Skip to main content

Advertisement

Log in

Fate of heavy metals and bacterial community composition following biogas slurry application in a single rice cropping system

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Biogas slurry (BS) is widely used as a valuable fertilizer for crop production. However, little is known about the effects of long-term BS application on potential pollution risk of heavy metals and bacterial community in paddy field. This study aimed to determine the accumulation and rice plant uptake of heavy metals (Cd, Cr, Pb, Cu, and Zn), as well as soil bacterial community composition following repeated BS application in a single rice cropping system.

Materials and methods

In this study, four treatments were included in a long-term field experiment: CK, no fertilizers; MF, mineral fertilizers, 270 kg urea-N ha–1; and two application rates of BS (BS1, 270 kg N ha–1 and BS2, 540 kg N ha–1). The heavy metals (Cd, Cr, Pb, Cu, and Zn) in soils and rice plants were measured by an inductively coupled plasma mass spectrometer and the soil bacterial community composition was analyzed using Illumina MiSeq sequencing of the 16S rRNA.

Results and discussion

Soil Zn concentrations were significantly greater in the BS treatments than in the MF treatment. Biogas slurry application significantly increased the heavy metals concentrations in rice plants, compared to the CK treatment. The concentrations of Cd and Pb in grain, and Cu and Zn concentrations in straw were significantly increased by the BS2 treatment compared to the MF treatment, respectively. However, the Cd, Cr, Pb, Cu, and Zn concentrations in grain and soil were all within the safety limits after long-term BS application. Application of BS and of MF resulted in similar bacterial alpha-diversities, and both increased them compared to the CK treatment. Fertilization significantly enhanced the relative abundances of phyla Proteobacteria, Actinobacteria, and Myxococcota but reduced that of Planctomycetota compared to the CK. While, there were no significant differences in those phyla among fertilized treatments. The relative abundances of genera Thiobacillus and Ellin6067 was decreased by the BS2 treatment compared to the MF treatment. Redundancy analysis (RDA) showed that soil organic carbon, available phosphorus and available potassium were the main factors shaping soil bacterial community composition. Spearman’s correlation demonstrated that soil Cd concentration had stronger correlation with some bacterial genera of Bryobacter, Vicinamibacteraceae, and Ellin6067.

Conclusions

Overall, we conclude that BS application can be considered to substitute mineral fertilizers for rice production. However, the accumulation of heavy metals in paddy soil, especially for Zn, should be considered after long-term BS application.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abubaker J, Risberg K, Pell M (2012) Biogas residues as fertilisers – effects on wheat growth and soil microbial activities. Appl Energ 99:126–134

    CAS  Google Scholar 

  • Arbat G, Roselló A, Domingo Olivé F, Puig-Bargués J, González Llinàs E, Duran-Ros M, Pujol J, Ramírez de Cartagena F (2013) Soil water and nitrate distribution under drip irrigated corn receiving pig slurry. Agr Water Manage 120:11–22

    Google Scholar 

  • Bian B, Lin C, Lv L (2016) Health risk assessment of heavy metals in soil-plant system amended with biogas slurry in Taihu basin, China. Environ Sci Pollut Res 23:16955–16964

    Google Scholar 

  • Bian B, suo Wu H, Lv L, Fan Y, Lu H (2015) Health risk assessment of metals in food crops and related soils amended with biogas slurry in Taihu Basin: perspective from field experiment. Environ Sci Pollut Res 22:14358–14366

    CAS  Google Scholar 

  • Bian B, Wu H, Zhou L (2015b) Contamination and risk assessment of heavy metals in soils irrigated with biogas slurry: a case study of Taihu basin. Environ Monit Assess 187:155

    Google Scholar 

  • Bourceret A, Cebron A, Tisserant E, Poupin P, Bauda P, Beguiristain T, Leyval C (2016) The bacterial and fungal diversity of an aged PAH- and heavy metal-contaminated soil is affected by plant cover and edaphic parameters. Microb Ecol 71:711–724

    CAS  Google Scholar 

  • Breidenbach B, Blaser MB, Klose M, Conrad R (2016) Crop rotation of flooded rice with upland maize impacts the resident and active methanogenic microbial community. Environ Microbiol 18:2868–2885

    CAS  Google Scholar 

  • Cao Y, Wang J, Wu H, Yan S, Guo D, Wang G, Ma Y (2016) Soil chemical and microbial responses to biogas slurry amendment and its effect on Fusarium wilt suppression. Appl Soil Ecol 107:116–123

    Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  Google Scholar 

  • Chen J, He F, Zhang X, Sun X, Zheng J, Zheng J (2014) Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiol Ecol 87: 164-181

    Article  CAS  Google Scholar 

  • Chen D, Yuan L, Liu Y, Ji J, Hou H (2017a) Long-term application of manures plus chemical fertilizers sustained high rice yield and improved soil chemical and bacterial properties. Eur J Agron 90:34–42

    Google Scholar 

  • Chen C, Zhang J, Lu M, Qin C, Chen Y, Yang L, Huang Q, Wang J, Shen Z, Shen Q (2016) Microbial communities of an arable soil treated for 8 years with organic and inorganic fertilizers. Biol Fert Soils 52:455–467

    CAS  Google Scholar 

  • Chen G, Zhao G, Zhang H, Shen Y, Fei H, Cheng W (2017b) Biogas slurry use as N fertilizer for two-season Zizania aquatica Turcz in China. Nutr Cycl Agroecosys 107:303–320

    CAS  Google Scholar 

  • Cheng J, Chen Y, He T, Liao R, Liu R, Yi M, Huang L, Yang Z, Fu T, Li X (2017) Soil nitrogen leaching decreases as biogas slurry DOC/N ratio increases. Appl Soil Ecol 111:105–113

    Google Scholar 

  • Chodak M, Gołębiewski M, Morawska-Płoskonka J, Kuduk K, Niklińska M (2013) Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl Soil Ecol 64:7–14

    Google Scholar 

  • Dai H, Chen Y, Yang X, Cui J, Sui P (2017) The effect of different organic materials amendment on soil bacteria communities in barren sandy loam soil. Environ Sci Pollut Res 24:24019–24028

    CAS  Google Scholar 

  • Ding W, Xu X, He P, Ullah S, Zhang J, Cui Z, Zhou W (2018) Improving yield and nitrogen use efficiency through alternative fertilization options for rice in China: A meta-analysis. Field Crop Res 227:11–18

    Google Scholar 

  • Domingo-Olivé F, Bosch-Serra ÀD, Yagüe MR, Poch RM, Boixadera J (2016) Long term application of dairy cattle manure and pig slurry to winter cereals improves soil quality. Nutr Cycl Agroecosys 104: 39-51

    Article  Google Scholar 

  • Du S, Ya T, Zhang M, Zhu M, Li N, Liu S, Wang X (2020) Distinct microbial communities and their networks in an anammox coupled with sulfur autotrophic/mixotrophic denitrification system. Environ Pollut 262:114190

    CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  Google Scholar 

  • Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017

    CAS  Google Scholar 

  • Formentini TA, Mallmann FJK, Pinheiro A, Fernandes CVS, Bender MA, da Veiga M, dos Santos DR, Doelsch E (2015) Copper and zinc accumulation and fractionation in a clayey Hapludox soil subject to long-term pig slurry application. Sci Total Environ 536:831–839

    CAS  Google Scholar 

  • Fox A, Ikoyi I, Creamer R, Lanigan G, Schmalenberger A (2017) Microbial community structure and function respond more strongly to temporal progression than to the application of slurry in an Irish grassland. Appl Soil Ecol 120:97–104

    Google Scholar 

  • Guo J, Liu W, Zhu C, Luo G, Kong Y, Ling N, Wang M, Dai J, Shen Q, Guo S (2017) Bacterial rather than fungal community composition is associated with microbial activities and nutrient-use efficiencies in a paddy soil with short-term organic amendments. Plant Soil 424:335–349

    Google Scholar 

  • Heintze G, Eickenscheidt T, Schmidhalter U, DrÖSler M (2017) Influence of soil organic carbon on greenhouse gas emission potential after application of biogas residues or cattle slurry: Results from a pot experiment. Pedosphere 27: 807-821

    Article  CAS  Google Scholar 

  • Hernández D, Polo A, Plaza C (2013) Long-term effects of pig slurry on barley yield and N use efficiency under semiarid Mediterranean conditions. Eur J Agron 44:78–86

    Google Scholar 

  • Hou H, Zhou S, Hosomi M, Toyota K, Yosimura K, Mutou Y, Nisimura T, Takayanagi M, Motobayashi T (2007) Ammonia emissions from anaerobically-digested slurry and chemical fertilizer applied to flooded forage rice. Water Air Soil Pollut 183:37–48

    CAS  Google Scholar 

  • Jin H, Chang Z (2011) Distribution of heavy metal contents and chemical fractions in anaerobically digested manure slurry. Appl Biochem Biotechnol 164:268–282

