Changes in soil microbial biomass C, ATP and microbial ATP concentrations due to increasing soil Cd levels in Chinese paddy soils growing rice (Oryza sativa)

  • Gaoyang Qiu
  • Min Zhu
  • Jun Meng
  • Yu Luo
  • Hongjie Di
  • Jianming Xu
  • Philip C. Brookes
Regular Paper



The mean biomass ATP concentration in aerobic soils is around 10–11 μmol ATP g−1 biomass C, within a fairly narrow range. It is much lower in short-term incubated laboratory waterlogged soils. However, the biomass ATP concentration in waterlogged paddy soils under field conditions remains unknown. This is investigated.


Soil microbial biomass C (biomass C), ATP, biomass ATP and heavy metal (Cd, Zn, and Cu) concentrations in soil and rice were measured in a Chinese paddy soil growing rice. Soils and plants were analyzed at day 0, 30, 75 and 90, over the 90 day growing period with inputs of inorganic fertilizer, or biochar and manure singly or in combination.


Both biomass C and ATP concentrations increased, range from 14.9–30.5% for microbial biomass C and 115.8–160.1% for ATP, from initial values until the end of the experiment following manure or biochar addition. An important result was that the biomass ATP concentration increased throughout the growth period. There were also significant negative correlations (p < 0.05) between total and available Cd and these three microbial parameters, despite the low levels of Cd. Over the same period, total plant Cd concentrations increased, and soil Cd decreased. This suggests that the rice acted as a bioaccumulator. The microbial biomass was then in a continually decreasingly toxic environment and responded rapidly by increasing its size.


These results demonstrate clear differences in microbial energy dynamics between aerobic and anaerobic microbial populations. Both ATP and biomass C are useful bioindicators of the effects of cadmium contamination on microbial processes in waterlogged soil.


Soil microbial biomass C Soil microbial biomass ATP Biomass ATP concentrations Waterlogged soil Soil cd concentrations 



Adenosine 5′-triphosphate


Microbial biomass C


Cadmium; Zn: Zinc




2% manure


2% manure combined with 2% biochar


2% biochar


Mingzhusimiao rice variety


Jiaxing-33 rice variety



We gratefully acknowledge the helpful and positive criticism of two anonymous referees. This work was financially supported by the National Natural Science Foundation of China (41721001), the Science and Technology Program of Zhejiang Province (2018C03028) and the China Agriculture Research System. PCB also thanks the Chinese Government for the award of a Chinese Thousand Talents Fellowship.

Supplementary material

11104_2018_3899_MOESM1_ESM.doc (134 kb)
ESM 1 (DOC 133 kb)


