The responses of extracellular enzyme activities and microbial community composition under nitrogen addition in an upland soil

English version

Autoři: Sami Ullah ^aff001; Chao Ai ^aff001; Shaohui Huang ^aff001; Jiajia Zhang ^aff001; Liangliang Jia ^aff002; Jinchuan Ma ^aff001; Wei Zhou ^aff001; Ping He ^aff001
Působiště autorů: Ministry of Agriculture Key Laboratory of Plant Nutrition and Fertilizer, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China ^aff001; Hebei Academy of Agriculture and Forestry Sciences, Hebei, PR China ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223026

Souhrn

Tremendous amounts of nitrogen (N) fertilizer have been added to arable lands, often resulting in substantial effects on terrestrial ecosystems, including soil acidification, altered enzyme activities and changes in microbial community composition. Soil microbes are the major drivers of soil carbon (C) and N cycling; therefore, understanding the response of microbial communities to elevated N inputs is of significant importance. This study was carried out to investigate the influences of different N fertilization rates (0, 182, and 225 kg ha^-1 representing control, low, and high N supply for each crop season for summer maize and winter wheat) on soil biochemical attributes, extracellular enzyme activities, and the microbial community composition in a winter wheat-summer maize rotation cropping system in north-central China. The results showed that N addition significantly decreased the soil pH in both the wheat and maize seasons. Microbial biomass N (MBN) decreased following N fertilization in the wheat season, while the opposite trend in MBN was observed in the maize season. Response ratio analysis showed that the activities of enzymes involved in C, N, and phosphorus cycling were significantly enhanced under N enrichment in both the wheat and maize seasons, and higher enzyme activities were noted in the high N addition treatment than in the low N addition treatment. A linear increase in fungal abundance with the N addition gradient was observed in the wheat season, whereas the fungal abundance increased and then decreased in the maize season. The bacterial abundance showed an increased and then decreased trend in response to the N addition gradient in both the wheat and maize crop seasons. Moreover, the partial least squares path model (PLS-PM) analysis showed that soil pH and soil organic carbon (SOC) were the most important soil variables, causing shifts in the soil bacteria. Furthermore, compared with the N-cycling enzymes, the C-cycling enzymes were significantly affected by the soil pH and SOC. Taken together, these results suggest that the effect of N addition on enzyme activities was consistent in both crop seasons, while the effects on MBN and microbial community composition to N addition were highly variable in the two crop seasons. Moreover, N fertilization-induced changes in the soil chemical properties such as soil acidity and SOC played a substantial role in shaping the microbial community.

Klíčová slova:

Agricultural soil science – Bacteria – Cereal crops – Crops – Fertilizers – Maize – Wheat – Soil pH

Zdroje

1. Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, et al. The global nitrogen cycle in the twenty-first century. Philosophical Transactions of the Royal Society B: Biological Sciences. 2013;368(1621):20130164.

2. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science. 2008;320(5878):889–92. doi: 10.1126/science.1136674 18487183

3. Lassaletta L, Billen G, Grizzetti B, Anglade J, Garnier J. 50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland. Environmental Research Letters. 2014;9(10):105011.

4. Guo JH, Liu XJ, Zhang Y, Shen JL, Man WX, Zhang WF, et al. Significant acidification in major Chinese croplands. Science. 2010;327(5968):1008. doi: 10.1126/science.1182570 20150447

5. Phoenix GK, Hicks WK, Cinderby S, Kuylenstierna JC, Stock WD, Dentener FJ, et al. Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Global Change Biology. 2006;12(3):470–6.

6. Wang C, Lu X, Mori T, Mao Q, Zhou K, Zhou G, et al. Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest. Soil Biol Biochem. 2018;121:103–12.

7. Zhao S, Qiu S, Cao C, Zheng C, Zhou W, He P. Responses of soil properties, microbial community and crop yields to various rates of nitrogen fertilization in a wheat–maize cropping system in north-central China. Agriculture Ecosystems & Environment. 2014;194(3):29–37.

