Research article |
|
|
|
|
Plant property regulates soil bacterial community structure under altered precipitation regimes in a semi-arid desert grassland, China |
ZHANG Lihua1,2,*(), GAO Han1,2, WANG Junfeng3, ZHAO Ruifeng1,2, WANG Mengmeng1,2, HAO Lianyi1,2, GUO Yafei1,2, JIANG Xiaoyu1,2, ZHONG Lingfei1,2 |
1College of Geography and Environment Science, Northwest Normal University, Lanzhou 730070, China 2Key Laboratory of Resource Environment and Sustainable Development of Oasis, Lanzhou 730070, China 3College of Grassland Agriculture, Northwest Agriculture and Forestry University, Yangling 712100, China |
|
|
Abstract Variations of precipitation have great impacts on soil carbon cycle and decomposition of soil organic matter. Soil bacteria are crucial participants in regulating these ecological processes and vulnerable to altered precipitation. Studying the impacts of altered precipitation on soil bacterial community structure can provide a novel insight into the potential impacts of altered precipitation on soil carbon cycle and carbon storage of grassland. Therefore, soil bacterial community structure under a precipitation manipulation experiment was researched in a semi-arid desert grassland in Chinese Loess Plateau. Five precipitation levels, i.e., control, reduced and increased precipitation by 40% and 20%, respectively (referred here as CK, DP40, DP20, IP40, and IP20) were set. The results showed that soil bacterial alpha diversity and rare bacteria significantly changed with altered precipitation, but the dominant bacteria and soil bacterial beta diversity did not change, which may be ascribed to the ecological strategy of soil bacteria. The linear discriminate analysis (LDA) effect size (LEfSe) method found that major response patterns of soil bacteria to altered precipitation were resource-limited and drought-tolerant populations. In addition, increasing precipitation greatly promoted inter-species competition, while decreasing precipitation highly facilitated inter-species cooperation. These changes in species interaction can promote different distribution ratios of bacterial populations under different precipitation conditions. In structural equation model (SEM) analysis, with changes in precipitation, plant growth characteristics were found to be drivers of soil bacterial community composition, while soil properties were not. In conclusion, our results indicated that in desert grassland ecosystem, the sensitive of soil rare bacteria to altered precipitation was stronger than that of dominant taxa, which may be related to the ecological strategy of bacteria, species interaction, and precipitation-induced variations of plant growth characteristics.
|
Received: 30 July 2022
Published: 31 May 2023
|
Corresponding Authors:
*ZHANG Lihua (E-mail: zhanglihualz@126.com)
|
Cite this article:
ZHANG Lihua, GAO Han, WANG Junfeng, ZHAO Ruifeng, WANG Mengmeng, HAO Lianyi, GUO Yafei, JIANG Xiaoyu, ZHONG Lingfei. Plant property regulates soil bacterial community structure under altered precipitation regimes in a semi-arid desert grassland, China. Journal of Arid Land, 2023, 15(5): 602-619.
URL:
http://jal.xjegi.com/10.1007/s40333-023-0013-8 OR http://jal.xjegi.com/Y2023/V15/I5/602
|
|
|
[1] |
Amend A S, Martiny A C, Allison S D, et al. 2016. Microbial response to simulated global change is phylogenetically conserved and linked with functional potential. The ISME Journal, 10(1): 109-118.
doi: 10.1038/ismej.2015.96
|
|
|
[2] |
Anderson M J, Ellingsen K E, McArdle B H. 2006. Multivariate dispersion as a measure of beta diversity. Ecology Letters, 9(6): 683-693.
doi: 10.1111/j.1461-0248.2006.00926.x
pmid: 16706913
|
|
|
[3] |
Bao S D. 2000. Soil and Agriculture Chemistry Analysis (3rd ed). Beijing: China Agricultural Press, 30-33. (in Chinese)
|
|
|
[4] |
Bhatti A A, Haq S, Bhat R A. 2017. Actinomycetes benefaction role in soil and plant health. Microb Pathogenesis, 111: 458-467.
doi: 10.1016/j.micpath.2017.09.036
|
|
|
[5] |
Boeddinghaus R S, Marhan S, Berner D, et al. 2019. Plant functional trait shifts explain concurrent changes in the structure and function of grassland soil microbial communities. Journal of Ecology, 107(5): 2197-2210.
