Skip to main content

Long-term nickel exposure altered the bacterial community composition but not diversity in two contrasting agricultural soils

Abstract

Nickel pollution imposes deleterious effects on soil ecosystem. The responses of soil microorganisms to long-term nickel pollution under field conditions remain largely unknown. Here, we used high-throughput sequencing to elucidate the impacts of long-term nickel pollution on soil bacterial communities in two contrasting agricultural soils. Our results found that the soil microbial biomass carbon consistently decreased along the nickel gradients in both soils. Nickel pollution selectively favored or impeded the prevalence of several dominant bacterial guilds, in particular, Actinobacteria showed tolerance, while Acidobacteria and Planctomycetes displayed sensitivity. Despite the apparent shifts in the bacterial community composition, no clear tendency in the bacterial diversity and abundance was identified along the nickel gradients in either soil. Collectively, we provide evidence that long-term nickel pollution shifted the soil bacterial communities, resulting in the decrease of microbial biomass although the bacterial diversity was not significantly changed.

This is a preview of subscription content, access via your institution.

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

References

  • Adamo P, Dudka S, Wilson MJ, McHardy WJ (1996) Chemical and mineralogical forms of Cu and Ni in contaminated soils from the Sudbury mining and smelting region Canada. Environ Pollut 91:11–19

    CAS  Article  Google Scholar 

  • Ager D, Evans S, Li H, Lilley AK, van der Gast CJ (2010) Anthropogenic disturbance affects the structure of bacterial communities. Environ Microbiol 12:670–678

    Article  Google Scholar 

  • Awasthi A, Singh M, Soni SK, Singh R, Kalra A (2014) Biodiversity acts as insurance of productivity of bacterial communities under abiotic perturbations. ISME J 8:2445–2452

    Article  Google Scholar 

  • Bååth E, Frostegård Å, Pennanen T, Fritze H (1995) Microbial community structure and pH response in relation to soil organic matter quality in wood-ash fertilized, clear-cut or burned coniferous forest soils. Soil Biol Biochem 27:229–240

    Article  Google Scholar 

  • Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC (1999) Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem 31:1021–1030

    CAS  Article  Google Scholar 

  • Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917

    CAS  Article  Google Scholar 

  • Berg J, Brandt KK, Al-Soud WA, Holm PE, Hansen LH, Sørensen SJ, Nybroe O (2012) Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term Cu exposure. Appl Environ Microbiol 78:7438–7446

    CAS  Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010a) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  Article  Google Scholar 

  • Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010b) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

    CAS  Article  Google Scholar 

  • Cempel M, Nikel G (2006) Nickel: a review of its sources and environmental toxicology. Polish J of Environ Stud 15:375–382

    CAS  Google Scholar 

  • Chen X, Zhang LM, Shen JP, Xu ZH, He JZ (2010) Soil type determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soil Sediment 10:1510–1516

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science 320:1034–1039

    CAS  Article  Google Scholar 

  • Field D, Tiwari B, Booth T, Houten S, Swan D, Bertrand N, Thurston M (2006) Open software for biologists: from famine to feast. Nat Biotechnol 24:801–804

    CAS  Article  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. PNAS 103:626–631

    CAS  Article  Google Scholar 

  • Fierer N, Schimel JP, Holden PA (2003) Influence of drying–rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71

    CAS  Article  Google Scholar 

  • Fierer N, Ladau J, Clemente JC, Leff JW, Owens SM, Pollard KS, Knight R, Gilbert JA, McCulley RL (2013) Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the united states. Science 342:621–624

    CAS  Article  Google Scholar 

  • Fuerst JA, Sagulenko E (2011) Beyond the bacterium: Planctomycetes challenge our concepts of microbial structure and function. Nat Rev 9:403–413

    CAS  Google Scholar 

  • Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    CAS  Article  Google Scholar 

  • Griffiths BS, Philippot L (2012) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37:112–129

    Article  Google Scholar 

  • Guo XY, Zuo YB, Wang BR, Li JM, Ma YB (2010) Toxicity and accumulation of copper and nickel in maize plants cropped on calcareous and acidic field soils. Plant Soil 333:365–373

    CAS  Article  Google Scholar 

  • Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47:453–467

    CAS  Article  Google Scholar 

  • He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374

    CAS  Article  Google Scholar 

  • He JZ, Zheng Y, Chen CR, He YQ, Zhang LM (2008) Microbial composition and diversity of an upland red soil under long-term fertilization treatments as revealed by culture-dependent and culture-independent approaches. J Soil Sediment 8:349–358

    CAS  Article  Google Scholar 

  • He JZ, Ge Y, Xu ZH, Chen CR (2009) Linking soil bacterial diversity to ecosystem multifunctionality using backward-elimination boosted tree analysis. J Soil Sediment 9:547–554

    CAS  Article  Google Scholar 

  • He JZ, Hu HW, Zhang LM (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem 55:146–154

    CAS  Article  Google Scholar 

  • Héry M, Nazaret S, Jaffré T, Normand P, Navarro E (2003) Adaptation to nickel spiking of bacterial communities in neocaledonian soils. Environ Microbiol 5:3–12

    Article  Google Scholar 

  • Hu HW, Zhang LM, Dai Y, Di HJ, He JZ (2013) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soil Sediment 13:1439–1449

