu JB, Zhang YQ, Wu B, Qin SG, Lai ZR (2014) Changes in soil organic carbon and its density fractions after shrub-planting for desertification control. Pol J Ecol 62:205–216. doi:10.3161/104.062.0202
Liu JB, Zhang YQ, Wu B, Qin SG, Jia X, Fa KY, Feng W, Lai ZR (2015) Effect of vegetation rehabilitation on soil carbon and its fractions in Mu Us Desert, northwest China. Int J Phytoremediation 17:529–537. doi:10.1080/15226514.2014.922923
Lozano YM, Hortal S, Armas C, Pugnaire FI (2014) Interactions among soil, plants, and microorganisms drive secondary succession in a dry environment. Soil Biol Biochem 78:298–306. doi:10.1016/j.soilbio.2014.08.007
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. doi:10.1093/bioinformatics/btr507
Merilä P, Malmivaara-Lämsä M, Spetz P, Stark S, Vierikko K, Derome J, Fritze H (2010) Soil organic matter quality as a link between microbial community structure and vegetation composition along a successional gradient in a boreal forest. Appl Soil Ecol 46:259–267. doi:10.1016/j.apsoil.2010.08.003
Nemergut DR, Cleveland CC, Wieder WR, Washenberger CL, Townsend AR (2010) Plot-scale manipulations of organic matter inputs to soils correlate with shifts in microbial community composition in a lowland tropical rain forest. Soil Biol Biochem 42:2153–2160. doi:10.1016/j.soilbio.2010.08.011
Prober SM, Leff JW, Bates ST et al (2015) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18:85–95. doi:10.1111/ele.12381
R Development Core Team (2011) R: A language and environment for statistical computing. R 21 Foundation for statistical computing, Vienna, Austria.
Scheibe A, Steffens C, Seven J, Jacob A, Hertel D, Leuschner C, Gleixner G (2015) Effects of tree identity dominate over tree diversity on the soil microbial community structure. Soil Biol Biochem 81:219–227. doi:10.1016/j.soilbio.2014.11.020
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. doi:10.1186/gb-2011-12-6-r60
Shen JP, Zhang LM, Guo JF, Ray JL, He JZ (2010) Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in northeast China. Appl Soil Ecol 46:119–124. doi:10.1016/j.apsoil.2010.06.015
Šnajdr J, Dobiášová P, Urbanová M, Petránková M, Cajthaml T, Frouz J, Baldrian P (2013) Dominant trees affect microbial community composition and activity in post-mining afforested soils. Soil Biol Biochem 56:105–115. doi:10.1016/j.soilbio.2012.05.004
Uroz S, Buée M, Murat C, Frey-Klett P, Martin F (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microbiol Rep 2:281–288. doi:10.1111/j.1758-2229.2009.00117.x
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. doi:10.1016/0038-0717(87)90052-6
Vokou D, Chalkos D, Karamanlidou G, Yiangou M (2002) Activation of soil respiration and shift of the microbial population balance in soil as a response to Lavandula stoechas essential oil. J Chem Ecol 28:755–768. doi:10.1023/A:1015236709767
Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270. doi:10.1073/pnas.1320054111
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38
Wang B, Xue S, Liu GB, Zhang GH, Li G, Ren ZP (2012) Changes in soil nutrient and enzyme activities under different vegetations in the Loess Plateau area, northwest China. Catena 92:186–195. doi:10.1016/j.catena.2011.12.004
Xu XF, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr 22:737–749. doi:10.1111/geb.12029
Yang ZP, Zhang Q, Wang YL, Zhang JJ, Chen MC (2011) Spatial and temporal variability of soil properties under Caragana microphylla shrubs in the northwestern Shanxi Loess Plateau, China. J Arid Environ 75:538–544. doi:10.1016/j.jaridenv.2011.01.007
Yang XL, Deng SQ, De Philippis R, Chen LZ, Hu CZ, Zhang WH (2012) Chemical composition of volatile oil from Artemisia ordosica and its allelopathic effects on desert soil microalgae, Palmellococcus miniatus. Plant Physiol Biochem 51:153–158. doi:10.1016/j.plaphy.2011.10.019
Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050. doi:10.1890/02-0433
Zeller B, Liu JX, Buchmann N, Richter A (2008) Tree girdling increases soil N mineralization in two spruce stands. Soil Biol Biochem 40:1155–1166. doi:10.1016/j.soilbio.2007.12.009
Zhu BB, Li ZB, Li P, Liu GB, Xue S (2010) Soil erodibility, microbial biomass, and physical–chemical property changes during long-term natural vegetation restoration: a case study in the Loess Plateau, China. Ecol Res 25:531–541. doi:10.1007/s11284-009-0683-5
Acknowledgments
This study was supported by the National Key Research and Development Program of China (no. 2016YFC0500905), National Natural Science Foundation of China (no. 31470711), and the Fundamental Research Funds for the Central Universities (no. 2015ZCQ-SB-02). We would like to thank the staff of the Yanchi Research Station. Special thanks to Weiwei She, Jun Liu and Li Wang for their help with sampling and measurements in the field and laboratory.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Liz Shaw.
Rights and permissions
About this article
Cite this article
Sun, Y., Zhang, Y., Feng, W. et al. Effects of xeric shrubs on soil microbial communities in a desert in northern China. Plant Soil 414, 281–294 (2017). https://doi.org/10.1007/s11104-016-3111-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-016-3111-y