    CAS  Google Scholar 

  • Legros S, Doelsch E, Feder F, Moussard G, Sansoulet J, Gaudet JP, Rigaud S, Doelsch IB, Macary HS, Bottero JY (2013) Fate and behaviour of Cu and Zn from pig slurry spreading in a tropical water–soil–plant system. Agric Ecosyst Environ 164:70–79

    CAS  Google Scholar 

  • Li S, Wu J, Huo Y, Zhao X, Xue L (2021) Profiling multiple heavy metal contamination and bacterial communities surrounding an iron tailing pond in Northwest China. Sci Total Environ 752:141827

    CAS  Google Scholar 

  • Liang B, Wang LY, Mbadinga SM, Liu JF, Yang SZ, Gu JD, Mu BZ (2015) Anaerolineaceae and Methanosaeta turned to be the dominant microorganisms in alkanes-dependent methanogenic culture after long-term of incubation. AMB Express 5:117

    Google Scholar 

  • Lin Y, Ye Y, Hu Y, Shi H (2019) The variation in microbial community structure under different heavy metal contamination levels in paddy soils. Ecotoxicol Environ Saf 180:557–564

    CAS  Google Scholar 

  • Ling N, Chen D, Guo H, Wei J, Bai Y, Shen Q, Hu S (2017) Differential responses of soil bacterial communities to long-term N and P inputs in a semi-arid steppe. Geoderma 292:25–33

    CAS  Google Scholar 

  • Liu J, Sui Y, Yu Z, Shi Y, Chu H, Jin J, Liu X, Wang G (2014) High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China. Soil Biol Biochem 70: 113-122

    Article  CAS  Google Scholar 

  • Liu T, Qin S, Pang Y, Yao J, Zhao X, Clough T, Wrage-Mönnig N, Zhou S (2019) Rice root Fe plaque enhances paddy soil NO emissions via Fe(II) oxidation-coupled denitrification 2. Soil Biol Biochem 139:107610

    CAS  Google Scholar 

  • Lu J, Jiang L, Chen D, Toyota K, Strong PJ, Wang H, Hirasawa T (2012) Decontamination of anaerobically digested slurry in a paddy field ecosystem in Jiaxing region of China. Agric Ecosyst Environ 146:13–22

    CAS  Google Scholar 

  • Lu LK (1999) Analytical methods of soil and agricultural chemistry. China Agri Sci Tech Press, Beijing (in Chinese)

    Google Scholar 

  • Ma Y, Wang Y, Chen Q, Li Y, Guo D, Nie X, Peng X (2020) Assessment of heavy metal pollution and the effect on bacterial community in acidic and neutral soils. Ecol Indic 117:106626

    CAS  Google Scholar 

  • Meng D, Li J, Liu T, Liu Y, Yan M, Hu J, Li X, Liu X, Liang Y, Liu H, Yin H (2019) Effects of redox potential on soil cadmium solubility: Insight into microbial community. J Environ Sci 75:224–232

    Google Scholar 

  • Moreno-García B, Guillén M, Quílez D (2017) Response of paddy rice to fertilisation with pig slurry in northeast Spain: Strategies to optimise nitrogen use efficiency. Field Crop Res 208:44–54

    Google Scholar 

  • Olsen S, Sommers L (1982) Phosphorus. In: Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties, Second ed. SSSA, Madison

  • Ovejero J, Ortiz C, Boixadera J, Serra X, Ponsá S, Lloveras J, Casas C (2016) Pig slurry fertilization in a double-annual cropping forage system under sub-humid Mediterranean conditions. Eur J Agron 81:138–149

    Google Scholar 

  • Pan X, Zhang S, Zhong Q, Gong G, Wang G, Guo X, Xu X (2020) Effects of soil chemical properties and fractions of Pb, Cd, and Zn on bacterial and fungal communities. Sci Total Environ 715:136904

    CAS  Google Scholar 

  • Peng S, Buresh RJ, Huang J, Yang J, Zou Y, Zhong X, Wang G, Zhang F (2006) Strategies for overcoming low agronomic nitrogen use efficiency in irrigated rice systems in China. Field Crop Res 96:37–47

    Google Scholar 

  • Rahaman MA, Zhang Q, Shi Y, Zhan X, Li G (2021) Biogas slurry application could potentially reduce NO emissions and increase crop yield 2. Sci Total Environ 778:146269