doi: 10.1111/1365-2745.13182
|
|
|
[6] |
Bouskill N J, Lim H C, Borglin S, et al. 2013. Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. The ISME Journal, 7(2): 384-394.
doi: 10.1038/ismej.2012.113
|
|
|
[7] |
Brookes P C, Landman A, Pruden G, et al. 1985. Chloroform fumigation and the release of soil nitrogen-A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology and Biochemistry, 17(6): 837-842.
doi: 10.1016/0038-0717(85)90144-0
|
|
|
[8] |
Caporaso J G, Kuczynski J, Stombaugh J, et al. 2010. QIIME allows analysis of high throughput community sequencing data. Nature Methods, 7(5): 335-336.
doi: 10.1038/nmeth.f.303
pmid: 20383131
|
|
|
[9] |
Caporaso J G, Lauber C L, Walters W A, et al. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences, 108(1): 4516-4522.
|
|
|
[10] |
Chaudhry V, Rehman A, Mishra A, et al. 2012. Changes in bacterial community structure of agricultural land due to long-term organic and chemical amendments. Microbial Ecology, 64(2): 450-460.
doi: 10.1007/s00248-012-0025-y
pmid: 22419103
|
|
|
[11] |
Che R, Wang S, Wang Y, et al. 2019. Total and active soil fungal community profiles were significantly altered by six years of warming but not by grazing. Soil Biology and Biochemistry, 139: 107611, doi: 10.1016/j.soilbio.2019.107611.
doi: 10.1016/j.soilbio.2019.107611
|
|
|
[12] |
Chen H, Zhao X, Lin Q, et al. 2019. Using a combination of PLFA and DNA-based sequencing analyses to detect shifts in the soil microbial community composition after a simulated spring precipitation in a semi-arid grassland in China. Science of the Total Environment, 657: 1237-1245.
doi: 10.1016/j.scitotenv.2018.12.126
|
|
|
[13] |
Chen Y, Xu T, Veresoglou S D, et al. 2017. Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biology and Biochemistry, 110: 12-21.
doi: 10.1016/j.soilbio.2017.02.015
|
|
|
[14] |
De Deyn G B, Cornelissen J H C, Bardgett R D. 2008. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecology Letters, 11(5): 516-531.
doi: 10.1111/j.1461-0248.2008.01164.x
pmid: 18279352
|
|
|
[15] |
Delgado-Baquerizo M, Maestre F T, Gallardo A, et al. 2013. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature, 502(7473): 672-676.
doi: 10.1038/nature12670
|
|
|
[16] |
Deng Y, Jiang Y H, Yang Y, et al. 2012. Molecular ecological network analyses. BMC Bioinformatics, 13: 113, doi: 10.1186/1471-2105-13-113.
doi: 10.1186/1471-2105-13-113
pmid: 22646978
|
|
|
[17] |
Du L, Wang R, Gao X, et al. 2020. Divergent responses of soil bacterial communities in erosion-deposition plots on the Loess Plateau. Geoderma, 358: 113995, doi: 10.1016/j.geoderma.2019.113995.
doi: 10.1016/j.geoderma.2019.113995
|
|
|
[18] |
Du L, Guo S, Gao X, et al. 2021. Divergent responses of soil fungal communities to soil erosion and deposition as evidenced in topsoil and subsoil. Science of the Total Environment, 755: 142616, doi: 10.1016/j.scitotenv.2020.142616.
doi: 10.1016/j.scitotenv.2020.142616
|
|
|
[19] |
Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10): 996-998.
doi: 10.1038/nmeth.2604
pmid: 23955772
|
|
|
[20] |
Fierer N, Schimel J P. 2002. Effects of drying-rewetting frequency on soil carbon and nitrogen transformations. Soil Biology and Biochemistry, 34(6): 777-787.
doi: 10.1016/S0038-0717(02)00007-X
|
|
|
[21] |
Fierer N, Bradford M A, Jackson R B. 2007. Toward an ecological classification of soil bacteria. Ecology, 88(6): 1354-1364.
doi: 10.1890/05-1839
pmid: 17601128
|
|
|
[22] |
Grime J P. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist, 111(982): 1169-1194.
doi: 10.1086/283244
|
|
|
[23] |
Guo Y, Zhang L, Zhao R, et al. 2021. Response of plant community characteristics to precipitation change in desert steppe from a monthly-scale perspective. Chinese Journal of Ecology, 40(7): 1895-1906. (in Chinese)
|
|
|
[24] |
Harris R F. 1981. Effect of water potential on microbial growth and activity. Water Potential Relations in Soil Microbiology, 9: 23-95.