8. Treseder KK. Nitrogen additions and microbial biomass: A meta-analysis of ecosystem studies. Ecol Lett. 2008;11(10):1111–20. doi: 10.1111/j.1461-0248.2008.01230.x 18673384

9. Fisk MC, Schmidt SK. Microbial responses to nitrogen additions in alpine tundra soil. Soil Biol Biochem. 1996;28(6):751–5.

10. Wang F, Chen S, Wang Y, Zhang Y, Hu C, Liu B. Long-term nitrogen fertilization elevates the activity and abundance of nitrifying and denitrifying microbial communities in an upland soil: implications for nitrogen loss from intensive agricultural systems. Frontiers in microbiology. 2018;9:2424. doi: 10.3389/fmicb.2018.02424 30405543

11. Ai C, Liang G, Sun J, Wang X, Zhou W. Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma. 2012;173-174(2):330–8.

12. Wang X, Song D, Liang G, Zhang Q, Ai C, Zhou W. Maize biochar addition rate influences soil enzyme activity and microbial community composition in a fluvo-aquic soil. Applied soil ecology. 2015;96:265–72.

13. Geisseler D, Scow KM. Long-term effects of mineral fertilizers on soil microorganisms–A review. Soil Biol Biochem. 2014;75:54–63.

14. Boxman AW, Blanck K, Brandrud T-E, Emmett BA, Gundersen P, Hogervorst RF, et al. Vegetation and soil biota response to experimentally-changed nitrogen inputs in coniferous forest ecosystems of the NITREX project. For Ecol Manage. 1998;101(1–3):65–79.

15. Zhang C, Song Z, Zhuang D, Wang J, Xie S, Liu G. Urea fertilization decreases soil bacterial diversity, but improves microbial biomass, respiration, and N-cycling potential in a semiarid grassland. Biol Fertility Soils. 2019:1–14.

16. Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD. High-throughput fluorometric measurement of potential soil extracellular enzyme activities. Journal of visualized experiments: JoVE. 2013;(81).

17. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, et al. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem. 2013;58:216–34.

18. Dai X, Zhou W, Liu G, Liang G, He P, Liu Z. Soil C/N and pH together as a comprehensive indicator for evaluating the effects of organic substitution management in subtropical paddy fields after application of high-quality amendments. Geoderma. 2019;337:1116–25.

19. Deng S, Tabatabai M. Cellulase activity of soils. Soil Biol Biochem. 1994;26(10):1347–54.

20. Jian S, Li J, Chen J, Wang G, Mayes MA, Dzantor KE, et al. Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis. Soil Biol Biochem. 2016;101:32–43.

21. Ai C, Zhang S, Zhang X, Guo D, Zhou W, Huang S. Distinct responses of soil bacterial and fungal communities to changes in fertilization regime and crop rotation. Geoderma. 2018;319:156–66.

22. Hartmann A, Schmid M, Van Tuinen D, Berg G. Plant-driven selection of microbes. Plant Soil. 2009;321(1–2):235–57.

23. Liljeroth E, Kuikman P, Van Veen J. Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic matter at different soil nitrogen levels. Plant Soil. 1994;161(2):233–40.

24. Ai C, Liang G, Sun J, Wang X, He P, Zhou W. Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvo-aquic soil. Soil Biol Biochem. 2013;57:30–42.

25. China Agriculture Press. 2016. China agriculture yearbook. (In Chinese.) China Agric. Press, Beijing.

26. Zhang J, He P, Xu X, Wang Y, Jia L, Cui R, et al. Nutrient expert improves nitrogen efficiency and environmental benefits for summer maize in China. Agronomy Journal. 2017;109(3):1082–90.

27. Zhang J, He P, Xu X, Ding W, Ullah S, Wang Y, et al. Nutrient Expert Improves Nitrogen Efficiency and Environmental Benefits for Winter Wheat in China. Agronomy Journal. 2018.

28. Zhang X, Zeng H, Wang W. Two contrasting seasonal patterns in microbial nitrogen immobilization from temperate ecosystems. Ecol Indicators. 2018;93:164–72.