    Article  Google Scholar 

  • Hu HW, Xu ZH, He JZ (2014) Ammonia-oxidizing archaea play a predominant role in acid soil nitrification. Adv Agron 125:261–302

    Article  Google Scholar 

  • Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    CAS  Article  Google Scholar 

  • Khan S, Hesham AE, Qiao M, Rehman S, He JZ (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res 17:288–296

    CAS  Article  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    CAS  Article  Google Scholar 

  • Lejon DPH, Pascault N, Ranjard L (2010) Differential copper impact on density, diversity and resistance of adapted culturable bacterial populations according to soil organic status. Eur J Soil Biol 46:168–174

    CAS  Article  Google Scholar 

  • Li J, Zheng YM, Liu YR, Ma YB, Hu HW, He JZ (2014) Initial copper stress strengthens the resistance of soil microorganisms to a subsequent copper stress. Microb Ecol 67:931–941

    CAS  Article  Google Scholar 

  • Liu YR, Zheng YM, Shen JP, Zhang LM, He JZ (2010) Effects of mercury on the activity and community composition of soil ammonia oxidizers. Environ Sci Pollut Res 17:1237–1244

    CAS  Article  Google Scholar 

  • Ma YB, Lombi E, Oliver IW, Nolan AL, Mclaughlin MJ (2006) Long-term aging of copper added to soils. Environ Sci Technol 40:6310–6317

    CAS  Article  Google Scholar 

  • Macdonald CA, Singh BK, Peck JA, van Schaik AP, Hunter LC, Horswell J, Campbell CD, Speir TW (2007) Long-term exposure to Zn-spiked sewage sludge alters soil community structure. Soil Biol Biochem 39:2576–2586

    CAS  Article  Google Scholar 

  • Macdonald CA, Clark IM, Zhao FJ, Hirsch PR, Singh BK, McGrath SP (2011) Long-term impacts of zinc and copper enriched sewage sludge additions on bacterial, archaeal and fungal communities in arable and grassland soils. Soil Biol Biochem 43:932–941

    CAS  Article  Google Scholar 

  • Magoè T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  Google Scholar 

  • Marcina C, Marcin G, Justynac M, Katarzynac K, Mariac N (2013) Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl Soil Ecol 64:7–14

    Article  Google Scholar 

  • McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2011) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618

    Article  Google Scholar 

  • Mirete S, de Figueras CG, González-Pastor JE (2007) Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Appl Environ Microbiol 73:6001–6011

    CAS  Article  Google Scholar 

  • Shen JP, Xu ZH, He JZ (2014) Frontiers in the microbial processes of ammonia oxidation in soils and sediments. J Soil Sediment 14:1023–1029

    CAS  Article  Google Scholar 

  • Singh BK, Quince C, Macdonald CA, Khachane A, Thomas N, Al-Soud WA, Sørensen SJ, He ZL, White D, Sinclair A, Crooks B, Zhou JZ, Campbell CD (2014) Loss of microbial diversity in soils is coincident with reductions in some specialized functions. Environ Microbiol 16:2408–2420

    Article  Google Scholar 

  • Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5’-nuclease assays. Appl Environ Microbiol 66:4605–4614

    CAS  Article  Google Scholar 

  • Trivedi P, Anderson IC, Singh BK (2013) Microbial modulators of soil carbon storage: integrating genomic and metabolic knowledge for global prediction. Trends Microbiol 21:614–651

    Article  Google Scholar 

  • Wakelin SA, Chu GX, Lardner R, Liang YC, McLaughlin MJ (2010) A single application of Cu to field soil has long term effects on bacterial community structure, diversity, and soil processes. Pedobiologia 53:149–158

    CAS  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  Article  Google Scholar 

  • Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, Vos PD, Verstraete W, Boon N (2009) Initial community evenness favours functionality under selective stress. Nature 458:623–626

    CAS  Article  Google Scholar 

  • Wu JS, Joergensen RG, Pommerening B (1990) Measurement of soil microbial biomass C by fumigation-extraction-an automated procedure. Soil Biol Biochem 22:1167–1169

    CAS  Article  Google Scholar 

  • Yang GY, Luo W, Zhang TB, Wan HF, Gao YX (2007) The distribution of Ni contents in agricultural soils in the Pearl River Delta, China. Ecol Environ 16:818–821 (in Chinese)

    Google Scholar 

Download references

Acknowledgments

This work was financially supported by National Science Foundation of China (51221892 and 41201523).We gratefully acknowledge Li-Mei Zhang and Miao-Miao Zhang for their assistance during the field sampling.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ji-Zheng He.

Additional information

Responsible editor: Zhihong Xu

Capsule: Nickel pollution altered soil bacterial community composition but not diversity.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, J., Hu, HW., Ma, YB. et al. Long-term nickel exposure altered the bacterial community composition but not diversity in two contrasting agricultural soils. Environ Sci Pollut Res 22, 10496–10505 (2015). https://doi.org/10.1007/s11356-015-4232-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4232-1

Keywords

  • Nickel pollution
  • Soil bacterial community
  • Diversity
  • Abundance
  • Community composition
  • Soil microbial biomass carbon
  • Field experiment