Skip to main content
SpringerLink
Log in

Shifts in the structure and function of the microbial community in response to metal pollution of fresh water sediments in Finland

  • Sustainable Risk Management of Contaminated Land and Sediment - NORDROCS 2016
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Mining is a common source of metals in aquatic ecosystems. Metal loading in the environment is thought to be a selective pressure that induces compositional and functional changes within the affected microbial community in the sediment. This study aims to explore shifts in the diversity, structure, and functional gene abundance of microbial communities in the sediment of the copper mining-induced contaminated lakes in Finland.

Materials and methods

The sediment microbial community structures and abundance of the functional groups involved in carbon/nitrogen/sulfur cycling in four lakes located downstream from metal mines (Kirkkoselkä (KS), Junttiselkä (JS), Laakajärvi (LJ), and Sysmäjärvi (SJ)) and one reference lake (Parkkimanjärvi (PJ)) in Finland were compared using high throughput sequencing and quantitative PCR.

Results and discussion

Compared to the PJ reference lake sediment, the relative abundances were higher for Bacteroidetes, Gemmatimonadetes, Acidobacteria, and Nitrospirae but lower for Firmicutes and Alphaproteobacteria in the mine-contaminated sediment samples. The number of copies of copper-resistant genes (copA) in the two copper-contaminated sediments (5.34 × 106 and 4.95 × 106 copies ng−1 DNA for KS and JS, respectively) was significantly higher than that in the PJ sediment (1.33 × 106 copies ng−1 DNA). Methanogens (mcrA gene) accounted for 5.09–11.5% of the total archaea (16S rRNA) in these lake sediments. In addition, ammonia-oxidizing archaea (amoA gene) in the LJ sediment accounted for 36.0% of the total archaea but only 0.83–1.63% in the sediment of other lakes. The abundance of eight investigated functional groups accounted for 28.8% of the total bacteria in the PJ sediment but less than 1.3% in the metal-contaminated sediments. The canonical correspondence analysis showed that the microbial community structure of Lake LJ was scattered far from the other lakes and was significantly correlated with nitrate; the community structural change in the JS and KS sediments was positively correlated with copper or negatively correlated with nitrate concentration.

Conclusions

These results indicate that the sedimentary indigenous microbial community may shift its composition and structure as well as its function to increase its adaptability and/or resistance to metal-contaminated freshwater sediments.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Altimira F, Yáñez C, Bravo G, González M, Rojas LA, Seeger M (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12(1):193

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña 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

    Article  CAS  Google Scholar 

  • Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM (2007) The ribosomal database project (RDP-II): introducing my RDP space and quality controlled public data. Nucleic Acids Res 35:169–172

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    Article  CAS  Google Scholar 

  • Eggleton J, Thomas KV (2004) A review of factors affecting the release and bioavailability of contaminants during sediment disturbance events. Environ Int 30:973–980

    Article  CAS  Google Scholar 

  • Feinstein LM, Sul WJ, Blackwood CB (2009) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol 75(16):5428–5433

    Article  CAS  Google Scholar 

  • Gillan DC, Danis B, Pernet P, Joly G, Dubois P (2005) Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Appl Environ Microbiol 71(2):679–690

    Article  CAS  Google Scholar 

  • Gillan DC, Pernet P (2007) Adherent bacteria in heavy metal contaminated marine sediments. Biofouling 23:1e13

    Article  Google Scholar 

  • Giusti L (2001) Heavy metal contamination of brown seaweed and sediments from the UK coastline between the Wear River and the Tees River. Environ Int 26:275–286

    Article  CAS  Google Scholar 

  • González AG, Shirokova LS, Pokrovsky OS, Emnovad EE, Martíneze RE, Santana-Casianoa JM, González-Dávilaa M, Pokrovskib GS (2010) Adsorption of copper on Pseudomonas aureofaciens: protective role of surface exopolysaccharides. J Colloid Interface Sci 350(1):305–314

    Article  Google Scholar 

  • Gough HL, Stahl DA (2011) Microbial community structures in anoxic freshwater lake sediment along a metal contamination gradient. ISME J 5(3):543–558