29. Sinsabaugh RL, Hill BH, Shah JJF. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature. 2009;462(7274):795. doi: 10.1038/nature08632 20010687

30. Ma J, Li K, Cao C, Zheng C. Effect of long-term located organic-inorganic fertilizer application on fluvo-aquic soil fertility and crop yield. Plant Nutrition and Fertilizer Science. 2007;2:008.

31. Kalembasa SJ, Jenkinson DS. A comparative study of titrimetric and gravimetric methods for the determination of organic carbon in soil. J Sci Food Agric. 1973;24(9):1085–90.

32. Bremner JM, Mulvaney C. Nitrogen—Total 1. Methods of soil analysis Part 2 Chemical and microbiological properties. 1982;(methodsofsoilan2):595–624.

33. Brookes P, Landman A, Pruden G, Jenkinson D. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem. 1985;17(6):837–42.

34. Wu Y, Ding N, Wang G, Xu J, Wu J, Brookes PC. Effects of different soil weights, storage times and extraction methods on soil phospholipid fatty acid analyses. Geoderma. 2009;150(1–2):171–8.

35. Willers C, Jansen van Rensburg P, Claassens S. Phospholipid fatty acid profiling of microbial communities–a review of interpretations and recent applications. J Appl Microbiol. 2015;119(5):1207–18. doi: 10.1111/jam.12902 26184497

36. Luo Y, Hui D, Zhang D. Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology. 2006;87(1):53–63. doi: 10.1890/04-1724 16634296

37. Saiya-Cork K, Sinsabaugh R, Zak D. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem. 2002;34(9):1309–15.

38. Tenenhaus M, Vinzi VE, Chatelin Y-M, Lauro C. PLS path modeling. Comput Stat Data Anal. 2005;48(1):159–205.

39. Barberán A, Ramirez KS, Leff JW, Bradford MA, Wall DH, Fierer N. Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria. Ecol Lett. 2014;17(7):794–802. doi: 10.1111/ele.12282 24751288

40. Farrer EC, Suding KN. Teasing apart plant community responses to N enrichment: the roles of resource limitation, competition and soil microbes. Ecol Lett. 2016;19(10):1287–96. doi: 10.1111/ele.12665 27531674

41. Vitousek PM, Howarth RW. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry. 1991;13(2):87–115.

42. Wilson WA, Roach PJ, Montero M, Baroja-Fernández E, Muñoz FJ, Eydallin G, et al. Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev. 2010;34(6):952–85. doi: 10.1111/j.1574-6976.2010.00220.x 20412306

43. Thirukkumaran CM, Parkinson D. Microbial respiration, biomass, metabolic quotient and litter decomposition in a lodgepole pine forest floor amended with nitrogen and phosphorous fertilizers. Soil Biol Biochem. 2000;32(1):59–66.

44. Cleveland CC, Liptzin D. C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry. 2007;85(3):235–52.

45. Gu Y, Zhang X, Tu S, Lindström K. Soil microbial biomass, crop yields, and bacterial community structure as affected by long-term fertilizer treatments under wheat-rice cropping. European Journal of Soil Biology. 2009;45(3):239–46.

46. Serna-Chavez HM, Fierer N, Van Bodegom PM. Global drivers and patterns of microbial abundance in soil. Global Ecol Biogeogr. 2013;22(10):1162–72.

47. Wang X-L, Jia Y, Li X-G, Long R-J, Ma Q, Li F-M, et al. Effects of land use on soil total and light fraction organic, and microbial biomass C and N in a semi-arid ecosystem of northwest China. Geoderma. 2009;153(1–2):285–90.

48. Pierre WH. Nitrogenous Fertilizers and Soil Acidity: I. Effect of Various Nitrogenous Fertilizers on Soil Reaction1. Journal of the American Society of Agronomy. 1928;20.

49. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, et al. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl. 1997;7(3):737–50.

50. Shuqin J, Fang Z. Zero growth of chemical fertilizer and pesticide use: China’s objectives, progress and challenges. Journal of resources and ecology. 2018;9(1):50–9.

