Time-Dependent Hormetic Response of Soil Alkaline Phosphatase Induced by Cd and the Association with Bacterial Community Composition

  • Jiangang HanEmail author
  • Shengyan Wang
  • Diwu Fan
  • Yanhui Guo
  • Chenglei Liu
  • Yongli Zhu
Soil Microbiology


Hormetic dose-response that involved Cd in soils is increasingly paid attentions for risk assessment of Cd toxicity, but insufficient studies were conducted to define the temporary modification of soil enzyme and the potential microbial responses. The present study chooses soil alkaline phosphatase (ALP) as endpoint to uncover the time-dependent hormetic responses to low doses of Cd and its association with bacterial community composition. The results showed that addition of 0.01–3.0 mg kg−1 Cd significantly increased ALP’s activities with maximum stimulatory magnitude of 11.4–27.2%, indicating a typical hormesis. The response started at 12 h after Cd addition and maintained about 24 h. This demonstrated that the hormetic response is time-dependent and transient. Changes of soil bacterial community composition showed that, at 6 h, relative abundances (RAs) of Proteobacteria and Firmicutes at phylum and Pontibacter, Bacillaceae-Bacillus, Bacillaceae1-Bacillus, and Paenisporosarcina at genus significantly correlated with ALP’s activities at 12–36 h (P < 0.05). This suggests that soil bacteria likely showed an earlier response to Cd and potentially contributes to the subsequent soil enzyme’s hormesis. In addition, it was found that Gram-negative bacteria other than Gram-positive bacteria are prone to exhibiting a hormetic response under Cd stress. Our findings provide much insight into ecotoxicological risk assessment for soil Cd pollution.


Hormesis Cadmium Alkaline phosphatase Bacterial community composition 



We thank all the supporters of this article for their constructive comments.

Funding Information

This study was supported by the financial support of National Natural Science Foundation of China (No. 41375149, No. 41471191), Qing Lan Project of Jiangsu Province (Qinglan2016-15), and Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).


