Skip to main content
SpringerLink
Log in

Changes in Microbial Functional Diversity and Activity in Paddy Soils Irrigated with Industrial Wastewaters in Bandung, West Java Province, Indonesia

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Characteristics, such as microbial biomass, basal respiration, and functional diversity of the microbial communities, were investigated in paddy soils located in Bandung, West Java Province, Indonesia, that have been heavily polluted by industrial effluents for 31 years. Paddy soil samples (10–20 cm) were taken from two sites: polluted soils and unpolluted soils (as control sites). The polluted soils contained higher salinity, higher sodicity, higher nutrient contents, and elevated levels of heavy metals (Cr, Mn, Ni, Cu, and Zn) than unpolluted soils. Soil physicochemical properties, such as maximum water holding capacity, exchangeable sodium percentage, sodium adsorption ratio, and swelling factor, in polluted soils were much greater than those in unpolluted soils (P < 0.05). Changes in the physical and chemical soil properties were reflected by changes in the microbial communities and their activities. BIOLOG analysis indicated that the functional diversity of the microbial community of polluted soils increased and differed from that of unpolluted soils. Likewise, the average rate of color development (average well color development), microbial biomass (measured as DNA concentration), and the soil CO2 respiration were higher in polluted soils. These results indicate that major changes in the chemical and physical properties of paddy soils following the application of industrial wastewater effluents have had lasting impacts on the microbial communities of these soils. Thus, the increased activity, biomass, and functional diversity of the microbial communities in polluted soils with elevated salinity, sodicity, and heavy metal contents may be a key factor in enhancing the bioremediation process of these heavily polluted paddy soils.

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

Similar content being viewed by others

References

  • Agnelli, A., Ascher, J., Corti, G., Ceccherini, M. T., Nannipieri, P., & Pietramellara, G. (2004). Distribution of microbial communities in a forest soil profile investigated by microbial biomass, soil respiration and DGGE of total and extracellular DNA. Soil Biology & Biochemistry, 36, 859–868.

    Article  CAS  Google Scholar 

  • Anderson, J. P. E., & Domsch, K. H. (1973). Quantification of bacterial and fungal contributions to soil respiration. Archives of Microbiology, 93, 113–127.

    CAS  Google Scholar 

  • Bååth, E., Diaz-Ravina, M., Frostegård, Å., & Campbell, C. D. (1998). Effect of metal-rich sludge amendments on the soil microbial community. Applied and Environmental Microbiology, 64, 238–245.

    Google Scholar 

  • Bossio, D. A., & Scow, K. M. (1995). Impact of carbon and flooding on the metabolic diversity of microbial communities in soils. Applied and Environmental Microbiology, 61, 4043–4050.

    CAS  Google Scholar 

  • Bossio, D. A., & Scow, K. M. (1998). Impacts of carbon and flooding on soil microbial communities: Phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology, 35, 265–278.

    Article  CAS  Google Scholar 

  • Chaerun, S. K., Tazaki, K., Asada, R., & Kogure, K. (2004a). Bioremediation of coastal areas 5 years after the Nakhodka oil spill in the Sea of Japan: Isolation and characterization of hydrocarbon-degrading bacteria. Environment International, 30, 911–922.

    Article  CAS  Google Scholar 

  • Chaerun, S. K., Tazaki, K., Asada, R., & Kogure, K. (2004b). Alkane-degrading bacteria and heavy metals from the Nakhodka oil spill-polluted seashores in the Sea of Japan after five years of bioremediation. The Science Reports of Kanazawa University, 49, 25–46.

    Google Scholar 

  • Chaerun, S. K., Asada, R., & Tazaki, K. (2007). Biodegradation of heavy oil from the Nakhodka oil spill by indigenous microbial consortia. International Journal of Applied Environmental Sciences, 2, 19–30.

    Google Scholar 

  • Chang, S. X., Preston, C. M., & Weetman, G. F. (1995). Soil microbial biomass and microbial and mineralizable N in a clear-cut chronosequence on northern Vancouver Island, British Columbia. Canadian Journal of Forest Research, 25, 1595–1607.

    Article  Google Scholar 

  • De Leij, F. A. A. M., Whipps, J. M., & Lynch, J. M. (1993). The use of colony development for the characterization of bacterial communities in soil and roots. Microbial Ecology, 27, 81–97.

