Abstract
Soil nitrifiers have been showing an important role in assessing environmental pollution as sensitive biomarkers. In this study, the abundance and diversity of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) were investigated in long-term industrial waste effluent (IWE) polluted soils. Three different IWE polluted soils characterized as uncontaminated (R1), moderately contaminated (R2), and highly contaminated (R3) were collected in triplicate along Mahi River basin, Gujarat, Western India. Quantitative numbers of ammonia monooxygenase α-subunit (amoA) genes as well as 16S rRNA genes indicated apparent deleterious effect of IWE on abundance of soil AOA, AOB, bacteria, and archaeal populations. Relatively, AOB was more abundant than AOA in the highly contaminated soil R3, while predominance of AOA was noticed in uncontaminated (R1) and moderately contaminated (R2) soils. Soil potential nitrification rate (PNR) significantly (P < 0.05) decreased in polluted soils R2 and R3. Reduced diversity accompanied by apparent community shifts of both AOB and AOA populations was detected in R2 and R3 soils. AOB were dominated with Nitrosospira-like sequences, whereas AOA were dominated by Thaumarchaeal “group 1.1b (Nitrososphaera clusters).” We suggest that the significant reduction in abundance and diversity AOA and AOB could serve as relevant bioindicators for soil quality monitoring of polluted sites. These results could be further useful for better understanding of AOB and AOA communities in polluted soils.
Similar content being viewed by others
References
Alef, K., & Nannipieri, P. (1995). Methods in applied soil microbiology and biochemistry. London: Academic Press.
Allison, S. D., & Martiny, J. B. H. (2008). Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences of the United States of America, 105, 11512–11519.
Angel, R., Asaf, L., Ronen, Z., & Nejidat, A. (2010). Nitrogen transformations and diversity of ammonia-oxidizing bacteria in a desert ephemeral stream receiving untreated wastewater. Microbial Ecology, 59, 46–58.
Cao, H., Li, M., Hong, Y., & Gu, J. D. (2011). Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment. Systematic and Applied Microbiology, 34, 513–523.
Cao, P., Zhang, L. M., Shen, J. P., Zheng, Y. M., Di, H. J., & He, J. Z. (2012). Distribution and diversity of archaeal communities in selected Chinese soils. FEMS Microbiology and Ecology, 80, 146–158.
CPCB. (1996). Inventories of hazardous waste generation in five districts (Ahmedabad, Vadodara, Bharuch, Surat and Valsad) of Gujarat. Central Pollution Control Board (Ministry of Environment & Forests, Government of India). ISBN 8186396632. http://www.cpcb.nic.in/Publications_Dtls.php?msgid=11.
Erguder, T. H., Boon, N., Wittebolle, L., Marzorati, M., & Verstraete, W. (2009). Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiology and Ecology Reviews, 33, 855–869.
Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E., & Oakley, B. B. (2005). Ubiquity and diversity of ammonia oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America, 102, 14683–14688.
Ge, Y., Zhang, J., Zhang, L., Yang, M., & He, J. (2008). Long-term fertilization regimes affect bacterial community structure and diversity of an agricultural soil in northern China. Journal of Soils and Sediments, 8, 43–50.
Gubry-Rangin, C., Hai, B., Quince, C., Engel, M., Thomson, B. C., James, P., et al. (2011). Niche specialization of terrestrial archaeal ammonia oxidizers. Proceedings of the National Academy of Sciences of the United States of America, 108, 21206–21211.
Hatzenpichler, R. (2012). Diversity, physiology, and niche differentiation of ammonia oxidizing archaea. Applied and Environmental Microbiology, 78, 7501–7510.
Hatzenpichler, R., Lebedeva, E. V., Spieck, E., Stoecker, K., Richter, A., Daims, H., & Wagner, M. (2008). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proceedings of the National Academy of Sciences of the United States of America, 105, 2134–2139.
He, J. Z., Hu, H. W., & Zhang, L. M. (2012). Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biology and Biochemistry, 55, 146–154.
He, J. Z., Shen, J. P., Zhang, L. M., Zhu, Y. G., Zheng, Y. M., Xu, M. G., & Di, H. J. (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. Environmental Microbiology, 9, 2364–2374.
Ibekwe, A. M., Grieve, C. M., & Lyon, S. R. (2003). Characterization of microbial communities and composition in constructed dairy wetland wastewater effluent. Applied and Environmental Microbiology, 69, 5060–5069.
