Advertisement

Changes in soil microbial community response to precipitation events in a semi-arid steppe of the Xilin River Basin, China

  • Hui Zhang
  • Wenjun Liu
  • Xiaoming Kang
  • Xiaoyong Cui
  • Yanfen Wang
  • Haitao Zhao
  • Xiaoqing Qian
  • Yanbin Hao
Article
  • 6 Downloads

Abstract

In the context of climate change, precipitation is predicted to become more intense at the global scale. Such change may alter soil microbial communities and the microbially mediated carbon and nitrogen dynamics. In this study, we experimentally repackaged precipitation patterns during the growing season (from June to September) of 2012 in a semi-arid temperate steppe of the Xilin River Basin in Inner Mongolia of China, based on the 60-year growing season precipitation data. Specifically, we manipulated a total amount of 240 mm precipitation to experimental plots by taking the following treatments: (1) P6 (6 extreme precipitation events, near the 1st percentile); (2) P10 (10 extreme precipitation events, near the 5th percentile); (3) P16 (16 moderate precipitation events, near the 50th percentile); and (4) P24 (24 events, 60-year average precipitation, near the 50th percentile). At the end of the growing season, we analyzed soil microbial community structure and biomass, bacterial abundance, fungal abundance and bacterial composition, by using phospholipid fatty acid (PLFA), real-time quantitative polymerase chain reaction (RT-qPCR) and 16S rRNA gene clone library methods. The extreme precipitation events did not change soil microbial community structure (represented by the ratio of PLFA concentration in fungi to PLFA concentration in bacteria, and the ratio of PLFA concentration in gram-positive bacterial biomass to PLFA concentration in gram-negative bacterial biomass). However, the extreme precipitation events significantly increased soil microbial activity (represented by soil microbial biomass nitrogen and soil bacterial 16S rRNA gene copy numbers). Soil fungal community showed no significant response to precipitation events. According to the redundancy analysis, both soil microbial biomass nitrogen and soil ammonium nitrogen (NH4-N) were found to be significant in shaping soil microbial community. Acidobacteria, Actinobacteria and Proteobacteria were the dominant phyla in soil bacterial composition, and responded differently to the extreme precipitation events. Based on the results, we concluded that the extreme precipitation events altered the overall soil microbial activity, but did not impact how the processes would occur, since soil microbial community structure remained unchanged.

Keywords

extreme precipitation event phospholipid fatty acid (PLFA) soil microbial community RT-qPCR soil bacteria soil fungi 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This study was financially supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA19030202) and the International Cooperation and Exchange of National Natural Science Foundation of China (31761123001, 31761143018). We greatly appreciated the Inner Mongolia Grassland Ecosystem Research Station, Chinese Academy of Sciences for the field help. We thank PANG Zhe, ZHANG Biao, DING Kai, TANG Li and MA Shuang for their help in field experiments, and are grateful to CHE Rongxiao and SHAO Yanlin for data analysis of this manuscript.