    Google Scholar 

  • Dick, R. P. (1992). A review: Long-term effects of agricultural systems on soil biochemical and microbial parameters. Agriculture, Ecosystems & Environment, 40, 25–36.

    Article  CAS  Google Scholar 

  • DIN ISO 38414-S (1983). Deutsche Einheitsverfahren zur Wasser-, Abwasser-, und Schlammuntersuchung; Schlamm und Sediment. Beuth, Berlin, Wien, and Zurich.

  • DIN ISO 10694 (1996). Bodenbeschaffenheit—Bestimmung von organischem Kohlenstoff und Gesamtkohlenstoff nach trockener Verbrennung (Elementaranalyse). Beuth, Berlin, Vienna, Zurich.

  • DIN ISO 10390 (1997a). Bestimmung des pH-Wertes. Beuth, Berlin, Vienna, Zurich.

  • DIN ISO 13536 (1997b). Bestimmung der potentiellen Kationen-austauschkapazität und Basensätigung. Beuth, Berlin, Vienna, Zurich.

  • DIN ISO 13878 (1998). Bodenbeschaffenheit—Bestimmung des Gesamt-Stickstoffs durch trockene Verbrennung (Elementaranalyse). Beuth, Berlin, Vienna, Zurich.

  • Eweis, J. B., Ergas, S. J., Chang, D. P. Y., & Schroeder, E. D. (1998). Bioremediation principles. Boston: McGraw-Hill.

    Google Scholar 

  • Garcia, C., & Hernandez, T. (1996). Influence of salinity on the biological and biochemical activity of a calciothid soil. Plant and Soil, 178, 255–263.

    Article  CAS  Google Scholar 

  • Garland, J. L. (1996). Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biology & Biochemistry, 28, 213–221.

    Article  CAS  Google Scholar 

  • Geological Research and Development Centre of Indonesia (2003). Geological map of the Bandung Quadrangle, Jawa, Bandung, Indonesia.

  • Guggenberger, G., & Haider, K. M. (2002). Effect of mineral colloids on biogeochemical cycling of C, N, P and S in soil. In P. M. Huang, J.-M. Bollag, & N. Senesi (Eds.), Interactions between soil particles and microorganisms: impact on the terrestrial ecosystem (pp. 267–321). New York: Wiley.

    Google Scholar 

  • Hasebe, A., Kanazawa, S., & Takai, Y. (1984). Microbial biomass in paddy soil. I. Microbial biomass calculated from direct count using fluorescence microscope. Soil Science and Plant Nutrition, 30, 175–187.

    Google Scholar 

  • Hengstmann, U., Chin, K.-J., Janssen, P. H., & Liesack, W. (1999). Comparative phylogenetic assignment of environmental sequences of genes encoding 16 S rRNA and numerically abundant culturable bacteria from an anoxic rice paddy soil. Applied and Environmental Microbiology, 65, 5050–5058.

    CAS  Google Scholar 

  • Kaiser, E.-A., Mueller, T., Joergensen, R. G., Insam, H., & Heinimeyer, O. (1992). Evaluation of methods to estimate the soil microbial biomass and the relationship with soil texture and organic matter utilization. Soil Biology & Biochemistry, 24, 675–683.

    Article  CAS  Google Scholar 

  • Kandeler, E., Kampichler, C., & Horak, O. (1996). Influence of heavy metals on the functional diversity of soil microbial communities. Biology and Fertility of Soils, 23, 299–306.

    Article  CAS  Google Scholar 

  • Keren, R. (2000). Salinity. In M. E. Sumner (Ed.), Handbook of soil science (pp. G3–G26). Boca Raton: CRC Press LLC.

    Google Scholar 

  • Kong, W.-D., Zhu, Y.-G., Fu, B.-J., Marschner, P., & He, J.-Z. (2006). The veterinary antibiotic oxytetracycline and Cu influence functional diversity of the soil microbial community. Environmental Pollution, 143, 129–137.

    Article  CAS  Google Scholar 

  • Leckie, S. E., Prescott, C. E., Grayston, S. J., Neufeld, J. D., & Mohn, W. W. (2004). Comparison of chloroform fumigation-extraction, phospholipid fatty acid, and DNA methods to determine microbial biomass in forest humus. Soil Biology & Biochemistry, 36, 529–532.