Jin, T., Zhang, T., & Yan, Q. (2010). Characterization and quantification of ammonia-oxidizing archaea (AOA) and bacteria (AOB) in a nitrogen-removing reactor using T-RFLP and qPCR. Applied Microbiology and Biotechnology, 87, 1167–1176.
Kelly, J. J., Policht, K., Grancharova, T., & Hundal, L. S. (2011). Distinct responses in ammonia-oxidizing archaea and bacteria after addition of biosolids to an agricultural soil. Applied and Environmental Microbiology, 77, 6551–6558.
Kemnitz, D., Kolb, S., & Conrad, R. (2005). Phenotypi characterization of Rice Cluster III archaea without prior isolation by applying quantitative polymerase chain reaction to an enrichment culture. Environmental Microbiology, 7, 553–565.
Kowalchuk, G. A., & Stephen, J. R. (2001). Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annual Reviews of Microbiology, 55, 485–529.
Kurola, J., Salkinoja-Salonen, M., Aarnio, T., Hultman, J., & Romantschuk, M. (2005). Activity, diversity and population size of ammonia-oxidising bacteria in oil-contaminated land farming soil. FEMS Microbiology Letters, 250, 33–38.
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
Laverman, A. M., Speksnijder, A. G., Braster, M., Kowalchuk, G. A., Verhoef, H. A., & Van Verseveld, H. W. (2001). Spatiotemporal stability of an ammonia-oxidizing community in a nitrogen-saturated forest soil. Microbial Ecology, 42, 35–45.
Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G. W., et al. (2006). Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature, 442, 806–809.
Li, X., Zhum, Y. G., Cavagnaro, T. R., Chen, M., Sun, J., Chen, X., & Qiao, M. (2009). Do ammonia-oxidizing archaea respond to soil Cu contamination similarly as ammonia-oxidizing bacteria? Plant and Soil, 324, 209–217.
Limpiyakorn, T., Fürhacker, M., Haberl, R., Chodanon, T., Srithep, P., & Sonthiphand, P. (2013). amoA-encoding archaea in wastewater treatment plants: a review. Applied Microbiology and Biotechnology, 97, 1425–1439.
Liu, Y. R., Zheng, Y. M., Shen, J. P., Zhang, L. M., & He, J. Z. (2010). Effects of mercury on the activity and community composition of soil ammonia oxidizers. Environmental Science and Pollution Research, 17, 1237–1244.
Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R., & Stahl, D. A. (2009). Ammonia oxidation kinetics determines niche separation of nitrifying archaea and bacteria. Nature, 461, 976–979.
Marzorati, M., Wittebolle, L., Boon, N., Daffonchi, D., & Verstraete, V. (2008). How to get more out of molecular fingerprints: practical tools for microbial ecology. Environmental Microbiology, 10, 1571–1581.
Mertens, J., Broos, K., Wakelin, S. A., Kowalchuk, G. A., Springael, D., & Smolders, E. (2009). Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. The ISME Journal, 3, 916–923.
Nugroho, R. A., Rolling, W. F. M., Laverman, A. M., & Verhoef, H. A. (2007). Low nitrification rates in acid Scots pine forest soils are due to pH-related factors. Microbial Ecology, 53, 87–97.
Ollivier, J., Wanat, N., Austruy, A., Hitmi, A., Joussein, E., Welzl, G., Munch, J. C., & Schloter, M. (2012). Abundance and diversity of ammonia-oxidizing prokaryotes in the root–rhizosphere complex of Miscanthus × giganteus grown in heavy metal-contaminated soils. Microbial Ecology, 64, 1038–1046.
Papa, S., Bartoli, G., Pellegrino, A., & Fioretto, A. (2010). Microbial activities and trace element contents in an urban soil. Environmental Monitoring and Assessment, 165, 193–203.
Pester, M., Rattei, T., Flechl, S., Gröngröft, A., Richter, A., Overmann, J., et al. (2012). amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environmental Microbiology, 14, 525–539.
Prasad, D., Subrahmanyam, G., & Bolla, K. (2012). Effect of cadmium on abundance and diversity of free living nitrogen fixing Azotobacter spp. Journal of Environmental Science and Technology, 5, 184–191.
Prosser, J. I., & Nicol, G. W. (2008). Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environmental Microbiology, 10, 2931–2941.
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.
Ritz, K., Black, H. I. J., Campbell, C. D., Harris, J. A., & Wood, C. (2009). Selecting biological indicators for monitoring soils: a framework for balancing scientific and technical opinion to assist policy development. Ecological Indicators, 9, 1212–1221.