    CAS  Google Scholar 

  • Sasada Y, Win KT, Nonaka R, Win AT, Toyota K, Motobayashi T, Hosomi M, Dingjiang C, Lu J (2011) Methane and N2O emissions, nitrate concentrations of drainage water, and zinc and copper uptake by rice fertilized with anaerobically digested cattle or pig slurry. Biol Fert Soils 47:949–956

    CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    CAS  Google Scholar 

  • Singh JP, Vaidya BP, Goodey NM, Krumins JA (2019) Soil microbial response to metal contamination in a vegetated and urban brownfield. J Environ Manag 244:313–319

    CAS  Google Scholar 

  • Song J, Shen Q, Wang L, Qiu G, Shi J, Xu J, Brookes PC, Liu X (2018) Effects of Cd, Cu, Zn and their combined action on microbial biomass and bacterial community structure. Environ Pollut 243:510–518

    CAS  Google Scholar 

  • Tang Y, Wang L, Carswell A, Misselbrook T, Shen J, Han J (2020) Fate and transfer of heavy metals following repeated biogas slurry application in a rice-wheat crop rotation. J Environ Manag 270:110938

    CAS  Google Scholar 

  • Terhoeven-Urselmans T, Scheller E, Raubuch M, Ludwig B, Joergensen RG (2009) CO2 evolution and N mineralization after biogas slurry application in the field and its yield effects on spring barley. Appl Soil Ecol 42:297–302

    Google Scholar 

  • Tian W, Wang L, Li Y, Zhuang K, Li G, Zhang J, Xiao X, Xi Y (2015) Responses of microbial activity, abundance, and community in wheat soil after three years of heavy fertilization with manure-based compost and inorganic nitrogen. Agric Ecosyst Environ 213:219–227

    CAS  Google Scholar 

  • USDA/NRCS (1999) Soil Taxonomy. A basic system of soil classification for making and interpreting soil surveys, 2nd edn. U.S. Government Printing Office, Washington, DC

    Google Scholar 

  • van der Bom F, Nunes I, Raymond NS, Hansen V, Bonnichsen L, Magid J, Nybroe O, Jensen LS (2018) Long-term fertilisation form, level and duration affect the diversity, structure and functioning of soil microbial communities in the field. Soil Biol Biochem 122:91–103

    Google Scholar 

  • Walsh JJ, Rousk J, Edwards-Jones G, Jones DL, Williams AP (2012) Fungal and bacterial growth following the application of slurry and anaerobic digestate of livestock manure to temperate pasture soils. Biol Fertil Soils 48:889–897

    Google Scholar 

  • Wang C, Huang Y, Zhang C, Zhang Y, Yuan K, Xue W, Liu Y, Liu Y, Liu Z (2021) Inhibition effects of long-term calcium-magnesia phosphate fertilizer application on Cd uptake in rice: Regulation of the iron-nitrogen coupling cycle driven by the soil microbial community. J Hazard Mater 416:125916

    CAS  Google Scholar 

  • Wang J, Song Y, Ma T, Raza W, Li J, Howland JG, Huang Q, Shen Q (2017) Impacts of inorganic and organic fertilization treatments on bacterial and fungal communities in a paddy soil. Appl Soil Ecol 112: 42-50

    Article  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    CAS  Google Scholar 

  • Wentzel S, Schmidt R, Piepho H-P, Semmler-Busch U, Joergensen RG (2015) Response of soil fertility indices to long-term application of biogas and raw slurry under organic farming. Appl Soil Ecol 96:99–107

    Google Scholar 

  • Win AT, Toyota K, Win KT, Motobayashi T, Ookawa T, Hirasawa T, Chen D, Lu J (2014) Effect of biogas slurry application on CH4 and N2O emissions, Cu and Zn uptakes by whole crop rice in a paddy field in Japan. Soil Sci Plant Nutr 60:411–422

    CAS  Google Scholar 

  • Win KT, Nonaka R, Win AT, Sasada Y, Toyota K, Motobayashi T (2013) Effects of water saving irrigation and rice variety on greenhouse gas emissions and water use efficiency in a paddy field fertilized with anaerobically digested pig slurry. Paddy Water Environ 13:51–60

    Google Scholar 

  • Wu M, Qin H, Chen Z, Wu J, Wei W (2011) Effect of long-term fertilization on bacterial composition in rice paddy soil. Biol Fert Soils 47:397–405