51. Benitez E, Sainz H, Nogales R. Hydrolytic enzyme activities of extracted humic substances during the vermicomposting of a lignocellulosic olive waste. Bioresour Technol. 2005;96(7):785–90. doi: 10.1016/j.biortech.2004.08.010 15607191

52. Springob G, Kirchmann H. Bulk soil C to N ratio as a simple measure of net N mineralization from stabilized soil organic matter in sandy arable soils. Soil Biol Biochem. 2003;35(4):629–32.

53. Leprince F, Quiquampoix H. Extracellular enzyme activity in soil: effect of pH and ionic strength on the interaction with montmorillonite of two acid phosphatases secreted by the ectomycorrhizal fungus Hebeloma cylindrosporum. Eur J Soil Sci. 1996;47(4):511–22.

54. Yang S, Meng G, Zeng L. Enzyme Catalysis Kinetic Model of pH Effect on Activity of Endo-β-glucanase. Journal of Nanjing University of Science and Technology (Natural Science). 2006;1:021.

55. Francioli D, Schulz E, Lentendu G, Wubet T, Buscot F, Reitz T. Mineral vs. organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Frontiers in microbiology. 2016;7:1446. doi: 10.3389/fmicb.2016.01446 27683576

56. Allison SD, Czimczik CI, Treseder KK. Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Global Change Biology. 2008;14(5):1156–68.

57. Treseder KK, Vitousek PM. Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology. 2001;82(4):946–54.

58. Liu L, Greaver TL. A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett. 2010;13(7):819–28. doi: 10.1111/j.1461-0248.2010.01482.x 20482580

59. Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE. Soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biol Biochem. 2014;68:252–62.

60. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. Isme Journal Multidisciplinary Journal of Microbial Ecology. 2010;4(10):1340–51.

61. Ramirez KS, Craine JM, Fierer N. Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Global Change Biology. 2012;18(6):1918–27.

62. De Deyn GB, Cornelissen JH, Bardgett RD. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett. 2008;11(5):516–31. doi: 10.1111/j.1461-0248.2008.01164.x 18279352

63. Cusack DF, Karpman J, Ashdown D, Cao Q, Ciochina M, Halterman S, et al. Global change effects on humid tropical forests: Evidence for biogeochemical and biodiversity shifts at an ecosystem scale. Rev Geophys. 2016;54(3):523–610.

64. Swathi A T, Rakesh M, Premsai S B, Louis S T, William K T, Subhash C M. Chronic N-amended soils exhibit an altered bacterial community structure in Harvard Forest, MA, USA. FEMS Microbiol Ecol. 2013;83(2):478–93. doi: 10.1111/1574-6941.12009 22974374

65. Treseder KK, Allen MF. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytologist. 2002;155(3):507–15.

66. Kara Ö, Bolat İ, Çakıroğlu K, Öztürk M. Plant canopy effects on litter accumulation and soil microbial biomass in two temperate forests. Biol Fertility Soils. 2008;45(2):193–8.

67. Chu H, Lin X, Fujii T, Morimoto S, Yagi K, Hu J, et al. Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biology & Biochemistry. 2007;39(11):2971–6.

68. Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC. Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem. 1999;31(7):1021–30.

69. Tunlid A. Biochemical analysis of biomass, community structure, nutritional status and metabolic activity of microbial communities in soil. Soil biochemistry. 1992;7:229–62.

70. Calderon FJ, Jackson LE, Scow KM, Rolston DE. Short-term dynamics of nitrogen, microbial activity, and phospholipid fatty acids after tillage. Soil Sci Soc Am J. 2001;65(1):118–26.

71. Petersen SO, Klug MJ. Effects of sieving, storage, and incubation temperature on the phospholipid fatty acid profile of a soil microbial community. Appl Environ Microbiol. 1994;60(7):2421–30. 16349325

The responses of extracellular enzyme activities and microbial community composition under nitrogen addition in an upland soil

Souhrn

Klíčová slova:

Zdroje

PLOS One

Svět praktické medicíny 1/2024 (znalostní test z časopisu)

Koncepce osteologické péče pro gynekology a praktické lékaře

Sekvenční léčba schizofrenie

Hypertenze a hypercholesterolémie – synergický efekt léčby

Význam metforminu pro „udržitelnou“ terapii diabetu