References

  1. Allen M F. 2011. Linking water and nutrients through the vadose zone: a fungal interface between the soil and plant systems. Journal of Arid Land, 3(3): 155–163.CrossRefGoogle Scholar
  2. Bai Y F, Han X G, Wu J G, et al. 2004. Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature, 431(7005): 181–184.CrossRefGoogle Scholar
  3. Bapiri A, Bååth E, Rousk J. 2010. Drying-rewetting cycles affect fungal and bacterial growth differently in an arable soil. Microbial Ecology, 60(2): 419–428.CrossRefGoogle Scholar
  4. Barnard R L, Osborne C A, Firestone M K. 2013. Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. Isme Journal, 7(11): 2229–2241.CrossRefGoogle Scholar
  5. Bell C W, Tissue D T, Loik M E, et al. 2014. Soil microbial and nutrient responses to 7 years of seasonally altered precipitation in a Chihuahuan Desert grassland. Global Change Biology, 20(5): 1657–1673.CrossRefGoogle Scholar
  6. Belnap J, Phillips S L, Miller M E. 2004. Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia, 141(2): 306–316.CrossRefGoogle Scholar
  7. Berard A, Bouchet T, Sévenier G, et al. 2011. Resilience of soil microbial communities impacted by severe drought and high temperature in the context of Mediterranean heat waves. European Journal of Soil Biology, 47(6): 333–342.CrossRefGoogle Scholar
  8. 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. Isme Journal, 7(2): 384–394.CrossRefGoogle Scholar
  9. Broeckling C D, Broz A K, Bergelson J, et al. 2008. Root exudates regulate soil fungal community composition and diversity. Applied and Environmental Microbiology, 74(3): 738–744.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. Bustin S A, Benes V, Garson J A, et al. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55(4): 611–622.CrossRefGoogle Scholar
  12. Canarini A, Carrillo Y, Mariotte P, et al. 2016. Soil microbial community resistance to drought and links to C stabilization in an Australian grassland. Soil Biology and Biochemistry, 103: 171–180.CrossRefGoogle Scholar
  13. Che R, Deng Y, Wang F, et al. 2015. 16S rRNA-based bacterial community structure is a sensitive indicator of soil respiration activity. Journal of Soils and Sediments, 15(9): 1987–1990.CrossRefGoogle Scholar
  14. Chen D M, Mi J, Chu P F, et al. 2015. Patterns and drivers of soil microbial communities along a precipitation gradient on the Mongolian Plateau. Landscape Ecology, 30(9): 1669–1682.CrossRefGoogle Scholar
  15. Chen S P, Lin G, Huang J, et al. 2009. Dependence of carbon sequestration on the differential responses of ecosystem photosynthesis and respiration to rain pulses in a semiarid steppe. Global Change Biology, 15(10): 2450–2461.CrossRefGoogle Scholar
  16. Cregger M A, Schadt C W, McDowell N G, et al. 2012. Response of the soil microbial community to changes in precipitation in a semiarid ecosystem. Applied and Environmental Microbiology, 78(24): 8587–8594.CrossRefGoogle Scholar
  17. de Vries F T, Liiri M E, Bjørnlund L, et al. 2012. Land use alters the resistance and resilience of soil food webs to drought. Nature Climate Change, 2(4): 276–280.CrossRefGoogle Scholar
  18. Dijkstra F A, Augustine D J, Brewer P, et al. 2012. Nitrogen cycling and water pulses in semiarid grasslands: are microbial and plant processes temporally asynchronous? Oecologia, 170(3): 799–808.CrossRefGoogle Scholar
  19. Easterling D R, Meehl G A, Parmesan C. 2000. Climate extremes: observations, modeling, and impacts. Science, 289(5487): 2068–2074.CrossRefGoogle Scholar
  20. Edwards U, Rogall T, Blöcker H, et al. 1989. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S-ribosomal RNA. Nucleic Acids Research, 17(19): 7843–7853.Google Scholar
  21. Evans S E, Burke I C. 2013. Carbon and nitrogen decoupling under an 11-year drought in the shortgrass steppe. Ecosystems, 16(1): 20–33.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. Fierer N, Bradford M A, Jackson R B. 2007. Toward an ecological classification of soil bacteria. Ecology, 88(6): 1354–1364.CrossRefGoogle Scholar
  24. Frostegard A, Tunlid A, Bååth E. 1993. Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Applied and Environmental Microbiology, 59(11): 3605–3617.Google Scholar
  25. Gong D Y, Shi P J, Wang J A. 2004. Daily precipitation changes in the semi-arid region over northern China. Journal of Arid Environments, 59(4): 771–784.CrossRefGoogle Scholar
  26. Goodfellow M, Williams S T. 1983. Ecology of actinomycetes. Annual Review of Microbiology, 37: 189–216.CrossRefGoogle Scholar
  27. Gordon H, Haygarth P M, Bardgett R D. 2008. Drying and rewetting effects on soil microbial community composition and nutrient leaching. Soil Biology and Biochemistry, 40(2): 302–311.CrossRefGoogle Scholar