Rotthauwe, J. H., Witzel, K. P., & Liesack, W. (1997). The ammonia monooxygenase structural gene amoAas a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology, 63, 4704–4712.
Schleper, C., Jurgens, G., & Jonuscheit, M. (2005). Genomic studies of uncultivated archaea. Nature Reviews Microbiology, 3, 479–488.
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.
Shukurov, N., & Pen-mouratov, S. (2009). Soil biogeochemical properties of Angren industrial area, Uzbekistan. Journal of Soils and Sediments, 9, 206–215.
Smolders, E., Brans, K., Coppens, F., & Merckx, R. (2001). Potential nitrification rate as a tool for screening toxicity in metal contaminated soils. Environmental Toxicology and Chemistry, 20, 2469–2474.
Spang, A., Poehlein, A., Offre, P., Zumbrägel, S., Haider, S., Rychlik, N., et al. (2012). The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environmental Microbiology, 14, 3122–3145.
Stefanowicz, A. M., Niklinska, M., & Laskowski, R. (2008). Metals affect soil bacterial and fungal functional diversity differently. Environmental Toxicology and Chemistry, 27, 591–598.
Stephen, J. R., McCaig, A. E., Smith, Z., Prosser, J. I., & Embley, T. M. (1996). Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Applied and Environmental Microbiology, 62, 4147–4154.
Suzuki, M. T., Taylor, L. T., & DeLong, E. F. (2000). Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5I-nuclease assays. Applied and Environmental Microbiology, 66, 4605–4614.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.
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.
Tourna, M., Freitag, T. E., Nicol, G. W., & Prosser, J. I. (2008). Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environmental Microbiology, 10, 1357–1364.
Vasileiadis, S., Coppolecchia, D., Puglisi, E., Balloi, A., Mapelli, F., Hamon, R. E., Daniele, D., & Trevisan, M. (2012). Response of ammonia oxidizing bacteria and archaea to acute zinc stress and different moisture regimes in soil. Microbial Ecology, 64, 1028–1037.
Wang, X., Wen, X., Xia, Y., Hu, M., Zhao, F., & Ding, K. (2012). Ammonia oxidizing bacteria community dynamics in a pilot-scale wastewater treatment plant. PLoS ONE, 7, e36272.
Webster, G., Embley, T. M., & Prosser, J. I. (2002). Grassland management regimens reduce small-scale heterogeneity and species diversity of β-Proteobacterial ammonia oxidizer populations. Applied and Environmental Microbiology, 68, 20–30.
Wells, G. F., Park, H. D., Yeung, C. H., Eggleston, B., Francis, C. A., & Criddle, C. S. (2009). Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environmental Microbiology, 11, 2310–2328.
Wessen, E., & Hallin, S. (2011). Abundance of archaeal and bacterial ammonia oxidizers—possible bioindicator for soil monitoring. Ecological Indicators, 6, 1696–1698.
Xia, Y., Zhu, Y. G., Gu, Q., & He, J. Z. (2007). Does long-term fertilization treatment affect the response of soil ammonia-oxidizing bacterial communities to Zn contamination? Plant and Soil, 301, 245–254.
Yao, H., Campbell, C. D., Chapman, S. J., Freitag, T. E., Nicol, G. W., & Singh, B. K. (2013). Multi-factorial drivers of ammonia oxidizer communities: evidence from a national soil survey. Environmental Microbiology, 15, 2545–2556.
Zhang, L., Hu, H., Shen, J., & He, J. Z. (2011). Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. The ISME Journal, 6, 1032–1045.
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. doi:10.1007/s10661-013-3581-9.
Zhou, Z. F., Zheng, Y. M., Shen, J. P., Zhang, L. M., & He, J. Z. (2011). Response of denitrification genes nirS, nirK, and nosZ to irrigation water quality in a Chinese agricultural soil. Environmental Science and Pollution Research, 18, 1644–1652.
Acknowledgments
This work was supported by the Academy of Sciences for the Developing World (TWAS), Trieste, Italy and Chinese Academy of Sciences (CAS), Beijing, China under the scheme “TWAS-CAS fellowship programme for postgraduate research” to GS for the year 2010. This work was partly supported by the Natural Science Foundation of China (41371265, 41201523).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Subrahmanyam, G., Shen, JP., Liu, YR. et al. Response of ammonia-oxidizing archaea and bacteria to long-term industrial effluent-polluted soils, Gujarat, Western India. Environ Monit Assess 186, 4037–4050 (2014). https://doi.org/10.1007/s10661-014-3678-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10661-014-3678-9