|
|
|
[25] |
Ho A, Di Lonardo D P, Bodelier P L. 2017. Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiology Ecology, 93(3): fix006, doi: 10.1093/femsec/fix006.
doi: 10.1093/femsec/fix006
|
|
|
[26] |
Huang G, Li L, Su Y, et al. 2018. Differential seasonal effects of water addition and nitrogen fertilization on microbial biomass and diversity in a temperate desert. CATENA, 161: 27-36.
doi: 10.1016/j.catena.2017.09.030
|
|
|
[27] |
IPCC. 2013. Summary for policymakers. In: Stocker T F, Qin D, Plattner G K, et al. Climate Change 2013: The Physical Science Basis. Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, 25-45.
|
|
|
[28] |
Janoušková M, Kohout P, Moradi J, et al. 2018. Microarthropods influence the composition of rhizospheric fungal communities by stimulating specific taxa. Soil Biology and Biochemistry, 122: 120-130.
doi: 10.1016/j.soilbio.2018.04.016
|
|
|
[29] |
Jia M, Liu C, Li Y, et al. 2017. Response of fungal composition and diversity to simulated nitrogen deposition and manipulation of precipitation in soils of an Inner Mongolia desert steppe of northern China. Canadian Journal of Soil Science, 97(4): 613-625.
|
|
|
[30] |
Jordan S E, Palmquist K A, Bradford J B, et al. 2020. Soil water availability shapes species richness in mid-latitude shrub steppe plant communities. Journal of Vegetation Science, 31(4): 646-657.
doi: 10.1111/jvs.v31.4
|
|
|
[31] |
Knapp A K, Fay P A, Blair J M, et al. 2002. Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science, 298(5601): 2202-2205.
doi: 10.1126/science.1076347
pmid: 12481139
|
|
|
[32] |
Koyama A, Steinweg J M, Haddix M L, et al. 2018. Soil bacterial community responses to altered precipitation and temperature regimes in an old field grassland are mediated by plants. FEMS Microbiology Ecology, 94(1): fix156, doi: 10.1093/femsec/fix156.
doi: 10.1093/femsec/fix156
|
|
|
[33] |
Kuramae E, Gamper H, Van Veen J V, et al. 2011. Soil and plant factors driving the community of soil-borne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH. FEMS Microbiology Ecology, 77(2): 285-294.
doi: 10.1111/j.1574-6941.2011.01110.x
pmid: 21488909
|
|
|
[34] |
Lange M, Eisenhauer N, Sierra C A, et al. 2015. Plant diversity increases soil microbial activity and soil carbon storage. Nature Communications, 6: 7707, doi: 10.1038/ncomms7707.
doi: 10.1038/ncomms7707
|
|
|
[35] |
Lennon J T, Aanderud Z T, Lehmkuhl B K, et al. 2012. Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology, 93(8): 1867-1879.
doi: 10.1890/11-1745.1
pmid: 22928415
|
|
|
[36] |
Li H, Yang S, Xu Z, et al. 2017. Responses of soil microbial functional genes to global changes are indirectly influenced by aboveground plant biomass variation. Soil Biology and Biochemistry, 104: 18-29.
doi: 10.1016/j.soilbio.2016.10.009
|
|
|
[37] |
Li X, Yan Y, Lu X, et al. 2022. Responses of soil bacterial communities to precipitation change in the semi-arid alpine grassland of northern Tibet. Frontiers in Plant Science, 13: 1036369, doi: 10.3389/fpls.2022.1036369.
doi: 10.3389/fpls.2022.1036369
|
|
|
[38] |
Li Z, Xiao H, Tang Z, et al. 2015. Microbial responses to erosion-induced soil physico-chemical property changes in the hilly red soil region of southern China. European Journal of Soil Biology, 71: 37-44.
doi: 10.1016/j.ejsobi.2015.10.003
|
|
|
[39] |
Liu J, Wu N, Wang H, et al. 2016. Nitrogen addition affects chemical compositions of plant tissues, litter and soil organic matter. Ecology, 97(7): 1796-1806.
doi: 10.1890/15-1683.1
pmid: 27859176
|
|
|
[40] |
Liu X, Huang Z, Havrilla C A, et al. 2021. Plant litter crust role in nutrients cycling potentials by bacterial communities in a sandy land ecosystem. Land Degradation & Development, 32(11): 3194-3203.