    Article  CAS  Google Scholar 

  • Lefebvre, O., & Moletta, R. (2006). Treatment of organic pollution in industrial saline wastewater: A literature review. Water Research, 40, 3671–3682.

    Article  CAS  Google Scholar 

  • Levy, G. J. (2000). Sodicity. In M. E. Sumner (Ed.), Handbook of soil science (pp. G27–G63). Boca Raton: CRC Press LLC.

    Google Scholar 

  • Li, Q., Allen, H. L., & Wollum, A. G., II. (2004). Microbial biomass and bacterial functional diversity in forest soils: Effects of organic matter removal, compaction, and vegetation control. Soil Biology & Biochemistry, 36, 571–579.

    Article  CAS  Google Scholar 

  • Liu, B., Tu, C., Hu, S., Gumpertz, M., & Ristaino, J. B. (2007). Effect of organic, sustainable and conventional management strategies in grower fields on soil physical, chemical, and biological factors and the incidence of Southern blight. Applied Soil Ecology, 37, 202–214.

    Article  Google Scholar 

  • Liu, M., Hu, F., Chen, X., Huang, Q., Jiao, J., Zhang, B., et al. (2009). Organic amendments with reduced chemicall fertilizer promote soil microbial development and nutrient availability in a subtropical paddy field: The influence of quantity, type and application time of organic amendments. Applied Soil Ecology, 42, 166–175.

    Article  Google Scholar 

  • Liu, Z., Fu, B., Zheng, X., & Liu, G. (2010). Plant biomass, soil water content and soil N:P ratio regulating soil microbial functional diversity in a temperate steppe: A regional scale study. Soil Biology & Biochemistry, 42, 445–450.

    Article  CAS  Google Scholar 

  • Lorenz, N., Hintemann, T., Kramarewa, T., Katayama, A., Yasuta, T., Marschner, P., et al. (2006). Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure. Soil Biology & Biochemistry, 38, 1430–1437.

    Article  CAS  Google Scholar 

  • Lu, Y., Watanabe, A., & Kimura, M. (2002). Contribution of plant-derived carbon to soil microbial biomass dynamics in a paddy rice microcosm. Biology and Fertility of Soils, 36, 136–142.

    Article  CAS  Google Scholar 

  • Mamedov, A. I., & Levy, G. L. (2001). Clay dispersivity and aggregates stability effects on seal formation and erosion in effluent-irrigated soils. Soil Science, 166, 631–639.

    Article  CAS  Google Scholar 

  • Marstorp, H., & Witter, E. (1999). Extractable dsDNA and product formation as measurement of microbial growth in soil upon substrate addition. Soil Biology and Biochemistry, 31, 1443–1453.

    Article  CAS  Google Scholar 

  • McLean, J. S., Lee, J.-U., & Beveridge, T. J. (2002). Interactions of bacteria and environmental metals, fine-grained mineral development, and bioremediation strategies. In P. M. Huang, J.-M. Bollag, & N. Senesi (Eds.), Interactions between soil particles and microorganisms: impact on the terrestrial ecosystem (pp. 227–261). New York: Wiley.

    Google Scholar 

  • Menneer, J. C., McLay, C. D. A., & Lee, R. (2001). Effects of sodium-contaminated wastewater on soil permeability of two New Zealand soils. Australian Journal of Soil Research, 39, 877–891.

    Article  CAS  Google Scholar 

  • Nannipieri, P., Ascher, J., Ceccherini, M. T., Landi, L., Pietramellara, G., & Renella, G. (2003). Microbial diversity and soil functions. European Journal of Soil Science, 54, 655–670.

    Article  Google Scholar 

  • Richter, D., & Markewitz, D. (1995). How deep is soil? BioScience, 45, 600–609.

    Article  Google Scholar 

  • Rietz, D. N., & Haynes, R. J. (2003). Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biology & Biochemistry, 35, 845–854.

    Article  CAS  Google Scholar 

  • Sandaa, R.-A., Torsvik, V., & Enger, Ø. (2001). Influence of long-term heavy metal contamination on microbial communities in soil. Soil Biology & Biochemistry, 33, 287–295.

    Article  CAS  Google Scholar 

  • Sardinha, M., Muller, T., Schmeisky, H., & Joergensen, R. G. (2003). Microbial performance in soils along a salinity gradient under acidic conditions. Applied Soil Ecology, 23, 237–244.