  1. 1.
    Calabrese EJ, Baldwin LA (2003) Toxicology rethinks its central belief - Hormesis demands a reappraisal of the way risks are assessed. Nature 421(6924):691–692 PubMed PMID: WOS:000180938000017CrossRefGoogle Scholar
  2. 2.
    Calabrese EJ, Baldwin LA (2002) Defining hormesis. Hum Exp Toxicol 21(2):91–97 PubMed PMID: WOS:000176098800009CrossRefGoogle Scholar
  3. 3.
    Kaiser J (2003) Hormesis - Sipping from a poisoned chalice. Science 302(5644):376 −+. PubMed PMID: WOS:000185963200008CrossRefGoogle Scholar
  4. 4.
    Kastury F, Juhasz A, Beckmann S, Manefield M (2015) Ecotoxicity of neutral red (dye) and its environmental applications. Ecotoxicol Environ Saf 122:186–192 PubMed PMID: WOS:000364263000024CrossRefGoogle Scholar
  5. 5.
    Jin M, Liu X, Wu L, Liu M (2015) An improved assimilation method with stress factors incorporated in the WOFOST model for the efficient assessment of heavy metal stress levels in rice. Int J Appl Earth Obs Geoinf 41:118–129 PubMed PMID: WOS:000356996500011CrossRefGoogle Scholar
  6. 6.
    Chen Y-Y, Hu C-Y, Xiao J-X (2014) Effects of arbuscular mycorrhizal inoculation on the growth, zinc distribution and photosynthesis of two citrus cultivars grown in low-zinc soil. Trees-Struct Funct 28(5):1427–1436 PubMed PMID: WOS:000342420600015CrossRefGoogle Scholar
  7. 7.
    Jaiswal AK, Frenkel O, Elad Y, Lew B, Graber ER (2015) Non-monotonic influence of biochar dose on bean seedling growth and susceptibility to Rhizoctonia solani: the "Shifted R-max-Effect". Plant Soil 395(1–2):125–140 PubMed PMID: WOS:000361757400010CrossRefGoogle Scholar
  8. 8.
    Calabrese EJ (2009) Getting the dose-response wrong: why hormesis became marginalized and the threshold model accepted. Arch Toxicol 83(3):227–247 PubMed PMID: WOS:000263976700004CrossRefGoogle Scholar
  9. 9.
    Wang Q, Gu M, Ma X, Zhang H, Wang Y, Cui J et al (2015) Model optimization of cadmium and accumulation in switchgrass (Panicum virgatum L.): potential use for ecological phytoremediation in Cd-contaminated soils. Environmental Science And Pollution Research 22(21):16758–16771 PubMed PMID: WOS:000363964700047CrossRefGoogle Scholar
  10. 10.
    Jia L, Liu Z, Chen W, Ye Y, Yu S, He X (2015) Hormesis Effects Induced by Cadmium on Growth and Photosynthetic Performance in a Hyperaccumulator, Lonicera japonica Thunb. J Plant Growth Regul 34(1):13–21 PubMed PMID: WOS:000351414800002CrossRefGoogle Scholar
  11. 11.
    Liu Z, Chen W, He X, Jia L, Huang Y, Zhang Y et al (2013) Cadmium-Induced Physiological Response in Lonicera japonica Thunb. Clean-Soil Air Water 41(5):478–484 PubMed PMID: WOS:000317866600011CrossRefGoogle Scholar
  12. 13.
    Wang C, Rong H, Liu H, Wang X, Gao Y, Deng R et al (2018) Detoxification mechanisms, defense responses, and toxicity threshold in the earthworm Eisenia foetida exposed to ciprofloxacin-polluted soils. Science Of the Total Environment 612:442–449 PubMed PMID: WOS:000413313700047CrossRefGoogle Scholar
  13. 13.
    Lefcort H, Freedman Z, House S, Pendleton M (2008) Hormetic effects of heavy metals in aquatic snails: Is a little bit of pollution good? Ecohealth 5(1):10–17 PubMed PMID: WOS:000254756600003CrossRefGoogle Scholar
  14. 14.
    Langdon KA, McLaughlin MJ, Kirby JK, Merrington G (2014) The effect of soil properties on the toxicity of silver to the soil nitrification process. Environ Toxicol Chem 33(5):1170–1178 PubMed PMID: WOS:000334488700030CrossRefGoogle Scholar
  15. 15.
    Gao Y, Mao L, Miao C-y, Zhou P, Cao J-j, Zhi Y-e et al (2010) Spatial characteristics of soil enzyme activities and microbial community structure under different land uses in Chongming Island, China: Geostatistical modelling and PCR-RAPD method. Sci Total Environ 408(16):3251–3260 PubMed PMID: WOS:000279773200025CrossRefGoogle Scholar
  16. 16.
    Ciarkowska K, Gargiulo L, Mele G (2016) Natural restoration of soils on mine heaps with similar technogenic parent material: A case study of long-term soil evolution in Silesian-Krakow Upland Poland. Geoderma 261:141–150 PubMed PMID: WOS:000362130900014CrossRefGoogle Scholar
  17. 17.
    Fang L, Liu Y, Tian H, Chen H, Wang Y, Huang M (2017) Proper land use for heavy metal-polluted soil based on enzyme activity analysis around a Pb-Zn mine in Feng County, China. Environ Sci Pollut Res 24(36):28152–28164 PubMed PMID: WOS:000417874400050CrossRefGoogle Scholar