doi: 10.1002/ldr.v32.11
|
|
|
[41] |
Lynch M D J, Neufeld J D. 2015. Ecology and exploration of the rare biosphere. Nature Reviews Microbiology, 13(4): 217-229.
doi: 10.1038/nrmicro3400
pmid: 25730701
|
|
|
[42] |
Magoč T, Salzberg S L. 2011. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21): 2957-2963.
doi: 10.1093/bioinformatics/btr507
pmid: 21903629
|
|
|
[43] |
Makhalanyane T P, Valverde A, Gunnigle E, et al. 2015. Microbial ecology of hot desert edaphic systems. FEMS Microbiology Reviews, 39(2): 203-221.
doi: 10.1093/femsre/fuu011
pmid: 25725013
|
|
|
[44] |
Manzoni S, Schimel J P, Porporato A. 2012. Responses of soil microbial communities to water stress: Results from a meta-analysis. Ecology, 93(4): 930-938.
doi: 10.1890/11-0026.1
pmid: 22690643
|
|
|
[45] |
Manzoni S, Schaeffer S M, Katul G, et al. 2014. A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils. Soil Biology and Biochemistry, 73: 69-83.
doi: 10.1016/j.soilbio.2014.02.008
|
|
|
[46] |
Meier C L, Bowman W D. 2008. Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proceedings of the National Academy of Sciences, 105(50): 19780-19785.
|
|
|
[47] |
Meisner A, Jacquiod S, Snoek B L, et al. 2018. Drought legacy effects on the composition of soil fungal and prokaryote communities. Frontiers in Microbiology, 9: 294, doi: 10.3389/fmicb.2018.00294.
doi: 10.3389/fmicb.2018.00294
pmid: 29563897
|
|
|
[48] |
Mitchell R J, Hester A J, Campbell C D, et al. 2010. Is vegetation composition or soil chemistry the best predictor of the soil microbial community?. Plant and Soil, 333(1): 417-430.
doi: 10.1007/s11104-010-0357-7
|
|
|
[49] |
Na X, Yu H, Wang P, et al. 2019. Vegetation biomass and soil moisture coregulate bacterial community succession under altered precipitation regimes in a desert steppe in northwestern China. Soil Biology and Biochemistry, 136: 107520, doi: 10.1016/j.soilbio.2019.107520.
doi: 10.1016/j.soilbio.2019.107520
|
|
|
[50] |
Ochoa-Hueso R, Collins S L, Delgado-Baquerizo M, et al. 2018. Drought consistently alters the composition of soil fungal and bacterial communities in grasslands from two continents. Global Change Biology, 24(7): 2818-2827.
doi: 10.1111/gcb.14113
pmid: 29505170
|
|
|
[51] |
Preece C, Verbruggen E, Liu L, et al. 2019. Effects of past and current drought on the composition and diversity of soil microbial communities. Soil Biology and Biochemistry, 131: 28-39.
doi: 10.1016/j.soilbio.2018.12.022
|
|
|
[52] |
Prein A F, Rasmussen R M, Ikeda K, et al. 2017. The future intensification of hourly precipitation extremes. Nature Climate Change, 7(1): 48-52.
doi: 10.1038/NCLIMATE3168
|
|
|
[53] |
Ren H, Xu Z, Huang J, et al. 2015. Increased precipitation induces a positive plant-soil feedback in a semi-arid grassland. Plant and Soil, 389(1): 211-223.
doi: 10.1007/s11104-014-2349-5
|
|
|
[54] |
Rickbeil G J M, Coops N C, Andrew M E, et al. 2014. Assessing conservation regionalization schemes: Employing a beta diversity metric to test the environmental surrogacy approach. Diversity and Distributions, 20(5): 503-514.
doi: 10.1111/ddi.2014.20.issue-5
|
|
|
[55] |
Shade A, Jones S E, Caporaso J G, et al. 2014. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio, 5(4): e01371-14, doi: 10.1128/mBio.01371-14.
doi: 10.1128/mBio.01371-14
|
|
|
[56] |
She W, Bai Y, Zhang Y, et al. 2018. Resource availability drives responses of soil microbial communities to short-term precipitation and nitrogen addition in a desert shrubland. Frontiers in Microbiology, 9: 186, doi: 10.3389/fmicb.2018.00186.
