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Long-term phosphorus addition downregulate microbial investments on enzyme productions in a mature tropical forest

  • Cong Wang
  • Taiki Mori
  • Qinggong Mao
  • Kaijun Zhou
  • Zhuohang Wang
  • Yongqun Zhang
  • Hui Mo
  • Xiankai LuEmail author
  • Jiangming Mo
Soils, Sec 4 • Ecotoxicology • Research Article
  • 76 Downloads

Abstract

Purpose

Phosphorus (P) addition could largely alter soil microbial activity. However, effects of long-term P addition on soil extracellular enzyme activity are not well understood in tropical forests.

Materials and methods

To address this question, we measured absolute activities (activity per unit of dry soil) and specific activities (activity per unit of microbial biomass carbon) of enzymes involved in carbon (C), nitrogen (N), and P cycling in a 10-year P addition experimental site in a tropical forest.

Results and discussion

Phosphorus addition decreased acid phosphatase absolute and specific activity by 37% and 47%, respectively. As to N-acquisition enzymes, P addition increased leucine amino peptidase absolute activity but decreased β-1,4-N-acetylglucosaminidase absolute activity by 33%. Meanwhile, P addition had no effects on leucine amino peptidase specific activity but decreased β-1,4-N-acetylglucosaminidase specific activity by 43%. Among C-acquisition enzymes, cellobiohydrolase, α-glucosidase, and β-glycosidase absolute and specific activities showed no significant responses to P addition, while P addition decreased β-xylosidase absolute and specific activity by 15% and 27% respectively. Phosphorus addition also decreased phenol oxidase absolute activity by 30% and peroxidase absolute activity by 29%.

Conclusions

These results suggest a strong P shortage for microorganisms and that P addition could decline microbial productions of enzymes in phosphorus-poor tropical forests. Results from this study emphasize again the important role of available P in tropical forests.

Keywords

Enzyme activity Phosphorus addition Phosphorus availability Phosphorus limitation Tropical forest 

Notes

Acknowledgments

We wish to thank Shaoming Cai and Yongxing Li for their assistance in field work. We also thank Xiaoping Pan and Xiaoying You for their help in laboratory work.

Funding information

This study was funded by the National Natural Science Foundation of China (No. 41731176, 41473112), the National Basic Research Program of China (2014CB954400), and Youth Innovation Promotion Association CAS (No. 2015287).

Supplementary material

11368_2019_2450_MOESM1_ESM.docx (34 kb)
ESM 1 (DOCX 34 kb)