  18. 18.
    Zhang W, Zhang M, An S, Lin K, Li H, Cui C et al (2012) The combined effect of decabromodiphenyl ether (BDE-209) and copper (Cu) on soil enzyme activities and microbial community structure. Environ Toxicol Pharmacol 34(2):358–369 PubMed PMID: WOS:000313155600029CrossRefGoogle Scholar
  19. 19.
    Guo X-L, Gu J, Chen Z-X, Gao H, Qin Q-J, Sun W et al (2012) Effects of heavy metals pollution on soil microbial communities metabolism and soil enzyme activities in coal mining area of Tongchuan, Shaanxi Province of Northwest China. Chin J Appl Ecol 23(3):798–806Google Scholar
  20. 20.
    Pan J, Yu L (2011) Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecol Eng 37(11):1889–1894 PubMed PMID: WOS:000295303500033CrossRefGoogle Scholar
  21. 21.
    Meng Q-F, Yang J-S, Yao R-J, Yu S-P, Zhang C-Y, Ji R-L (2012) Effects of single and complex heavy metal pollution on soil enzyme activity. Ecol Environ Sci. 21(3):545–550Google Scholar
  22. 22.
    Tan X, Liu Y, Yan K, Wang Z, Lu G, He Y et al (2017) Differences in the response of soil dehydrogenase activity to Cd contamination are determined by the different substrates used for its determination. Chemosphere 169:324–332 PubMed PMID: WOS:000393003300039CrossRefGoogle Scholar
  23. 23.
    Feng D, Teng Y, Wang J, Wu J (2016) The Combined Effect of Cu, Zn and Pb on Enzyme Activities in Soil from the Vicinity of a Wellhead Protection Area. Soil & Sediment Contamination 25(3):279–295 PubMed PMID: WOS:000375850900004CrossRefGoogle Scholar
  24. 24.
    Agathokleous E, Mouzaki-Paxinou A-C, Saitanis CJ, Paoletti E, Manning WJ (2016) The first toxicological study of the antiozonant and research tool ethylene diurea (EDU) using a Lemna minor L. bioassay: Hints to its mode of action. Environ Pollut 213:996–1006 PubMed PMID: WOS:000377921800106CrossRefGoogle Scholar
  25. 25.
    Belz RG, Duke SO (2014) Herbicides and plant hormesis. Pest Management Science 70(5):698–707 PubMed PMID: WOS:000334285200003CrossRefGoogle Scholar
  26. 26.
    Chen Q, Ni J (2012) Ammonium removal by Agrobacterium sp LAD9 capable of heterotrophic nitrification-aerobic denitrification. J Biosci Bioeng 113(5):619–623 PubMed PMID: WOS:000304635100014CrossRefGoogle Scholar
  27. 27.
    Noumsi CJ, Pourhassan N, Darnajoux R, Deicke M, Wichard T, Burrus V et al (2016) Effect of organic matter on nitrogenase metal cofactors homeostasis in Azotobacter vinelandii under diazotrophic conditions. Environ Microbiol Rep 8(1):76–84 PubMed PMID: WOS:000371481100011CrossRefGoogle Scholar
  28. 28.
    Boldt-Burisch K, Naeth MA (2017) Heterogeneous soil conditions influence fungal alkaline phosphatase activity in roots of Lotus corniculatus. Appl Soil Ecol 116:55–63 PubMed PMID: WOS:000402492200006CrossRefGoogle Scholar
  29. 29.
    Vlahovic M, Lazarevic J, Peric-Mataruga V, Ilijin L, Mrdakovic M (2009) Plastic responses of larval mass and alkaline phosphatase to cadmium in the gypsy moth larvae. Ecotoxicol Environ Saf 72(4):1148–1155 PubMed PMID: WOS:000265767900020CrossRefGoogle Scholar
  30. 30.
    Deng JQ, Liu BQ, Wang Y, Liu W, Cai JF, Long R et al (2016) Application of second-generation high-throughput sequencing based on MiSeq sequencer to the study of diatom species diversity of water samples. Oxid Commun 39(2):1385–1391 PubMed PMID: WOS:000381320400013. English Google Scholar
  31. 31.
    Fordyce SL, Mogensen HS, Borsting C, Lagace RE, Chang CW, Rajagopalan N et al (2015) Second-generation sequencing of forensic STRs using the Ion Torrent (TM) HID STR 10-plex and the Ion PGM (TM). Forensic Sci Int-Genet 14:132–140 PubMed PMID: WOS:000345612700020. English CrossRefGoogle Scholar
  32. 32.
    Mohd-Yusoff NF, Ruperao P, Tomoyoshi NE, Edwards D, Gresshoff PM, Biswas B et al (2015) Scanning the Effects of Ethyl Methanesulfonate on the Whole Genome of Lotus japonicus Using Second-Generation Sequencing Analysis. G3-Genes Genomes Genet 5(4):559–567 PubMed PMID: WOS:000352293000009. English Google Scholar
  33. 33.
    Gao ZG, Zhang LQ (2006) Multi-seasonal spectral characteristics analysis of coastal salt marsh vegetation in Shanghai, China. Estuar Coast Shelf Sci 69(1–2):217–224 PubMed PMID: WOS:000239855300019CrossRefGoogle Scholar