  1. Atkinson CJ, Fitzgerald JD, Hipps NA (2010) Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. Plant Soil 337:1–18CrossRefGoogle Scholar
  2. Beattie RE, Henke W, Campa MF, Hazen TC, Rex McAliley L, Campbell JH (2018) Variation in microbial community structure correlates with heavy-metal contamination in soils decades after mining ceased. Soil Biol Biochem 126:57–63CrossRefGoogle Scholar
  3. Borjesson G, Menichetti L, Thornton B, Campbell CD, Katterer T (2016) Seasonal dynamics of the soil microbial community: assimilation of old and young carbon sources in a long-term field experiment as revealed by natural 13C abundance. Eur J Soil Sci 67:79–89CrossRefGoogle Scholar
  4. Brock Biol Microorg (2014) 13h Edition (Michael T. Madigan T., John M. Martinko, , David A. Stahl, Thomas Brock. (Eds). Benjamin CumminsGoogle Scholar
  5. Brookes PC, YanFeng C, Chen C, Qiu G, Luo Yu XJ (2017) Is the rate of mineralization of soil organic carbon under microbiological control? Soil Biol Biochem 243:510–518Google Scholar
  6. Chander K, Brookes PC (1991) Microbial biomass dynamics during the decomposition of glucose and maize in metal-contaminated and non-contaminated soils. Soil Biol Biochem 23:917–925Google Scholar
  7. Dahlin S, Witter E, Mårtensson A, Turner A, Bååth E (1997) Where's the limit? Changes in the microbiological properties of agricultural soils at low levels of metal contamination. Soil Biol Biochem 29:1405–1415CrossRefGoogle Scholar
  8. Ding Y, Liu Y, Liu S, Li Z, Tan X, Huang X, Zeng G, Zhou L, Zheng B (2016) Biochar to improve soil fertility. A review. Agron Sustain Dev 36:1–18CrossRefGoogle Scholar
  9. Idrees M, Batool S, Kalsoom T, Yasmeen S, Kalsoom A, Raina S, Zhuang Q, Kong J (2018) Animal manure-derived biochars produced via fast pyrolysis for the removal of divalent copper from aqueous media. J Enciron Manage 213:109–118Google Scholar
  10. Inubushi K, Brookes PC, Jenkinson DS (1989) Adenosine 5′-triphosphate and adenylate energy charge in waterlogged soil. Soil Biol Biochem 21:733–739CrossRefGoogle Scholar
  11. Inubushi K, Brookes PC, Jenkinson DS (1991) Soil microbial biomass C, N and ninhydrin-N in aerobic and anaerobic soils measured by the fumigation-extraction method. Soil Biol Biochem 23:737–741CrossRefGoogle Scholar
  12. Jenkinson DS (1977) The soil microbial biomass. New Zealand Soil News 25:213–218Google Scholar
  13. Jenkinson DS, Ladd JN (1981) Microbial biomass in soil, measurement and turn over. In: Paul EA, Ladd JN (eds) Soil Biochem. Marcel Dekker press, New York, pp 415–471Google Scholar
  14. Jiang H, Han XZ, Zou WX, Hao XX, Zhang B (2018) Seasonal and long-term changes in soil physical properties and organic carbon fractions as affected by manure application rates in the Mollisol region of Northeast China. Agric Ecosyst Environ 268:133–143CrossRefGoogle Scholar
  15. Jin XX, An TT, Gall AR, Li SY, Filley T, Wang JK (2018) Enhanced conversion of newly-added maize straw to soil microbial biomass C under plastic film mulching and organic manure management. Geoderma 313:154–162CrossRefGoogle Scholar
  16. Li XQ, Meng DL, Li J, Yin HQ, Liu HW, Liu XD, Cheng C, Xiao YH, Liu ZH, Yan ML (2017) Response of soil microbial communities and microbial interactions to long-term heavy metal contamination. Environ Pollut 231:908–917CrossRefGoogle Scholar
  17. Liu M, Hu F, Chen X, Huang Q, Jiao J, Zhang B, Li H (2009) Organic amendments with reduced chemical fertilizer promote soil microbial development and nutrient availability in a subtropical paddy field: the influence of quantity, type and application time of organic amendments. Appl Soil Ecol 42:166–175CrossRefGoogle Scholar
  18. Luo Y, Durenkamp M, De Nobili M, Lin QM, Devonshire BJ, Brookes PC (2012) Microbial biomass growth, following incorporation of biochars produced at 350 °C or 700 °C, in a silty-clay loam soil of high and low pH. Soil Biol Biochem 57:513–523CrossRefGoogle Scholar