    Google Scholar 

  • Xu M, Xian Y, Wu J, Gu Y, Yang G, Zhang X, Peng H, Yu X, Xiao Y, Li L (2019) Effect of biogas slurry addition on soil properties, yields, and bacterial composition in the rice-rape rotation ecosystem over 3 years. J Soils Sediments 19:2534–2542

    CAS  Google Scholar 

  • Xun W, Xiong W, Huang T, Ran W, Li D, Shen Q, Li Q, Zhang R (2016) Swine manure and quicklime have different impacts on chemical properties and composition of bacterial communities of an acidic soil. Appl Soil Ecol 100:38–44

    Google Scholar 

  • Yang L, Qin Z, Tu L (2015) Responses of rice yields in different rice-cropping systems to climate variables in the middle and lower reaches of the Yangtze River, China. Food Secur 7:951–963

    Google Scholar 

  • Yang Y, Li X, Liu J, Zhou Z, Zhang T, Wang X (2017) Bacterial diversity as affected by application of manure in red soils of subtropical China. Biol Fertil Soils 53:639–649

    Google Scholar 

  • Ye J, Zhang R, Nielsen S, Joseph SD, Huang D, Thomas T (2016) A combination of biochar-mineral complexes and compost improves soil bacterial processes, soil quality, and plant properties. Front Microbiol 7:372

    Google Scholar 

  • Zeng XY, Li SW, Leng Y, Kang XH (2020) Structural and functional responses of bacterial and fungal communities to multiple heavy metal exposure in arid loess. Sci Total Environ 723:138081

    CAS  Google Scholar 

  • Zhang C, Nie S, Liang J, Zeng G, Wu H, Hua S, Liu J, Yuan Y, Xiao H, Deng L, Xiang H (2016) Effects of heavy metals and soil physicochemical properties on wetland soil microbial biomass and bacterial community structure. Sci Total Environ 557–558:785–790

    Google Scholar 

  • Zhang J, Wang M, Cao Y, Liang P, Wu S, Leung AO, Christie P (2017a) Replacement of mineral fertilizers with anaerobically digested pig slurry in paddy fields: assessment of plant growth and grain quality. Environ Sci Pollut Res 24:8916–8923

    CAS  Google Scholar 

  • Zhang X, Zhang R, Gao J, Wang X, Fan F, Ma X, Yin H, Zhang C, Feng K, Deng Y (2017b) Thirty-one years of rice-rice-green manure rotations shape the rhizosphere microbial community and enrich beneficial bacteria. Soil Biol Biochem 104:208–217

    CAS  Google Scholar 

  • Zhao J, Ni T, Li Y, Xiong W, Ran W, Shen B, Shen Q, Zhang R (2014) Responses of bacterial communities in arable soils in a rice-wheat cropping system to different fertilizer regimes and sampling times. PLoS One 9:e85301

    Google Scholar 

  • Zhao J, Ni T, Xun W, Huang X, Huang Q, Ran W, Shen B, Zhang R, Shen Q (2017) Influence of straw incorporation with and without straw decomposer on soil bacterial community structure and function in a rice-wheat cropping system. Appl Microbiol Biotechnol 101:4761–4773

    CAS  Google Scholar 

  • Zhao J, Zhang R, Xue C, Xun W, Sun L, Xu Y, Shen Q (2014b) Pyrosequencing reveals contrasting soil bacterial diversity and community structure of two main winter wheat cropping systems in China. Microb Ecol 67:443–453

    Google Scholar 

  • Zheng X, Fan J, Cui J, Wang Y, Zhou J, Ye M, Sun M (2016) Effects of biogas slurry application on peanut yield, soil nutrients, carbon storage, and microbial activity in an Ultisol soil in southern China. J Soils Sediments 16:449–460

    CAS  Google Scholar 

Download references

Funding

This work was jointly funded by the Natural Science Foundation for Youths of Zhejiang Province of China (LQ19C150005), the key Research and Development Program of Zhejiang Province of China (2019C02017, 2021C02035, 2020C02030-06), the Project of Unification of Water and Soil Science for One Healthy funded by Zhejiang Academy of Agricultural Sciences, and the Construction Project of Agricultural Green Development Pilot Support System of Huangyan District of Taizhou City (HY202001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhaoming Chen.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible editor: Yuan Ge

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 400 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Q., Chen, Z., Zhao, J. et al. Fate of heavy metals and bacterial community composition following biogas slurry application in a single rice cropping system. J Soils Sediments 22, 968–981 (2022). https://doi.org/10.1007/s11368-021-03117-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-021-03117-4

Keywords

Navigation