Advertisement

Environmental Science and Pollution Research

, Volume 23, Issue 6, pp 5644–5653 | Cite as

Effects of long-term radionuclide and heavy metal contamination on the activity of microbial communities, inhabiting uranium mining impacted soils

  • Silvena Boteva
  • Galina Radeva
  • Ivan Traykov
  • Anelia KenarovaEmail author
Research Article

Abstract

Ore mining and processing have greatly altered ecosystems, often limiting their capacity to provide ecosystem services critical to our survival. The soil environments of two abandoned uranium mines were chosen to analyze the effects of long-term uranium and heavy metal contamination on soil microbial communities using dehydrogenase and phosphatase activities as indicators of metal stress. The levels of soil contamination were low, ranging from ‘precaution’ to ‘moderate’, calculated as Nemerow index. Multivariate analyses of enzyme activities revealed the following: (i) spatial pattern of microbial endpoints where the more contaminated soils had higher dehydrogenase and phosphatase activities, (ii) biological grouping of soils depended on both the level of soil contamination and management practice, (iii) significant correlations between both dehydrogenase and alkaline phosphatase activities and soil organic matter and metals (Cd, Co, Cr, and Zn, but not U), and (iv) multiple relationships between the alkaline than the acid phosphatase and the environmental factors. The results showed an evidence of microbial tolerance and adaptation to the soil contamination established during the long-term metal exposure and the key role of soil organic matter in maintaining high microbial enzyme activities and mitigating the metal toxicity. Additionally, the results suggested that the soil microbial communities are able to reduce the metal stress by intensive phosphatase synthesis, benefiting a passive environmental remediation and provision of vital ecosystem services.

Keywords

Soil contamination Uranium and heavy metals Dehydrogenase Phosphatase Soil organic matter 

Notes

Acknowledgments

This research was supported by the National Science Fund of the Bulgarian Ministry of Education and Science (Grant DO12-131/ 2008). The authors thank Assoc. Prof. Rosen Tzonev (Sofia University “St. Kl. Ohridski”, The Faculty of Biology) for providing information for the type of vegetation at the study sites.

Compliance with ethical standards

Conflict of interests

The authors declare that they have no competing interests.