  28. Gschwendtner S, Tejedor J, Bimueller C, et al. 2014. Climate change induces shifts in abundance and activity pattern of bacteria and archaea catalyzing major transformation steps in nitrogen turnover in a soil from a mid-European beech forest. PLoS ONE, 9(12): e116614.CrossRefGoogle Scholar
  29. Hao Y B, Wang Y F, Cui X Y. 2010. Drought stress reduces the carbon accumulation of the Leymus chinensis steppe in Inner Mongolia, China. Chinese Journal of Plant Ecology, 34(8): 898–906. (in Chinese)Google Scholar
  30. Hao Y B, Niu H S, Wang Y F, et al. 2011. Rainfall variability in ecosystem CO2 flux studies. Climate Research, 46(1): 77–83.CrossRefGoogle Scholar
  31. Hao Y B, Kang X M, Cui X Y, et al. 2012. Verification of a threshold concept of ecologically effective precipitation pulse: From plant individuals to ecosystem. Ecological Informatics, 12: 23–30.CrossRefGoogle Scholar
  32. Hao Y B, Kang X M, Wu X, et al. 2013. Is frequency or amount of precipitation more important in controlling CO2 fluxes in the 30-year-old fenced and the moderately grazed temperate steppe? Agriculture, Ecosystems & Environment, 171: 63–71.CrossRefGoogle Scholar
  33. Heisler-White J L, Knapp A K, Kelly E F. 2008. Increasing precipitation event size increases aboveground net primary productivity in a semi-arid grassland. Oecologia, 158(1): 129–140.CrossRefGoogle Scholar
  34. Hill T C J, Walsh K A, Harris J A, et al. 2003. Using ecological diversity measures with bacterial communities. Fems Microbiology Ecology, 43(1): 1–11.CrossRefGoogle Scholar
  35. Horz H P, Barbrook A, Field C B, et al. 2004. Ammonia-oxidizing bacteria respond to multifactorial global change. Proceedings of the National Academy of Sciences of the United States of America, 101(42): 15136–15141.CrossRefGoogle Scholar
  36. Horz H P, Rich V, Avrahami S, et al. 2005. Methane-oxidizing bacteria in a California upland grassland soil: Diversity and response to simulated global change. Applied and Environmental Microbiology, 71(5): 2642–2652.CrossRefGoogle Scholar
  37. Hu Y L, Wang S G, Song X P, et al. 2017. Precipitation changes in the mid-latitudes of the Chinese mainland during 1960–2014. Journal of Arid Land, 9(6): 924–937.CrossRefGoogle Scholar
  38. Huang X, Hao Y, Wang Y, et al. 2010. Partitioning of evapotranspiration and its relation to carbon dioxide fluxes in Inner Mongolia steppe. Journal of Arid Environments, 74(12): 1616–1623.CrossRefGoogle Scholar
  39. Hueso S, García C, Hernández T. 2012. Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils. Soil Biology and Biochemistry, 50: 167–173.CrossRefGoogle Scholar
  40. Ihrmark K, Bodeker I T M, Cruz-Martinez K, et al. 2012. New primers to amplify the fungal ITS2 region–evaluation by 454-sequencing of artificial and natural communities. Fems Microbiology Ecology, 82(3): 666–677.CrossRefGoogle Scholar
  41. Islam K R, Weil R R. 1998. A rapid microwave digestion method for colorimetric measurement of soil organic carbon. Communications in Soil Science and Plant Analysis, 29(15–16): 2269–2284.CrossRefGoogle Scholar
  42. Jentsch A, Kreyling J, Beierkuhnlein C. 2007. A new generation of climate-change experiments: events, not trends. Frontiers in Ecology and the Environment, 5(7): 365–374.CrossRefGoogle Scholar
  43. Kaisermann A, Maron P A, Beaumelle L, et al. 2015. Fungal communities are more sensitive indicators to non-extreme soil moisture variations than bacterial communities. Applied Soil Ecology, 86: 158–164.CrossRefGoogle Scholar
  44. Klamer M, Bååth E. 1998. Microbial community dynamics during composting of straw material studied using phospholipid fatty acid analysis. Fems Microbiology Ecology, 27(1): 9–20.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Knapp A K, Beier C, Briske D D, et al. 2008. Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience, 58(9): 811–821.CrossRefGoogle Scholar
  47. Knapp A K, Avolio M L, Beier C, et al. 2017. Pushing precipitation to the extremes in distributed experiments: recommendations for simulating wet and dry years. Global Change Biology, 23(5): 1774–1782.CrossRefGoogle Scholar
  48. Landesman W J, Dighton J. 2010. Response of soil microbial communities and the production of plant-available nitrogen to a two-year rainfall manipulation in the New Jersey Pinelands. Soil Biology and Biochemistry, 42(10): 1751–1758.CrossRefGoogle Scholar
  49. Li M, Jiang L, Sun Z, et al. 2012. Effects of flue gas desulfurization gypsum by-products on microbial biomass and community structure in alkaline-saline soils. Journal of Soils and Sediments, 12(7): 1040–1053.CrossRefGoogle Scholar