References

  1. Aber J, McDowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I (1998) Nitrogen saturation in temperate forest ecosystems - hypotheses revisited. Bioscience 48:921–934CrossRefGoogle Scholar
  2. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944CrossRefGoogle Scholar
  3. Allison VJ, Condron LM, Peltzer DA, Richardson SJ, Turner BL (2007) Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand. Soil Biol Biochem 39:1770–1781CrossRefGoogle Scholar
  4. Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J Vis Exp (81):50961.  https://doi.org/10.3791/50961
  5. Burns R (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427CrossRefGoogle Scholar
  6. Camenzind T, Haettenschwiler S, Treseder KK, Lehmann A, Rillig MC (2018) Nutrient limitation of soil microbial processes in tropical forests. Ecol Monogr 88:4–21CrossRefGoogle Scholar
  7. Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365CrossRefGoogle Scholar
  8. Chen H, Dong S, Liu L, Ma C, Zhang T, Zhu X, Mo J (2013) Effects of experimental nitrogen and phosphorus addition on litter decomposition in an old-growth tropical forest. PLoS One 8:e84101.  https://doi.org/10.1371/journal.pone.0084101 CrossRefGoogle Scholar
  9. Chrost RJ (1991) Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. In: Chrost RJ (ed) . Springer-Verlag, New YorkCrossRefGoogle Scholar
  10. Cleveland CC, Townsend AR, Schmidt SK (2002) Phosphorus limitation of microbial processes in moist tropical forests: evidence from short-term laboratory incubations and field studies. Ecosystems 5:0680–0691CrossRefGoogle Scholar
  11. Cusack DF, Macy J, McDowell WH (2016) Nitrogen additions mobilize soil base cations in two tropical forests. Biogeochemistry 128:67–88CrossRefGoogle Scholar
  12. Deng Q, Hui D, Dennis S, Reddy KC (2017) Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: a meta-analysis. Glob Ecol Biogeogr 26:713–728CrossRefGoogle Scholar
  13. Dick RP, Burns RG (2011) A brief history of soil enzymology research. In: Dick RP (ed) Methods of soil enzymology, vol 9. Soil Science Society of America Book Series. pp 1–34. doi: https://doi.org/10.2136/sssabookser9.c1
  14. Dong WY, Zhang XY, Liu XY, Fu XL, Chen FS, Wang HM, Sun XM, Wen XF (2015) Responses of soil microbial communities and enzyme activities to nitrogen and phosphorus additions in Chinese fir plantations of subtropical China. Biogeosciences 12:5537–5546CrossRefGoogle Scholar
  15. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142CrossRefGoogle Scholar
  16. Fang YT, Gundersen P, Mo JM, Zhu WX (2008) Input and output of dissolved organic and inorganic nitrogen in subtropical forests of South China under high air pollution. Biogeosciences 5:339–352CrossRefGoogle Scholar
  17. Fanin N, Haettenschwiler S, Schimann H, Fromin N (2015) Interactive effects of C, N and P fertilization on soil microbial community structure and function in an Amazonian rain forest. Funct Ecol 29:140–150CrossRefGoogle Scholar
  18. Fog K, Aring RE (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63:433–462CrossRefGoogle Scholar
  19. Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos Trans R Soc Lond Ser B Biol Sci 368(1621):2013164.  https://doi.org/10.1098/rstb.2013.0164 Google Scholar
  20. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892CrossRefGoogle Scholar
  21. Gurmesa GA, Lu X, Gundersen P, Mao Q, Zhou K, Fang Y, Mo J (2016) High retention of (15) N-labeled nitrogen deposition in a nitrogen saturated old-growth tropical forest. Glob Chang Biol 22:3608–3620CrossRefGoogle Scholar
  22. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862CrossRefGoogle Scholar
  23. Hassett JE, Zak DR (2005) Aspen harvest intensity decreases microbial biomass, extracellular enzyme activity, and soil nitrogen cycling. Soil Sci Soc Am J 69:227–235CrossRefGoogle Scholar
  24. Holdridge LR (1967) Life zone ecology. Tropical Science Center, San Jose, Costa RicaGoogle Scholar
  25. Huang Z, Fan Z (1982) The climate of Dinghushan. In: Tropical and subtropical forest ecosystem, Vol 1, pp 11–23 Science Press, Beijing (in Chinese with English abstract)Google Scholar
  26. Jenkinson D (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7CrossRefGoogle Scholar
  27. Kaiser K, Guggenberger G, Haumaier L, Zech W (2001) Seasonal variations in the chemical composition of dissolved organic matter in organic forest floor layer leachates of old-growth Scots pine (Pinus sylvestris L.) and European beech (Fagus sylvatica L.) stands in northeastern Bavaria, Germany. Biogeochemistry 55:103–143CrossRefGoogle Scholar