    Article  Google Scholar 

  • He LY, Zhang YF, Ma HY, Su LN, Chen ZJ, Wang QY, Qian M, Sheng XF (2010) Characterization of copper-resistant bacteria and assessment of bacterial communities in rhizosphere soils of copper-tolerant plants. Appl Soil Ecol 44(1):49–55

    Article  Google Scholar 

  • Hoostal MJ, Bidart-Bouzat MG, Bouzat JL (2008) Local adaptation of microbial communities to heavy metal stress in polluted sediments of Lake Erie. FEMS Microbiol Ecol 65(1):156–168

    Article  CAS  Google Scholar 

  • Jose J, Giridhar R, Anas A, Loka Bharathi PA, Nair S (2011) Heavy metal pollution exerts reduction/adaptation in the diversity and enzyme expression profile of heterotrophic bacteria in Cochin estuary, India. Environ Pollut 159:2775e2780

    Article  Google Scholar 

  • Kang S, Nostrand JDV, Gough HL, He Z, Hazen TC, Stahl DA, Zhou J (2013) Functional gene array-based analysis of microbial communities in heavy metals-contaminated lake sediments. FEMS Microbiol Ecol 86(2):200

    Article  CAS  Google Scholar 

  • Li XF, Zhu YG, Cavagnaro TR, Chen MM, Sun JW, Chen XP, Qiao M (2009) Do ammonia-oxidizing archaea respond to soil Cu contamination similarly as ammonia-oxidizing bacteria? Plant Soil 324(1–2):209–217

    Article  CAS  Google Scholar 

  • Li X, Zhu YG, Shaban B, Bruxner TJC, Bond PL, Huang LB (2015) Assessing the genetic diversity of Cu resistance in mine tailings through high-throughput recovery of full-length copA genes. Sci Rep 5:13258. doi:10.1038/srep13258

    Article  CAS  Google Scholar 

  • Lors C, Tiffreau C, Laboudigue A (2004) Effects of bacterial activities on the release of heavy metals from contaminated dredged sediments. Chemosphere 56:619–630

    Article  CAS  Google Scholar 

  • Mackintosh TJ, Davis JA, Thompson RM (2016) Impacts of multiple stressors on ecosystem function: leaf decomposition in constructed urban wetlands. Environ Pollut 208:221–232

    Article  CAS  Google Scholar 

  • Mäkinen J, Lerssi J (2007) Characteristics and seasonal variation of sediments in Lake Junttiselkä, Pyhäsalmi, Finland. Mine Water Environ 26(4):217–228

    Article  Google Scholar 

  • Nealson KH (1997) Sediment bacteria: who’s there, what are they doing, and what’s new? Annu Rev Earth Planet Sci 25:403–434

    Article  CAS  Google Scholar 

  • Ni C, Horton DJ, Rui J, Henson MW, Jiang Y, Huang X, Learman DR (2016) High concentrations of bioavailable heavy metals impact freshwater sediment microbial communities. Ann Microbiol 66(3):1003–1012

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet G, Kindt R, Legendre P, O’Hara RG, Simpson GL (2010) Vegan: community ecology package. R Package Version 1:17–11

    Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  Google Scholar 

  • Ryan RP, Ryan DJ, Dowling DN (2005) Multiple metal resistant transferable phenotypes in bacteria as indicators of soil contamination with heavy metals. J Soils Sediments 5:95–100

    Article  CAS  Google Scholar 

  • Sauvain L, Bueche M, Junier T, Masson M, Wunderlin T, Kohler-Milleret R, Diez EG, Loizeau J, Tercier-Waeber M, Junier P (2014) Bacterial communities in trace metal contaminated lake sediments are dominated by endospore-forming bacteria. Aqua Sci 76(1):33–46

    Article  CAS  Google Scholar 

  • Sun FL, Fan LL, Xie GJ (2016) Effect of copper on the performance and bacterial communities of activated sludge using Illumina MiSeq platforms. Chemosphere 156:212–219

