Abstract
Pseudomonas sp. strain WBC-3 mineralizes the priority pollutant para-nitrophenol (PNP) and releases nitrite (NO2 −), which is probably involved in the nitrification. In this study, the rate of PNP removal in soil bioaugmented with strain WBC-3 was more accelerated with more NO2 − accumulation than in uninoculated soils. Strain WBC-3 survived well and remained stable throughout the entire period. Real-time polymerase chain reaction (real-time PCR) indicated a higher abundance of ammonia-oxidizing bacteria (AOB) than ammonia-oxidizing archaea (AOA), suggesting that AOB played a greater role in nitrification in the original sampled soil. Real-time PCR and multivariate analysis based on the denaturing gradient gel electrophoresis showed that PNP contamination did not significantly alter the abundance and community structure of ammonia oxidizers except for inhibiting the AOB abundance. Bioaugmentation of PNP-contaminated soil showed a significant effect on AOB populations and community structure as well as AOA populations. In addition, ammonium (NH4 +) variation was found to be the primary factor affecting the AOB community structure, as determined by the correlation between the community structures of ammonia oxidizers and environmental factors. It is here proposed that the balance between archaeal and bacterial ammonia oxidation could be influenced significantly by the variation in NH4 + levels as caused by bioaugmentation of contaminated soil by a pollutant containing nitrogen.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abell GCJ, Banks J, Ross DJ, Keane JP, Robert SS, Revill AT, Volkman JK (2011) Effects of estuarine sediment hypoxia on nitrogen fluxes and ammonia oxidizer gene transcription. FEMS Microbiol Ecol 75:111–122. doi:10.1111/j.1574-6941.2010.00988.x
Avrhami S, Conrad R (2003) Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Appl Environ Microbiol 69:6152–6164. doi:10.1128/aem. 69.10.6152-6164.2003
Bouchez T, Patureau D, Dabert P, Juretschko S, Dore J, Delgenes P, Moletta R, Wagner M (2000) Ecological study of a bioaugmentation failure. Environ Microbiol 2:179–190. doi:10.1046/j.1462-2920.2000.00091.x
Chi XQ, Zhang JJ, Zhao S, Zhou NY (2013) Bioaugmentation with a consortium of bacterial nitrophenol-degraders for remediation of soil contaminated with three nitrophenol isomers. Environ Pollut 172:33–41. doi:10.1016/j.envpol.2012.08.002
Cunliffe M, Kertesz MA (2006) Effect of Sphingobium-yanoikuyae B1 inoculation on bacterial community dynamics and polycyclic aromatic hydrocarbon degradation in aged and freshly PAH-contaminated soils. Environ Pollut 144:228–237. doi:10.1016/j.envpol.2005.12.026
Dechesne A, Pallud C, Bertolla F, Grundmann GL (2005) Impact of the microscale distribution of a Pseudomonas strain introduced into soil on potential contacts with indigenous bacteria. Appl Environ Microbiol 71:8123–8131. doi:10.1128/aem. 71.12.8123-8131.2005
Fawcett JK, Scott JE (1960) A rapid and precise method for the determination of urea. J Clin Pathol 13:156–159. doi:10.1136/jcp.13.2.156
Guo XF, Wang ZH, Zhou SP (2004) The separation and determination of nitrophenol isomers by high-performance capillary zone electrophoresis. Talanta 64:135–139. doi:10.1016/j.talanta.2004.01.020
He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (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 9:2364, 2007. Environ Microbiol 9:3152. doi:10.1111/j.1462-2920.2007.01481.x
Hofferle S, Nicol GW, Pal L, Hacin J, Prosser JI, Mandic-Mulec I (2010) Ammonium supply rate influences archaeal and bacterial ammonia oxidizers in a wetland soil vertical profile. FEMS Microbiol Ecol 74:302–315. doi:10.1111/j.1574-6941.2010.00961.x
Keener WK, Arp DJ (1994) Transformations of aromatic-compounds by nitrosomonas-europaea. Appl Environ Microbiol 60:1914–1920
Keith LH, Telliard WA (1979) Priority pollutants I-A perspective view. Environ Sci Technol 13:416–423. doi:10.1021/es60152a601