References

  1. Aleksieva P, Spasova D, Radoevska S (2003) Acid phosphatase distribution and localization in the fungus Humicola lutea. Z Naturforsch C 58c(3/4):239–43Google Scholar
  2. Antunes SC, Pereira R, Marques SM, Castro BB, Gonçalves F (2011) Impaired microbial activity caused by metal pollution: a field study in a deactivated uranium mining area. Sci Total Environ 410–411:87–95CrossRefGoogle Scholar
  3. Beazley MJ, Martinez RJ, Webb SM, Sobecky PA, Taillefert M (2011) The effect of pH and natural microbial phosphatase activity on the speciation of uranium in subsurface soils. Geochem Cosmochim Act 75:5648–63CrossRefGoogle Scholar
  4. Beazley MJ, Martinez RJ, Sobecky PA, Webb SM, Taillefert M (2007) Uranium biomineralization as a result of bacterial phosphatase activity: insights from bacterial isolates from a contaminated subsurface. Environ Sci Technol 41:5701–7CrossRefGoogle Scholar
  5. Borie F, Rubio R (2003) Total and organic phosphorus in Chilean volcanic soils. Gayana Bot 60:69–78CrossRefGoogle Scholar
  6. Caetano AL, Marques CR, Gavina A, Carvalho F, Gonçalves F, da Silva ER, Pereira R (2014) Contribution for the derivation of a soil screening value (SSV) for uranium, using a natural reference soil. Plos One 9(10):e108041CrossRefGoogle Scholar
  7. Chaudhuri D, Tripathy S, Veeresh H, Powell MA, Hart BR (2003) Relationship of chemical fractions of heavy metals with microbial and enzyme activities in sludge and ash-amended acid lateritic soil from India. Environ Geol 45:115–23CrossRefGoogle Scholar
  8. Cheng J, Shi Z, Zhu Y (2007) Assessment and mapping of environmental quality in agricultural soils of Zhejiang Province, China. J Environ Sci 19:50–4CrossRefGoogle Scholar
  9. 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 64:7–14CrossRefGoogle Scholar
  10. Dalal RC (1977) Soil organic phosphorus. Adv Agron 29:83–118CrossRefGoogle Scholar
  11. Diaz-Raviña M, Bååth E, Frostegård A (1994) Multiple heavy metal tolerance of soil bacterial communities and its measurement by a thymidine incorporation technique. Appl Environ Microb 60:2238–47Google Scholar
  12. Fisher B, Costanza R, Turner RK, Morling P (2007) Defining and classifying ecosystem services for decision making, CSERGE Working Paper EDM. No 07–04:20, Available at: http://hdl.handle.net/10419/80264 Google Scholar
  13. Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–414CrossRefGoogle Scholar
  14. Gu Y, Wag P, Kong C (2009) Urease, invertase, dehydrogenase and polyphenoloxidase activities in paddy soils influenced by allelophatic rice variety. Eur J Soil Biol 45:436–41CrossRefGoogle Scholar
  15. Keeney DR, Nelson DW (1982) Nitrogen-inorganic forms. In: Page AL, Miller RH, Keeney D (eds) Methods of soil analysis, part 2. Soil Sci Soc Am, Madison, WI, pp 643–98Google Scholar
  16. Kenarova A, Radeva G (2010) Inhibitory effects of total and water soluble concentrations of heavy metals on microbial dehydrogenase activity. CR Acad Bulg Sci 63:1029–34Google Scholar
  17. Kenarova A, Radeva G, Traykov I, Boteva S (2014) Community level physiological profiles of bacterial communities inhabiting uranium mining impacted sites. Ecotox Environ Safe 100:226–32CrossRefGoogle Scholar
  18. Khan S, Hesham AE, Qiao M, Rehman S, He J (2010) Effect of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res 17:288–96CrossRefGoogle Scholar
  19. Kremen C, Ostfeld RS (2005) A call to ecologists: measuring, analyzing, and managing ecosystem services. Front Ecol Environ 3:540–8CrossRefGoogle Scholar
  20. Kumar M, Kaur PP, Granjewala D (2008) Isolation of periplasmic alkaline phosphatase from Rhizobium bacteria. Res J Microbiol 3:157–62CrossRefGoogle Scholar
  21. Kumar R, Nongkhlaw M, Acharya C, Joshi SR (2013) Uranium (U) tolerant bacterial diversity from U ore deposit of Domiasiat in North-east India and its prospective utilization in bioremediation. Microbes Environ 28:33–41CrossRefGoogle Scholar
  22. Madejón E, Burgos P, López R, Cabrera F (2001) Soil enzymatic response to addition of heavy metals with organic residues. Biol Fert Soils 34:144–50CrossRefGoogle Scholar
  23. MoEW (Ministry of Environment and Water) (2008) Ordinance 3: Bulgarian limit values of harmful substances in soils Available at: http://www.moew.government.bg/ (in bulgarian)