    Article  CAS  Google Scholar 

  • Utgikar VP, Tabak HH, Haines JR, Govind R (2003) Quantification of toxic and inhibitory impact of copper and zinc on mixed cultures of sulfate-reducing bacteria. Biotech Bioengin 82(3):306–312

    Article  CAS  Google Scholar 

  • Väänänen K, Kauppila T, Mäkinen J, Leppänen MT, Lyytikäinen M, Akkanen J (2016) Ecological risk assessment of boreal sediments affected by metal mining: metal geochemistry, seasonality, and comparison of several risk assessment methods. Integr Environ Assess Manag 12(4):759–771

    Article  Google Scholar 

  • Vignesh S, Dahms HU, Emmanuel KV, Gokul MS, Muthukumar K, Kim BR, James RA (2014) Physicochemical parameters aid microbial community? A case study from marine recreational beaches, Southern India. Environ Monit Assess 186:1875–1887

    Article  CAS  Google Scholar 

  • Volodina LA, Zhigach AN, Leĭpunskiĭ IO, Fedorov II (2009) Mechanism of the toxic action of copper nanoparticles on Escherichia coli bacteria. Biofizika 54(6):1060

    CAS  Google Scholar 

  • Wieland F, Hartert C (1999) Mechanisms of vesicle formation: insights from the COP system. Curr Opin Cell Biol 11(4):440–446

    Article  CAS  Google Scholar 

  • Xie Y, Wang J, Wu Y, Ren C, Song C, Yang J, Zhang X (2016) Using in situ bacterial communities to monitor contaminants in river sediments. Environ Pollut 212:348–357

    Article  CAS  Google Scholar 

  • Yin H, Niu J, Ren Y, Cong J, Zhang X, Fan FL, Xia Y, Zhang X, Deng J, Xie M, He Z, Zhou J, Liang Y, Liu X (2015) An integrated insight into the response of sedimentary microbial communities to heavy metal contamination. Sci Rep 5(1):14266. doi:10.1038/srep14266

    Article  CAS  Google Scholar 

  • Yu C, He X, Zhang C, Li C, Liu J (2015) Treatment of iron and copper in wastewater by immobilized sulfate reducing bacteria and producing H2S by an indirect method. FOG - Freiberg Online Geosci 40:109–115

    Google Scholar 

  • Zhang X, Gu Q, Long XE, Li ZL, Liu DX, Ye DH, He CQ, Liu XY, Väänänen K, Chen XP (2016) Anthropogenic activities drive the microbial community and its function in urban river sediment. J Soils Sediments 16(2):716–725

    Article  CAS  Google Scholar 

  • Mato Rodriguez L, Alatossava T (2010) Effects of copper on germination, growth and sporulation of Clostridium tyrobutyricum. Food Microbiology 27(3):434–437

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Key Research and Development Project by Most of China (2016YFA0601000), the National Natural Science Foundation of China (41373097, 31300443 41101230), the Shanghai Science and Technology Committee (12231202004), the Shanghai Key Laboratory of Bio-Energy Crops (10DZ2271800), and the Kone Foundation (Finland).

Author information

Authors and Affiliations

  1. School of Environmental and Chemical Engineering, Shanghai University, Shanghai, 200444, China

    Xue-Ping Chen, Hao-Yu Chen, Jing Sun, Xu Zhang, Chi-Quan He, Xiao-Yan Liu, Xin Huang, Min Yang & Fu-Shun Wang

  2. Department of Environmental and Biological Sciences, University of Eastern Finland, 80101, Joensuu, Finland

    Kristiina Väänänen

Authors
  1. Xue-Ping Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hao-Yu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chi-Quan He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiao-Yan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xin Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Min Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fu-Shun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kristiina Väänänen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xue-Ping Chen or Kristiina Väänänen.

Additional information

Responsible editor: Martin Romantschuk

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, XP., Chen, HY., Sun, J. et al. Shifts in the structure and function of the microbial community in response to metal pollution of fresh water sediments in Finland. J Soils Sediments 18, 3324–3333 (2018). https://doi.org/10.1007/s11368-017-1782-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-017-1782-5

Keywords

Search

Navigation