Labana S, Pandey G, Paul D, Sharma NK, Basu A, Jain RK (2005) Pot and field studies on bioremediation of p-nitrophenol contaminated soil using Arthrobacter protophormiae RKJ100. Environ Sci Technol 39:3330–3337. doi:10.1021/es0489801
Lessner DJ, Johnson GR, Parales RE, Spain JC, Gibson DT (2002) Molecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765. Appl Environ Microbiol 68:634–641. doi:10.1128/aem. 68.2.634-641.2002
Liu S, Shen L, Lou L, Tian G, Zheng P, Hu B (2013) Spatial distribution and factors shaping the niche segregation of ammonia-oxidizing microorganisms in the Qiantang River, China. Appl Environ Microbiol 79:4065–4071. doi:10.1128/aem. 00543-13
Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979. doi:10.1038/nature08465
McCaig AE, Glover LA, Prosser JI (2001) Numerical analysis of grassland bacterial community structure under different land management regimens by using 16S ribosomal DNA sequence data and denaturing gradient gel electrophoresis banding patterns. Appl Environ Microbiol 67:4554–4559. doi:10.1128/aem. 67.10.4554-4559.2001
McCarty GW (1999) Modes of action of nitrification inhibitors. Biol Fertil Soils 29:1–9. doi:10.1007/s003740050518
Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10:3002–3016. doi:10.1111/j.1462-2920.2008.01764.x
Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16S ribosomal-RNA. Appl Environ Microbiol 59:695–700
Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978. doi:10.1111/j.1462-2920.2008.01701.x
Norman RJ, Edberg JC, Stucki JW (1985) Determination of nitrate in soil extracts by dual wavelength ultraviolet spectrophotometry. Soil Sci Soc Am J 49:1182–1185
Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531. doi:10.1016/j.tim.2012.08.001
Sahan E, Muyzer G (2008) Diversity and spatio-temporal distribution of ammonia-oxidizing Archaea and Bacteria in sediments of the Westerschelde estuary. FEMS Microbiol Ecol 64:175–186. doi:10.1111/j.1574-6941.2008.00462.x
Schwieger F, Tebbe CC (1998) A new approach to utilize PCR-single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol 64:4870–4876
Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611. doi:10.1111/j.1462-2920.2008.01578.x
Singer AC, van der Gast CJ, Thompson IP (2005) Perspectives and vision for strain selection in bioaugmentation. Trends Biotechnol 23:74–77. doi:10.1016/j.tibtech.2004.12.012
Sverdrup LE, Ekelund F, Krogh PH, Nielsen T, Johnsen K (2002) Soil microbial toxicity of eight polycyclic aromatic compounds: effects on nitrification, the genetic diversity of bacteria, and the total number of protozoans. Environ Toxicol Chem 21:1644–1650. doi:10.1897/1551-5028
Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071. doi:10.1038/ismej.2010.191
Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ (2006) Archaeal nitrification in the ocean. PNAS 103:12317–12322. doi:10.1073/pnas.0600756103
Zhang JJ, Liu H, Xiao Y, Zhang XE, Zhou NY (2009) Identification and characterization of catabolic para-nitrophenol 4-monooxygenase and para-benzoquinone reductase from Pseudomonas sp. Strain WBC-3. J Bacteriol 191:2703–2710. doi:10.1128/jb.01566-08
Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045. doi:10.1038/ismej.2011.168
Zhao S, Ramette A, Niu GL, Liu H, Zhou NY (2009) Effects of nitrobenzene contamination and of bioaugmentation on nitrification and ammonia-oxidizing bacteria in soil. FEMS Microbiol Ecol 70:315–323. doi:10.1111/j.1574-6941.2009.00773.x
Acknowledgments
This work is supported by the National Natural Science Foundation of China (21077130).
Conflict of interest
We declare that we have no conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chi, XQ., Liu, K. & Zhou, NY. Effects of bioaugmentation in para-nitrophenol-contaminated soil on the abundance and community structure of ammonia-oxidizing bacteria and archaea. Appl Microbiol Biotechnol 99, 6069–6082 (2015). https://doi.org/10.1007/s00253-015-6462-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-015-6462-z