  28. Koch AL (1985) The macroeconomics of bacterial growth. In: Fletcher M, Floodgate GD (eds) Bacteria in their natural environments. Academic Press, London, pp 1–42Google Scholar
  29. Li J, Li Z, Wang F, Zou B, Chen Y, Zhao J, Mo Q, Li Y, Li X, Xia H (2015) Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol Fertil Soils 51:207–215CrossRefGoogle Scholar
  30. Liu G, Jiang N, Le Z (1996) Soil physical and chemical analysis and description of soil profiles. Stands Press of China, Beijing (in Chinese) Google Scholar
  31. Liu L, Gundersen P, Zhang T, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38CrossRefGoogle Scholar
  32. Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459–462CrossRefGoogle Scholar
  33. Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704CrossRefGoogle Scholar
  34. Matson PA, McDowell WH, Townsend AR, Vitousek PM (1999) The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46:67–83Google Scholar
  35. McDowell WH, Likens GE (1988) Origin, composition, and flux of dissolved organic carbon in the Hubbard Brook valley. Ecol Monogr 58:177–195CrossRefGoogle Scholar
  36. Mo J, Brown S, Peng S, Kong G (2003) Nitrogen availability in disturbed, rehabilitated and mature forests of tropical China. For Ecol Manag 175:573–583CrossRefGoogle Scholar
  37. Mori T, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hardjono A, Ohta S (2015) Phosphorus addition reduced microbial respiration during the decomposition of Acacia mangium litter in South Sumatra, Indonesia. Tropics 24:113–118CrossRefGoogle Scholar
  38. Mori T, Imai N, Yokoyama D, Kitayama K (2018a) Effects of nitrogen and phosphorus fertilization on the ratio of activities of carbon-acquiring to nitrogen-acquiring enzymes in a primary lowland tropical rainforest in Borneo, Malaysia. Soil Sci Plant Nutr 64:554–557CrossRefGoogle Scholar
  39. Mori T, Lu X, Aoyagi R, Mo J, Ostertag R (2018b) Reconsidering the phosphorus limitation of soil microbial activity in tropical forests. Funct Ecol 32:1145–1154CrossRefGoogle Scholar
  40. Nannipieri P, Trasar-Cepeda C, Dick RP (2017) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19CrossRefGoogle Scholar
  41. Nottingham AT, Hicks LC, Ccahuana AJQ, Salinas N, Bååth E, Meir P (2017) Nutrient limitations to bacterial and fungal growth during cellulose decomposition in tropical forest soils. Biol Fertil Soils 54:219–228CrossRefGoogle Scholar
  42. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190CrossRefGoogle Scholar
  43. Quiquampoix H, Abadie J, Baron MH, Leprince F, Matumoto-Pintro PT, Ratcliffe RG, Staunton S (1995) Mechanisms and consequences of protein adsorption on soil mineral surfaces. In: proteins at interfaces II. ACS Symp Ser:321–333.  https://doi.org/10.1021/bk-1995-0602.ch023
  44. Raiesi F, Beheshti A (2014) Soil specific enzyme activity shows more clearly soil responses to paddy rice cultivation than absolute enzyme activity in primary forests of northwest Iran. Appl Soil Ecol 75:63–70CrossRefGoogle Scholar
  45. Rojo M, Carcedo S, Mateos M (1990) Distribution and characterization of phosphatase and organic phosphorus in soil fractions. Soil Biol Biochem 22(2):169–174CrossRefGoogle Scholar
  46. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  47. Shen C, Liu D, Peng S, Sun Y (1999) 14C measurement of forest soils in Dinghushan Biosphere Reserve. Sci Bull 44:251–256CrossRefGoogle Scholar
  48. Sinsabaugh RL (1994) Enzymatic analysis of microbial pattern and process. Biol Fertil Soils 17:69–74CrossRefGoogle Scholar
  49. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  50. Sinsabaugh RL, Shah JJF (2012) Ecoenzymatic stoichiometry and ecological theory. In: Futuyma DJ (ed) Annual review of ecology, evolution, and systematics, Vol 43. pp 313–343. doi: https://doi.org/10.1146/annurev-ecolsys-071112-124414, 43
  51. Sinsabaugh RL, Follstad Shah JJ, Hill BH, Elonen CM (2011) Ecoenzymatic stoichiometry of stream sediments with comparison to terrestrial soils. Biogeochemistry 111:455–467CrossRefGoogle Scholar
  52. Skujiņš J, Burns RG (1976) Extracellular enzymes in soil. CRC Crit Rev Microbiol 4:383–421CrossRefGoogle Scholar
  53. Steinweg JM, Dukes JS, Wallenstein MD (2012) Modeling the effects of temperature and moisture on soil enzyme activity: linking laboratory assays to continuous field data. Soil Biol Biochem 55:85–92CrossRefGoogle Scholar