  24. Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soils. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action, vol 26, Biological Processes in Soil Phosphorus Cycling, Series: Soil Biology, Springer–Verlag Berlin Heidelberg., pp 215–44CrossRefGoogle Scholar
  25. Olsen SR (1982) Phosphorus. In: Page AL, Miller RH, Keeney D (eds) Methods of soil analysis, part 2. Agronomy Monograph, Soil Sci Soc Am, Madison, WI, pp 1040–2Google Scholar
  26. Palmer MA, Bernhardt E, Chornesky E et al (2004) Ecology for a crowded planet. Science 304:1251–2CrossRefGoogle Scholar
  27. Pan J, Yu L (2011) Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecol Eng 37:1889–94CrossRefGoogle Scholar
  28. Powers LG, Mills HJ, Palumbo AV, Zhang CL, Delaney K, Sobecky PA (2002) Introduction of a plasmid-encoded phoA gene for constitutive overproduction of alkaline phosphatase in three subsurface Pseudomonas isolates. FEMS Microbiol Ecol 41:115–23CrossRefGoogle Scholar
  29. Radeva G, Kenarova A, Bachvarova V, Flemming K, Popov I, Vassilev D, Selenska-Pobell S (2013) Bacterial diversity at abandoned uranium mining and milling sites in Bulgaria as revealed by 16S rRNA genetic diversity study. Water Air Soil Poll 224:1748CrossRefGoogle Scholar
  30. Roy S, Bhattacharyya P, Ghosh AK (2004) Influence of toxic metals on activity of acid and alkaline phosphatase enzymes in metal-contaminated landfill soils. Aust J Soil Res 42:339–44CrossRefGoogle Scholar
  31. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–69CrossRefGoogle Scholar
  32. Stephen MGD, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800CrossRefGoogle Scholar
  33. Stoyanova T, Traykov I, Yaneva I, Bogoev V (2010) Ecological quality assessment of Luda River, Bulgaria. Natura Montenegrina 9:341–8Google Scholar
  34. Stoyanova T, Traykov I, Yaneva I, Bogoev V (2011) Heavy metals and radionuclides in river impacted by uranium mining, Bulgaria. J Balkan Ecol 14:83–91Google Scholar
  35. Tabatabai MA (1994) Soil enzymes. In: Weaver RW, Angle JS, Bottomley PS (eds) Methods of soil analysis, part 2: microbiological and biochemical properties. Soil Sci Soc Am, Madison, WI, pp 778–833Google Scholar
  36. Tan X, Chang SX, Kabzems R (2008) Soil compaction and forest soil removal reduce microbial biomass and enzyme activities in a boreal aspen forest soil. Biol Fert Soils 44:471–9CrossRefGoogle Scholar
  37. Tejada M, Moreno JL, Hernandez MT, Garcia C (2008) Soil amendments with organic wastes reduce the toxicity of nickel to soil enzyme activities. Eur J Soil Biol 44:129–40CrossRefGoogle Scholar
  38. Topashka-Ancheva M, Мetcheva R, Gerasimova T, Dimitrov K (2010) Murids as a test system to assess environmental influences on genetic apparatus. Scientific conference, Sofia 24 – 25 June 2010, “Biodiversity and Healthy Environment”, Book of Abstracts, pp 86–87Google Scholar
  39. Trevors JT (1984) Dehydrogenase activity in soil: a comparison between INT and TTC assay. Soil Biol Biochem 16:673–4CrossRefGoogle Scholar
  40. Vitousek PM, Harold MA (1997) Human domination of Earth's ecosystems. Science 277:494–9CrossRefGoogle Scholar
  41. Wang YP, Shi J, Wang H, Lin Q, Chen XC, Chen YX (2007) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotox Environ Safe 67:75–81CrossRefGoogle Scholar
  42. Wyszkowska J, Borowik A, Kucharski J, Baćmaga M, Tomkiel M, Boros-Lajszner E (2013) The effect of organic fertilizers on the biochemical properties of soil contaminated with zinc. Plant Soil Environ 59:500–4Google Scholar
  43. Yuan B, Yue D (2012) Soil microbial and enzymatic activities across a chronosequence of Chinese pine plantation development on the loess plateau of China. Pedosphere 22:1–12CrossRefGoogle Scholar
  44. Yung MC, Jiao Y (2014) Biomineralization of uranium by PhoY phosphatase activity aids cell survival in Caulobacter crescentus. Appl Environ Microbiol 80:4795–804CrossRefGoogle Scholar
  45. Zhang X, Li F, Liu T, Xu C, Duan D, Peng C, Zhu S, Shi J (2013) The variations in the soil enzyme activity, protein expression, microbial biomass, and community structure of soil contaminated by heavy metals. ISRN Soil Sci Article ID 803150, doi: 10.1155/2013/803150

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Silvena Boteva
    • 1
  • Galina Radeva
    • 2
  • Ivan Traykov
    • 1
  • Anelia Kenarova
    • 1
    Email author
  1. 1.Faculty of BiologySofia University “St. Kl. Ohridski”SofiaBulgaria
  2. 2.Institute of Molecular Biology, Bulgarian Academy of SciencesSofiaBulgaria

Personalised recommendations