  19. Mondini C, Contin L, Leita M, De Nobili M (2002) Response of microbial biomass to air-drying and rewetting in soils and compost. Geoderma 105:111–124CrossRefGoogle Scholar
  20. Phillips IR (1999) Copper, lead, cadmium and zinc sorption by waterlogged and air-dry soil. Soil Sediment Contam 8:343–364CrossRefGoogle Scholar
  21. Poucke RV, Ainsworth J, Maeseele M, Ok YS, Meers E, Tack FMG (2018) Chemical stabilization of cd-contaminated soil using biochar. Appl Geochem 88:122–130CrossRefGoogle Scholar
  22. Qiu GY, Chen Y, Luo Y, Xu JM, Brookes PC (2015) The microbial ATP concentration in aerobic and anaerobic Chinese soils. Soil Biol Biochem 92:38–40CrossRefGoogle Scholar
  23. Redmile GM, Brookes PC (2011) Evaluation of substitutes for paraquat in soil microbial ATP determinations using the trichloroacetic acid based reagent of Jenkinson and Oades (1979). Soil Biol Biochem 43:1098–1100CrossRefGoogle Scholar
  24. Renella G, Chaudri AM, Brookes PC (2002) Fresh additions of heavy metals do not model long-term effects on microbial biomass and activity. Soil Biol Biochem 34:121–124CrossRefGoogle Scholar
  25. Renella G, Mench M, Landi L, Nannipieri P (2005) Microbial activity and hydrolase synthesis in long-term cd-contaminated soils. Soil Biol Biochem 37:133–139CrossRefGoogle Scholar
  26. Song J, Shen Q, Wang L, Qiu G, Shi J, Xu J, Brookes LX (2018) Effects of cd, cu, Zn and their combined action on microbial biomass and bacterial community structure. Environ Pollut 243:510–518CrossRefGoogle Scholar
  27. Suksabye P, Pimthong A, Dhurakit P, Mekvichitsaeng P, Thiravetyan P (2016) Effect of biochars and microorganisms on cadmium accumulation in rice grains grown in cd-contaminated soil. Environ Sci Pollut Res 23:962–973CrossRefGoogle Scholar
  28. Wu B, Guo SH, Zhang LY, Li FM (2018) Risk forewarning model for rice grain cd pollution based on Bayes theory. Sci Total Environ 618:1343–1349CrossRefGoogle Scholar
  29. Yagüe MR, Domingo-Olive F, Dolores Bosch-Serra A, Maria Poch R, Boixadera J (2016) Dairy cattle manure effects on soil quality: porosity, earthworms, aggregates and soil orgainc carbon fractions. Land Degrad Dev 27:1753–1762CrossRefGoogle Scholar
  30. Yang YJ, Chen JM, Huang Q, Tang SQ, Wang JL, Hu PS, Shao GS (2018) Can liming reduce cadmium (cd) accumulation in rice (Oryza sativa) in slightly acidic soils? A contradictory dynamic equilibrium between cd uptake capacity of roots and cd immobilisation in soils. Chemosphere 193:547–556CrossRefGoogle Scholar
  31. Yin DX, Wang X, Peng B, Tan CY, Ma LQ (2017) Effect of biochar and Fe-biochar on cd and as mobility and transfer in soil-rice system. Chemosphere 186:928–937CrossRefGoogle Scholar
  32. Zhang C, Nie S, Liang J, Zeng GM, Wu HP, Hua SS, Liu JY, Yuan YJ, Xiao HB, Deng LJ, Xiang HY (2016) Effects of heavy metals and soil physicochemical properties on wetland soil microbial biomass and bacterial community structure. Sci Total Environ 557:785–790CrossRefGoogle Scholar
  33. Zheng R, Chen Z, Cai C, Tie B, Liu X, Reid BJ, Huang Q, Lei M, Sun G, Baltrėnaitė E (2015) Mitigating heavy metal accumulation into rice (Oryza sativa L.) using biochar amendment—a field experiment in Hunan, China. Environ Sci Pollut Res 22:11097–11108CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Gaoyang Qiu
    • 1
  • Min Zhu
    • 1
  • Jun Meng
    • 1
  • Yu Luo
    • 1
  • Hongjie Di
    • 1
  • Jianming Xu
    • 1
  • Philip C. Brookes
    • 1
  1. 1.Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang Provincial Key Laboratory of Agricultural Resources and EnvironmentZhejiang UniversityHangzhouPeople’s Republic of China

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