Skip to main content

Effect of long-term industrial waste effluent pollution on soil enzyme activities and bacterial community composition

Abstract

Although numerous studies have addressed the influence of exogenous pollutants on microorganisms, the effect of long-term industrial waste effluent (IWE) pollution on the activity and diversity of soil bacteria was still unclear. Three soil samples characterized as uncontaminated (R1), moderately contaminated (R2), and highly contaminated (R3) receiving mixed organic and heavy metal pollutants for more than 20 years through IWE were collected along the Mahi River basin, Gujarat, western India. Basal soil respiration and in situ enzyme activities indicated an apparent deleterious effect of IWE on microbial activity and soil function. Community composition profiling of soil bacteria using 16S rRNA gene amplification and denaturing gradient gel electrophoresis (DGGE) method indicated an apparent bacterial community shift in the IWE-affected soils. Cloning and sequencing of DGGE bands revealed that the dominated bacterial phyla in polluted soil were affiliated with Firmicutes, Acidobacteria, and Actinobacteria, indicating that these bacterial phyla may have a high tolerance to pollutants. We suggested that specific bacterial phyla along with soil enzyme activities could be used as relevant biological indicators for long-term pollution assessment on soil quality.

Bacterial community profiling and soil enzyme activities in long-term industrial waste effluent polluted soils

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

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

References

  1. Alef, K., & Nannipieri, P. (1995). Methods in applied soil microbiology and biochemistry. London: Academic Press.

    Google Scholar 

  2. Bishnoi, K., Sain, U., Kumar, R., Singh, R., & Bishnoi, N. R. (2009). Distribution and biodegradation of polycyclic aromatic hydrocarbons in contaminated sites of Hisar (India). Indian Journal of Experimental Biology, 47, 210–217.

    CAS  Google Scholar 

  3. Bordenave, S., Goñi-Urriza, M. S., Caumette, P., & Duran, R. (2007). Effects of heavy fuel oil on the bacterial community structure of a pristine microbial mat. Applied and Environmental Microbiology, 73, 6089–6097.

    CAS  Article  Google Scholar 

  4. Colin, V. L., Villegas, L. B., & Abate, C. M. (2012). Indigenous microorganisms as potential bioremediators for environments contaminated with heavy metals. International Biodeterioration and Biodegradation, 69, 28–37.

    CAS  Article  Google Scholar 

  5. Cycoń, M., & Piotrowska-Seget, Z. (2015). Biochemical and microbial soil functioning after application of the insecticide imidacloprid. Journal of Environmental Sciences, 27, 147–158.

    Article  Google Scholar 

  6. Fließbach, A., Martens, R., & Reber, H. H. (1994). Soil microbial biomass and microbial activity in soil treated with heavy metal contaminated biosolids. Soil Biology and Biochemistry, 26, 1201–1205.

    Article  Google Scholar 

  7. Gil-Sotres, F., Trasar-Cepeda, C., Leirós, M. C., & Seoane, S. (2005). Different approaches to evaluating soil quality using biochemical properties. Soil Biology and Biochemistry, 37, 877–887.

    CAS  Article  Google Scholar 

  8. Gremion, F., Chatzinotas, A., & Harms, H. (2003). Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal contaminated bulk and rhizosphere soil. Environmental Microbiology, 5, 896–907.

    CAS  Article  Google Scholar 

  9. Hendrickx, B., Dejonghe, W., Boënne, W., Brennerova, M., Cernik, M., Lederer, T., et al. (2005). Dynamics of an oligotrophic bacterial aquifer community during contact with a groundwater plume contaminated with benzene, toluene, ethylbenzene and xylenes: an in situ mesocosm study. Applied and Environmental Microbiology, 71, 3815–3825.

    CAS  Article  Google Scholar 

  10. Igbinosa, E. O. (2015). Effect of cassava mill effluent on biological activity of soil microbial community. Environmental Monitoring and Assessment, 187, 418. doi:10.1007/s10661-015-4651-y.

    Article  Google Scholar 

  11. Janssen, P. H. (2006). Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Applied and Environmental Microbiology, 72, 1719–1728.

    CAS  Article  Google Scholar 

  12. Jones, S. E., & Lennon, J. T. (2010). Dormancy contributes to the maintenance of microbial diversity. Proceedings of the National Academy of Sciences of the United States of America, 107, 5881–5886.