    Article  Google Scholar 

  • Singh, Y., Singh, B., & Timsina, J. (2005). Crop residue management for nutrient cycling and improving soil productivity in rice-based cropping systems in the tropics. Advances in Agronomy, 85, 269–407.

    Article  CAS  Google Scholar 

  • Sparling, G. P., Hart, P. B. S., August, J. A., & Leslie, D. M. (1994). A comparison of soil and microbial carbon, nitrogen, and phosphorous contents, and macro-aggregate stability of a soil under native forest and after clearance for pastures and plantation forest. Biology and Fertility of Soils, 17, 91–100.

    Article  CAS  Google Scholar 

  • Sumner, M. E. (1993). Sodic soils: New perspectives. Australian Journal of Soil Research, 31, 683–750.

    Article  Google Scholar 

  • Toyota, K., Ritz, K., & Young, I. M. (1996). Survival of bacterial and fungal populations following chloroform-fumigation: Effects of soil matrix potential and bulk density. Soil Biology & Biochemistry, 28, 1545–1547.

    Article  CAS  Google Scholar 

  • Violante, A., Khrishnamurti, G. S. R., & Huang, P. M. (2002). Impact of organic substances on the formation and transformation of metal oxides in soil environments. In P. M. Huang, J.-M. Bollag, & N. Senesi (Eds.), Interactions between soil particles and microorganisms: impact on the terrestrial ecosystem (pp. 133–188). New York: Wiley.

    Google Scholar 

  • Wada, S., & Toyota, K. (2007). Repeated applications of farmyard manure enhance resistance and resilience of soil biological functions against soil disinfection. Biology and Fertility of Soils, 43, 349–356.

    Article  Google Scholar 

  • Yao, H., He, Z., Wilson, M. J., & Campbell, C. D. (2000). Microbial biomass and community structure in a sequence of soils with increasing fertility and changing land use. Microbial Ecology, 40, 223–237.

    CAS  Google Scholar 

  • Yao, H., Xu, J., & Huang, C. (2003). Substrate utilization pattern, biomass and activity of microbial communities in a sequence of heavy metal-polluted paddy soils. Geoderma, 115, 139–148.

    Article  CAS  Google Scholar 

  • Yuan, B.-C., Xu, X.-G., Li, Z.-Z., Gao, T.-P., Gao, M., Fan, X.-W., et al. (2007). Microbial biomass and activity in alkalized magnesic soils under arid conditions. Soil Biology & Biochemistry, 39, 3004–3013.

    Article  CAS  Google Scholar 

  • Zhang, Y., Liu, S., & Ma, J. (2006). Water-holding capacity of ground covers and soils in alphine and sub-alpine shrubs in western Sichuan, China. Acta Ecologica Sinica, 26, 2775–2781.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the IA-ITB (Ikatan Alumni Institut Teknologi Bandung), Indonesia. We are grateful to the ZALF Central Laboratory, Germany, for soil chemical analysis, and all the students of the Toyota laboratory for their assistance and cooperation. We also thank the anonymous reviewers for their constructive comments. SKC would like to express her thanks for the fellowship provided by the IDB during her postdoctoral research at the Department of Microbiology, University of Georgia, USA (2008-2009).

Author information

Authors and Affiliations

  1. School of Life Sciences and Technology, Institut Teknologi Bandung, Ganesha 10, Bandung, 40132, West Java, Indonesia

    Siti Khodijah Chaerun

  2. Centre for Life Sciences, Institut Teknologi Bandung, Ganesha 10, Bandung, 40132, West Java, Indonesia

    Nurmi P. D. Pangesti

  3. Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Koganei, Tokyo, 184-8588, Japan

    Koki Toyota

  4. Department of Microbiology, University of Georgia, Athens, GA, 30602, USA

    William B. Whitman

Authors
  1. Siti Khodijah Chaerun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nurmi P. D. Pangesti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Koki Toyota
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. William B. Whitman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Siti Khodijah Chaerun.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chaerun, S.K., Pangesti, N.P.D., Toyota, K. et al. Changes in Microbial Functional Diversity and Activity in Paddy Soils Irrigated with Industrial Wastewaters in Bandung, West Java Province, Indonesia. Water Air Soil Pollut 217, 491–502 (2011). https://doi.org/10.1007/s11270-010-0603-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-010-0603-x

Keywords

Search

Navigation