  54. Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954CrossRefGoogle Scholar
  55. Turner BL, Romero TE (2010) Stability of hydrolytic enzyme activity and microbial phosphorus during storage of tropical rain forest soils. Soil Biol Biochem 42:459–465CrossRefGoogle Scholar
  56. Turner BL, Wright SJ (2014) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117:115–130CrossRefGoogle Scholar
  57. Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370CrossRefGoogle Scholar
  58. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  59. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea-how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  60. Vitousek PM et al (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750Google Scholar
  61. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15CrossRefGoogle Scholar
  62. Wang C, Lu X, Mori T, Mao Q, Zhou K, Zhou G, Nie Y, Mo J (2018) Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest. Soil Biol Biochem 121:103–112CrossRefGoogle Scholar
  63. Wang S, Mori T, Mo J, Zhang W (2019) The responses of carbon- and nitrogen-acquiring enzymes to nitrogen and phosphorus additions in two plantations in southern China. J Forest Res.  https://doi.org/10.1007/s11676-019-00905-0
  64. Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol Rev Camb Philos Soc 67:321–358CrossRefGoogle Scholar
  65. Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113CrossRefGoogle Scholar
  66. Whittinghill KA, Currie WS, Zak DR, Burton AJ, Pregitzer KS (2012) Anthropogenic N deposition increases soil C storage by decreasing the extent of litter decay: analysis of field observations with an ecosystem model. Ecosystems 15:450–461CrossRefGoogle Scholar
  67. Xiao W, Chen X, Jing X, Zhu B (2018) A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biol Biochem 123:21–32CrossRefGoogle Scholar
  68. Yao Q, Li Z, Song Y, Wright SJ, Guo X, Tringe SG, Tfaily MM, Paša-Tolić L, Hazen TC, Turner BL, Mayes MA, Pan C (2018) Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. Nature Ecol Evol 2:499–509CrossRefGoogle Scholar
  69. Yokoyama D, Imai N, Kitayama K (2017) Effects of nitrogen and phosphorus fertilization on the activities of four different classes of fine-root and soil phosphatases in Bornean tropical rain forests. Plant Soil 416:463–476CrossRefGoogle Scholar
  70. Zhang W, Mo J, Yu G, Fang Y, Li D, Lu X, Wang H (2008) Emissions of nitrous oxide from three tropical forests in Southern China in response to simulated nitrogen deposition. Plant Soil 306:221–236CrossRefGoogle Scholar
  71. Zheng M, Huang J, Chen H, Wang H, Mo J (2015) Responses of soil acid phosphatase and beta-glucosidase to nitrogen and phosphorus addition in two subtropical forests in southern China. Eur J Soil Biol 68:77–84CrossRefGoogle Scholar
  72. Zheng M, Zhang T, Liu L, Zhu W, Zhang W, Mo J (2016) Effects of nitrogen and phosphorus additions on nitrous oxide emission in a nitrogen-rich and two nitrogen-limited tropical forests. Biogeosciences 13:3503–3517CrossRefGoogle Scholar
  73. Zhou Z, Wang C, Jin Y (2017) Stoichiometric responses of soil microflora to nutrient additions for two temperate forest soils. Biol Fertil Soils 53:397–406CrossRefGoogle Scholar
  74. Zhou K, Lu X, Mori T, Mao Q, Wang C, Zheng M, Mo H, Hou E, Mo J (2018) Effects of long-term nitrogen deposition on phosphorus leaching dynamics in a mature tropical forest. Biogeochemistry 138:215–224CrossRefGoogle Scholar
  75. Zhu F, Yoh M, Gilliam FS, Lu X, Mo J (2013) Nutrient limitation in three lowland tropical forests in southern China receiving high nitrogen deposition: insights from fine root responses to nutrient additions. PLoS One 8:e82661.  https://doi.org/10.1371/journal.pone.0082661 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Cong Wang
    • 1
    • 2
  • Taiki Mori
    • 1
    • 3
  • Qinggong Mao
    • 1
  • Kaijun Zhou
    • 4
  • Zhuohang Wang
    • 1
    • 2
  • Yongqun Zhang
    • 1
    • 2
  • Hui Mo
    • 1
  • Xiankai Lu
    • 1
    Email author
  • Jiangming Mo
    • 1
  1. 1.Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems and Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Forest Site EnvironmentForestry and Forest Products Research InstituteTsukubaJapan
  4. 4.Institute of Agricultural Resources and EnvironmentGuangdong Academy of Agricultural SciencesGuangzhouChina

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