  50. Liu W J, Li L F, Biederman J A, et al. 2017. Repackaging precipitation into fewer, larger storms reduces ecosystem exchanges of CO2 and H2O in a semiarid steppe. Agricultural and Forest Meteorology, 247: 356–364.CrossRefGoogle Scholar
  51. Mckenzie H A, Wallace H S. 1954. The Kjeldahl determination of nitrogen: A critical study of digestion conditions-temperature, catalyst, and oxidizing agent. Australian Journal of Chemistry, 7(1): 55–70.CrossRefGoogle Scholar
  52. Nielsen U N, Ball B A. 2015. Impacts of altered precipitation regimes on soil communities and biogeochemistry in arid and semi-arid ecosystems. Global Change Biology, 21(4): 1407–1421.CrossRefGoogle Scholar
  53. Pachauri R K, Allen M, Barros V. et al. 2014. Climate change 2014: Synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC (Intergovernmental Panel on Climate Change), Geneva, Switzerland.Google Scholar
  54. Placella S A, Brodie E L, Firestone M K. 2012. Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proceedings of the National Academy of Sciences of the United States of America, 109(27): 10931–10936.CrossRefGoogle Scholar
  55. R Development Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  56. 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.CrossRefGoogle Scholar
  57. Steenwerth K L, Jackson L E, Calderón F J, et al. 2005. Response of microbial community composition and activity in agricultural and grassland soils after a simulated rainfall. Soil Biology and Biochemistry, 37(12): 2249–2262.CrossRefGoogle Scholar
  58. Tiemann L K, Billings S A. 2011. Changes in variability of soil moisture alter microbial community C and N resource use. Soil Biology and Biochemistry, 43(9): 1837–1847.CrossRefGoogle Scholar
  59. Vance E D, Brookes P C, Jenkinson D S. 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry, 19(6): 703–707.CrossRefGoogle Scholar
  60. Weltzin J F, Loik M E, Schwinning S. 2003. Assessing the response of terrestrial ecosystems to potential changes in precipitation. BioScience, 53(10): 941–952.CrossRefGoogle Scholar
  61. Wilcox K R, von Fischer J C, Muscha J M, et al. 2015. Contrasting above- and belowground sensitivity of three Great Plains grasslands to altered rainfall regimes. Global Change Biology, 21(1): 335–344.CrossRefGoogle Scholar
  62. Xue K, Luo H F, Qi H Y, et al. 2005. Changes in soil microbial community structure associated with two types of genetically engineered plants analyzing by PLFA. Journal of Environmental Sciences, 17(1): 130–134.Google Scholar
  63. Zeglin L H, Bottomley P J, Jumpponen A, et al. 2013. Altered precipitation regime affects the function and composition of soil microbial communities on multiple time scales. Ecology, 94(10): 2334–2345.CrossRefGoogle Scholar
  64. Zhang N L, Liu W X, Yang H J, et al. 2013. Soil microbial responses to warming and increased precipitation and their implications for ecosystem C cycling. Oecologia, 173(3): 1125–1142.CrossRefGoogle Scholar
  65. Zhang X M, Zhang G M, Chen Q S, et al. 2013. Soil bacterial communities respond to climate changes in a temperate steppe. PloS ONE, 8(11): e7861.Google Scholar
  66. Zhang K P, Shi Y, Jing X, et al. 2016. Effects of short-term warming and altered precipitation on soil microbial communities in alpine grassland of the Tibetan Plateau. Frontiers in Microbiology, 7: 1032, doi: 10.3389/fmicb.2016.01032.Google Scholar
  67. Zhang W, Zhang G S, Wu X K, et al. 2017. Bacterial diversity in the sediment of Crescent Moon Spring, Kumtag Desert, Northwest China. Journal of Arid Land, 9(2): 278–286.CrossRefGoogle Scholar
  68. Zogg G P, Zak D R, Ringelberg D B, et al. 1997. Compositional and functional shifts in microbial communities due to soil warming. Soil Science Society of America Journal, 61(2): 475–481.CrossRefGoogle Scholar
  69. Zvyagintsev D G, Zenova G M, Doroshenko E A, et al. 2007. Actinomycete growth in conditions of low moisture. Biology Bulletin, 34(3): 242–247.CrossRefGoogle Scholar

Copyright information

© Xinjiang Institute of Ecology and Geography, the Chinese Academy of Sciences and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Hui Zhang
    • 1
    • 2
  • Wenjun Liu
    • 2
  • Xiaoming Kang
    • 3
  • Xiaoyong Cui
    • 2
  • Yanfen Wang
    • 2
  • Haitao Zhao
    • 4
  • Xiaoqing Qian
    • 1
    • 4
  • Yanbin Hao
    • 2
  1. 1.College of Bioscience and BiotechnologyYangzhou UniversityYangzhouChina
  2. 2.College of Life SciencesUniversity of Chinese Academy of SciencesBeijingChina
  3. 3.Institute of Wetland ResearchChinese Academy of ForestryBeijingChina
  4. 4.College of Environmental Science and EngineeringYangzhou UniversityYangzhouChina

Personalised recommendations