doi: 10.3389/fmicb.2018.00186
pmid: 29479346
|
|
|
[57] |
Sorensen P O, Germino M J, Feris K P. 2013. Microbial community responses to 17 years of altered precipitation are seasonally dependent and coupled to co-varying effects of water content on vegetation and soil C. Soil Biology and Biochemistry, 64: 155-163.
doi: 10.1016/j.soilbio.2013.04.014
|
|
|
[58] |
Standing D B, Castro J I R, Prosser J I, et al. 2005. Rhizosphere carbon flow:A driver of soil microbial diversity. In: Bardgett R D, Usher M B, Hopkins D W. Biological Diversity and Function in Soils. Cambridge: Cambridge University Press, 57-79.
|
|
|
[59] |
Umair M, Sun N, Du H, et al. 2020. Bacterial communities are more sensitive to water addition than fungal communities due to higher soil K and Na in a degraded Karst ecosystem of southwestern China. Frontiers in Microbiology, 11: 562546, doi: 10.3389/fmicb.2020.562546.
doi: 10.3389/fmicb.2020.562546
|
|
|
[60] |
Wang Q, Garrity G M, Tiedje J M, et al. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261-5267.
doi: 10.1128/AEM.00062-07
pmid: 17586664
|
|
|
[61] |
Wang S, Zuo X, Awada T, et al. 2021. Changes of soil bacterial and fungal community structure along a natural aridity gradient in desert grassland ecosystems, Inner Mongolia. CATENA, 205: 105470, doi: 10.1016/j.catena.2021.105470.
doi: 10.1016/j.catena.2021.105470
|
|
|
[62] |
Wang Y, Xie Y, Ma H, et al. 2022. Responses of soil microbial communities and networks to precipitation change in a typical steppe ecosystem of the Loess Plateau. Microorganisms, 10(4): 817, doi: 10.3390/microorganisms10040817.
doi: 10.3390/microorganisms10040817
|
|
|
[63] |
Wu K, Xu W, Yang W. 2020. Effects of precipitation changes on soil bacterial community composition and diversity in the Junggar Desert of Xinjiang, China. PeerJ, 8: e8433, doi: 10.7717/peerj.8433.
doi: 10.7717/peerj.8433
|
|
|
[64] |
Wu Z, Dijkstra P, Koch G W, et al. 2011. Responses of terrestrial ecosystems to temperature and precipitation change: A meta-analysis of experimental manipulation. Global Change Biology, 17(2): 927-942.
doi: 10.1111/gcb.2010.17.issue-2
|
|
|
[65] |
Xian W, Zhang X, Li W. 2020. Research status and prospect on bacterial phylum Chloroflexi. Acta Microbiologica Sinica, 60(9): 1801-1820. (in Chinese)
|
|
|
[66] |
Yan J, Wang L, Hu Y, et al. 2018. Plant litter composition selects different soil microbial structures and in turn drives different litter decomposition pattern and soil carbon sequestration capability. Geoderma, 319: 194-203.
doi: 10.1016/j.geoderma.2018.01.009
|
|
|
[67] |
Yang X, Zhu K, Loik M E, et al. 2021. Differential responses of soil bacteria and fungi to altered precipitation in a meadow steppe. Geoderma, 384: 114812, doi: 10.1016/j.geoderma.2020.114812.
doi: 10.1016/j.geoderma.2020.114812
|
|
|
[68] |
Zhang L, Xie Z, Zhao R, et al. 2018. Plant, microbial community and soil property responses to an experimental precipitation gradient in a desert grassland. Applied Soil Ecology, 127: 87-95.
doi: 10.1016/j.apsoil.2018.02.005
|
|
|
[69] |
Zhang N, Liu W, Yang H, et al. 2013. Soil microbial responses to warming and increased precipitation and their implications for ecosystem C cycling. Oecologia, 173(3): 1125-1142.
doi: 10.1007/s00442-013-2685-9
pmid: 23736549
|
|
|
[70] |
Zhang W, Wei H L, Gao H W, et al. 2005. Advances of studies on soil microbial diversity and environmental impact factors. Chinese Journal of Ecology, 24(1): 48-52. (in Chinese)
|
|
|
[71] |
Zhao Q, Jian S, Nunan N, et al. 2017. Altered precipitation seasonality impacts the dominant fungal but rare bacterial taxa in subtropical forest soils. Biology and Fertility of Soils, 53(2): 231-245.
doi: 10.1007/s00374-016-1171-z
|
|
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|