    CAS  Article  Google Scholar 

  13. Keshri, J., Mankazana, B. B., & Momba, M. N. (2014). Profile of bacterial communities in South African mine-water samples using Illumina next-generation sequencing platform. Applied Microbiology and Biotechnology, 99, 3233–3242.

    Article  Google Scholar 

  14. Khan, S., Cao, Q., Hesham, A. E. L., Xia, Y., & He, J. Z. (2007). Soil enzymatic activities and microbial community structure with different application rates of Cd and Pb. Journal of Environmental Sciences, 19, 834–840.

    CAS  Article  Google Scholar 

  15. Labunska, I., Stephenson, A., Brigden, K., Santillo, D., Stringer, R., Johnston, P.A., & Ashton, J. M. (1999). Organic and heavy metal contaminants in samples taken at three industrial estates in Gujarat, India. Green Peace Research Laboratories, Netherlands. Technical Note 05/99. (http://www.greenpeace.org/international/Global/international/planet2/report/1999/11/toxichotspots-a-greenpeace.pdf/).

  16. Liao, M., Xie, X., Ma, A., & Peng, Y. (2010). Different influences of cadmium on soil microbial activity and structure with Chinese cabbage cultivated and non-cultivated. Journal of Soils and Sediments, 10, 818–826.

    CAS  Article  Google Scholar 

  17. Nakatsu, C. H., Carmosini, N., Baldwin, B., Kourtev, P., Konopka, A., Nakatsu, C. H., et al. (2005). Soil microbial community responses to additions of organic carbon substrates and heavy metals (Pb and Cr). Applied and Environmental Microbiology, 71, 7679–7689.

    CAS  Article  Google Scholar 

  18. Popp, N., Schlömann, M., & Mau, M. (2006). Bacterial diversity in the active stage of a bioremediation system for mineral oil hydrocarbon-contaminated soils. Microbiology, 152, 3291–3304.

    CAS  Article  Google Scholar 

  19. Qu, J., Ren, G., Chen, B., Fan, J., & Yong, E. (2011). Effects of lead and zinc mining contamination on bacterial community diversity and enzyme activities of vicinal cropland. Environmental Monitoring and Assessment, 182, 597–606.

    CAS  Article  Google Scholar 

  20. Schlesinger, W. H., & Andrews, J. A. (2000). Soil respiration and global carbon cycle. Biogeochemistry, 48, 7–20.

    CAS  Article  Google Scholar 

  21. Sheik, C. S., Mitchell, T. W., Rizvi, F. Z., Rehman, Y., Faisal, M., et al. (2012). Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PloS One, 7, e40059.

    CAS  Article  Google Scholar 

  22. Shen, J. P., Zhang, L. M., Zhu, Y. G., Zhang, J. B., & He, J. Z. (2008). Abundance and composition of ammonia-oxidizing bacteria and ammonia oxidizing archaea communities of an alkaline sandy loam. Environmental Microbiology, 10, 1601–1611.

    CAS  Article  Google Scholar 

  23. Subrahmanyam, G., Archana, G., & Chamyal, L. S. (2011). Microbial activity and diversity in the late Pleistocene palaeosols of alluvial Mahi River basin, Gujarat, western India. Current Science India, 101, 202–209.

    CAS  Google Scholar 

  24. Subrahmanyam, G., Hu, H. W., Zheng, Y. M., Archana, G., He, J. Z., & Liu, Y. R. (2014a). Response of ammonia oxidizing microbes to the stresses of arsenic and copper in two acidic alfisols. Applied Soil Ecology, 77, 59–67.

    Article  Google Scholar 

  25. Subrahmanyam, G., Khonde, N., Maurya, D. M., Chamyal, L. S., & Archana, G. (2014b). Microbial activity and culturable bacterial diversity in the sediments of Great Rann of Kutch, a unique ecosystem, Western India. Pedosphere, 24, 45–55.

    Article  Google Scholar 

  26. Subrahmanyam, G., Shen, J. P., Liu, Y. R., Archana, G., & He, J. Z. (2014c). Response of ammonia-oxidizing archaea and bacteria to long-term industrial effluent-polluted soils, Gujarat, Western India. Environmental Monitoring and Assessment, 186, 4037–4050.