  34. 34.
    Fan D, Han J, Chen Y, Zhu Y, Li P (2018) Hormetic effects of Cd on alkaline phosphatase in soils across particle-size fractions in a typical coastal wetland. Science Of the Total Environment 613:792–797 PubMed PMID: WOS:000414160500082CrossRefGoogle Scholar
  35. 35.
    Calabrese EJ (2012) Hormesis: improving predictions in the low-dose zone. Exs 101:551–564 PubMed PMID: MEDLINE:22945582Google Scholar
  36. 36.
    Ardestani MM, van Gestel CAM (2013) Toxicodynamics of copper and cadmium in Folsomia candida exposed to simulated soil solutions. Environ Toxicol Chem 32(12):2746–2754 PubMed PMID: WOS:000326916800012CrossRefGoogle Scholar
  37. 37.
    Zhang Y, Shen G, Yu Y, Zhu H (2009) The hormetic effect of cadmium on the activity of antioxidant enzymes in the earthworm Eisenia fetida. Environ Pollut 157(11):3064–3068 PubMed PMID: WOS:000270119900020CrossRefGoogle Scholar
  38. 38.
    Calabrese EJ, Iavicoli I, Calabrese V (2012) Hormesis: why it is important to biogerontologists. Biogerontology 13(3):215–235 PubMed PMID: WOS:000304555500001CrossRefGoogle Scholar
  39. 39.
    Jia L, He X, Chen W, Liu Z, Huang Y, Yu S (2013) Hormesis phenomena under Cd stress in a hyperaccumulator-Lonicera japonica Thunb. Ecotoxicology 22(3):476–485 PubMed PMID: WOS:000316281300005CrossRefGoogle Scholar
  40. 40.
    Liu W, Zhou Q, Li P, Gao H, Han YP, Li XJ et al (2009) DNA mismatch repair related gene expression as potential biomarkers to assess cadmium exposure in Arabidopsis seedlings. J Hazard Mater 167(1–3):1007–1013 PubMed PMID: WOS:000267267000146CrossRefGoogle Scholar
  41. 41.
    Lin Y, Huang J-j, Dahms H-U, Zhen J-j, Ying X-p (2017) Cell damage and apoptosis in the hepatopancreas of Eriocheir sinensis induced by cadmium. Aquat Toxicol 190:190–198 PubMed PMID: WOS:000408783600022CrossRefGoogle Scholar
  42. 42.
    Chen X, Wang X, Gu X, Jiang Y, Ji R (2017) Oxidative stress responses and insights into the sensitivity of the earthworms Metaphire guillelmi and Eisenia fetida to soil cadmium. Sci Total Environ 574:300–306 PubMed PMID: WOS:000389090100030CrossRefGoogle Scholar
  43. 43.
    Mushak P (2016) Temporal stability of chemical hormesis (CH): Is CH just a temporary stop on the road to thresholds and toxic responses? Science Of the Total Environment 569:1446–1456 PubMed PMID: WOS:000382269000139CrossRefGoogle Scholar
  44. 44.
    Luo L, Gu JD (2016) Influence of Macrofaunal Burrows on Extracellular Enzyme Activity and Microbial Abundance in Subtropical Mangrove Sediment. Microb Ecol 76 (1): 92-101 PubMed PMID: WOS:000251119900021Google Scholar
  45. 45.
    Bani A, Borruso L, Fornasier F, Pioli S, Wellstein C, Brusetti L (2018) Microbial Decomposer Dynamics: Diversity and Functionality Investigated through a Transplantation Experiment in Boreal Forests. Microb Ecol 76 (4): 1030-1040 PubMed PMID: WOS:000260123900130Google Scholar
  46. 46.
    Wang T, Wang D, Lin Z, An Q, Yin C, Huang Q (2016) Prediction of mixture toxicity from the hormesis of a single chemical: A case study of combinations of antibiotics and quorum-sensing inhibitors with gram-negative bacteria. Chemosphere 150:159–167 PubMed PMID: WOS:000372765100021CrossRefGoogle Scholar
  47. 47.
    Deng Z, Lin Z, Zou X, Yao Z, Tian D, Wang D et al (2012) Model of Hormesis and Its Toxicity Mechanism Based on Quorum Sensing: A Case Study on the Toxicity of Sulfonamides to Photobacterium phosphoreum. Environ Sci Technol 46(14):7746–7754 PubMed PMID: WOS:000306441000042CrossRefGoogle Scholar
  48. 48.
    Mounaouer B, Nesrine A, Abdennaceur H (2014) Identification and characterization of heavy metal-resistant bacteria selected from different polluted sources. Desalin Water Treat 52(37–39):7037–7052 PubMed PMID: WOS:000345001300021CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Jiangang Han
    • 1
    • 2
    Email author
  • Shengyan Wang
    • 1
  • Diwu Fan
    • 1
  • Yanhui Guo
    • 1
  • Chenglei Liu
    • 1
  • Yongli Zhu
    • 1
  1. 1.College of Biology and the EnvironmentNanjing Forestry UniversityNanjingPeople’s Republic of China
  2. 2.Collaborative Innovation Center of Sustainable Forestry in Southern China of Jiangsu ProvinceNanjing Forestry UniversityNanjingPeople’s Republic of China

Personalised recommendations