    CAS  Article  Google Scholar 

  27. Tabatabai, M. A. (1994). Soil enzymes. In R.W. Weaver et al. (Eds.), Methods of soil analysis: microbiological and biochemical properties. Part 2. SSSA Book Ser. 5. Soil Sci Soc Am. Madison, pp. 775–834.

  28. Thavamani, P., Malik, S., Beer, M., Megharaj, M., & Naidu, R. (2012). Microbial activity and diversity in long-term mixed contaminated soils with respect to polyaromatic hydrocarbons and heavy metals. Journal of Environmental Management, 99, 10–17.

    CAS  Article  Google Scholar 

  29. Tian, Y., Liu, H. J., Zheng, T. L., Kwon, K. K., Kim, S. J., & Yan, C. L. (2008). PAHs contamination and bacterial communities in mangrove surface sediments of the Jiulong River Estuary, China. Marine Pollution Bulletin, 57, 707–715.

    CAS  Article  Google Scholar 

  30. U.S. EPA (1996) Method 3540C, Soxhlet extraction. <http://www.epa.gov/osw/hazard/testmethods/sw846/pdfs/3540c.pdf (14.03.14).

  31. Vance, E. D., Brookes, P. C., & Jenkinson, D. S. (1987). An extraction method for measuring microbial biomass C. Soil Biology and Biochemistry, 19, 703–707.

    CAS  Article  Google Scholar 

  32. Vivas, A., Moreno, B., del Val, C., Macci, C., Masciandaro, G., & Benitez, E. (2008). Metabolic and bacterial diversity in soils historically contaminated by heavy metals and hydrocarbons. Journal of Environmental Monitoring, 10, 1287–1296.

    CAS  Article  Google Scholar 

  33. Wang, Y. P., Shi, J. Y., Lin, Q., Chen, X. C., & Chen, Y. X. (2007). Heavy metal availability and impact on activity of soil microorganisms along a Cu/Zn contamination gradient. Journal of Environmental Sciences, 19, 848–853.

    CAS  Article  Google Scholar 

  34. Winding, A., Hund-Rinke, K., & Rutgers, M. (2005). The use of microorganisms in ecological soil classification and assessment concepts. Ecotoxicology and Environmental Safety, 62, 230–248.

    CAS  Article  Google Scholar 

  35. Yu, Z., & Morrison, M. (2004). Comparisons of different hypervariable regions of rrs genes for use in fingerprinting of microbial communities by PCR-denaturing gradient gel electrophoresis. Applied and Environmental Microbiology, 70, 4800–4806.

    CAS  Article  Google Scholar 

  36. Zhang, F. P., Li, C. F., Tong, L. G., Yue, L. X., Li, P., Ciren, Y. J., & Cao, C. G. (2010a). Response of microbial characteristics to heavy metal pollution of mining soils in central Tibet, China. Applied Soil Ecology, 45, 144–151.

    Article  Google Scholar 

  37. Zhang, W., Wang, H., Zhang, R., Yu, X. Z., Qian, P. Y., & Wong, M. H. (2010b). Bacterial communities in PAH contaminated soils at an electronic-waste processing center in China. Ecotoxicology, 19, 96–104.

    CAS  Article  Google Scholar 

  38. Zhang, Q., Zhu, L., Wang, J., Xie, H., Wang, J., Wang, F., & Sun, F. (2014). Effects of fomesafen on soil enzyme activity, microbial population, and bacterial community composition. Environmental Monitoring and Assessment, 186, 2801–2812.

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was funded by the Chinese Academy of Sciences (CAS), Beijing, China, and Academy of Sciences for the Developing World (TWAS), Trieste, Italy, under the scheme “TWAS-CAS fellowship programme for postgraduate research” to GS for the year 2010. This work was jointly supported by the National Natural Science Foundation of China (Grant No. 41322007) and the Foundation for Innovative Research Groups of the National Natural Science Foundation of China (Grant No. 51221892).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Li-Mei Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOC 28 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Subrahmanyam, G., Shen, JP., Liu, YR. et al. Effect of long-term industrial waste effluent pollution on soil enzyme activities and bacterial community composition. Environ Monit Assess 188, 112 (2016). https://doi.org/10.1007/s10661-016-5099-4

Download citation

Keywords

  • Industrial waste effluent
  • Long-term pollution
  • Soil enzyme activity
  • 16S rRNA gene
  • Denaturing gradient gel electrophoresis
  • Biological indicators