Abstract
The interaction between different volatile organic compounds (VOCs) is a critical issue associated with bioremediation of co-contaminated sites. Contradictory results have been reported on the effects of co-existence of VOCs on biodegradation of each VOC. These contradictions are thought to be caused by inter-study variability in microbial diversity. To examine the effects of co-existing VOCs on biodegradation of each VOC, a series of biodegradation tests were carried out with a microcosm capable of degrading all three VOCs: dichloromethane (DCM), benzene, and toluene. We added different combinations of the VOCs to the microcosm while monitoring VOC concentration and microbial community diversity. Degradation of DCM and benzene was minimally influenced by co-existence of other VOCs; however, degradation of toluene was dramatically enhanced by the co-existence of benzene. Propioniferax was identified in cultures exposed to benzene alone and cultures simultaneously exposed to benzene, toluene, and DCM. Propioniferax was dominant, but prior to this study, it was not known to degrade benzene, toluene, and DCM. In the cultures exposed to only toluene, Rhodanobacter, Mycobacterium, Bradyrhizobium, and Intrasporangium increased during the biodegradation. The former three bacteria increased more rapidly when benzene and DCM were also included. These results suggest that co-existence of benzene and DCM can enhance the activity of Rhodanobacter, Mycobacterium, and Bradyrhizobium and consequently accelerate the degradation of toluene.
Similar content being viewed by others
References
Alexander, M. (1994). Biodegradation and bioremediation. San Diego: Academic Press, Inc.
Alfreider, A., & Vogt, C. (2007). Bacterial diversity and aerobic biodegradation potential in a BTEX-contaminated aquifer. Water, Air, and Soil Pollution, 183, 415–426.
Alvarez, P. J., & Vogel, T. M. (1991). Substrate interactions of benzene, toluene, and para-xylene during microbial degradation by pure cultures and mixed culture aquifer slurries. Applied and Environmental Microbiology, 57, 2981–2985.
Bacosa, H. P., Suto, K., & Inoue, C. (2012). Bacterial community dynamics during the preferential degradation of aromatic hydrocarbons by a microbial consortium. International Biodeterioration & Biodegradation, 74, 109–115.
Bagley, D. M., Lalonde, M., Kaseros, V., Stastiuk, K. E., & Sleep, B. E. (2000). Acclimation of anaerobic systems to biodegrade tetrachloroethene in the presence of carbon tetrachloride and chloroform. Water Research, 34, 171–178.
Bucheli-Witschel, M., Hafner, T., Rüegg, I., & Egli, T. (2009). Benzene degradation by Ralstonia pickettii PKO1 in the presence of the alternative substrate succinate. Biodegradation, 20, 419–431.
Burback, B. L., & Perry, J. J. (1993). Biodegradation and biotransformation of groundwater pollutant mixtures by Mycobacterium vaccae. Applied and Environmental Microbiology, 59, 1025–1029.
Capel, P. D., & Larson, S. J. (1995). A chemodynamic approach for estimating losses of target organic chemicals from water during sample holding time. Chemosphere, 30, 1097–1107.
Cavalca, L., Dell’Amico, E., & Andreoni, V. (2004). Intrinsic bioremediability of an aromatic hydrocarbon-polluted groundwater: diversity of bacterial population and toluene monoxygenase genes. Applied Microbiology and Biotechnology, 64, 576–587.
Clement, B. G., Kehl, L. E., DeBord, K. L., & Kitts, C. L. (1998). Terminal restriction fragment patterns (TRFPs), a rapid, PCR-based method for the comparison of complex bacterial communities. Journal of Microbiological Methods, 31, 135–142.
Deeb, R. A., & Alvarez-Cohen, L. (1999). Temperature effects and substrate interactions during the aerobic biotransformation of BTEX mixtures by toluene-enriched consortia and Rhodococcus rhodochrous. Biotechnology and Bioengineering, 62, 526–536.
R Development Core Team (2015). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
Dunbar, J., Ticknor, L. O., & Kusuke, C. R. (2001). Phylogenetic specificity and reproducibility and new method for analysis of terminal restriction fragment profiles of 16S rRNA genes from bacterial communities. Applied and Environmental Microbiology, 67, 190–197.
Fahy, A., McGenity, T. J., Timmis, K. N., & Ball, A. S. (2006). Heterogeneous aerobic benzene-degrading communities in oxygen-depleted groundwaters. FEMS Microbiology Ecology, 58, 260–270.
Hayaishi, O., Katagiri, M., & Rothberg, S. (1957). Studies on oxygenases; pyrocatechase. The Journal of Biological Chemistry, 229, 905–920.
International Agency for Research Center (2015). List of classifications, Volumes 1–114. IARC Monographs List of Classifications by Cancer Site. http://monographs.iarc.fr/ENG/Classification/List_of_Classifications_Vol1-114.pdf. Accessed 25 Dec 2015.
Jayamani, I., & Cupples, A. M. (2015). Stable isotope probing and high-throughput sequencing implicate Xanthomonadaceae and Rhodocyclaceae in ethylbenzene degradation. Environmental Engineering Science, 32, 240–249.
Juwarkar, A. A., Singh, S. K., & Mudhoo, A. (2010). A comprehensive overview of elements in bioremediation. Reviews in Environmental Science and Bio/Technology, 9, 215–288.
Krausova, V. I., Robb, F. T., & González, J. M. (2006). Biodegradation of dichloromethane in an estuarine environment. Hydrobiologia, 559, 77–83.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, doi:10.1093/molbev/msw054. http://www.megasoftware.net/.
Lane, D. J. (1991). 16S/23S rRNA sequencing. In E. Stackebrandt & M. Goodfellow (Eds.), Nucleic acid techniques in bacterial systematics (pp. 115–175). John Wiley & Sons: Chichester.
Leahy, J. G., Batchelor, P. J., & Morcomb, S. M. (2003). Evolution of the soluble diiron monooxygenases. FEMS Microbiology Reviews, 27, 449–479.
Mackay, D., & Shiu, W. Y. (1981). A critical review of Henry’s low constants for chemicals of environmental interest. Journal of Physical and Chemical Reference Data, 10, 1175–1199.
Moeseneder, M. M., Arrieta, J. M., Muyzer, G., Winter, C., & Herndl, G. J. (1999). Optimization of terminal-restriction fragment length polymorphism analysis for complex marine bacterioplankton communities and comparison with denaturing gradient gel electrophoresis. Applied and Environmental Microbiology, 65, 3518–3525.
Muller, E. E. L., Bringel, F., & Vuilleumier, S. (2011). Dichloromethane-degrading bacteria in the genomic age. Research in Microbiology, 162, 869–876.
Nelson, M. J. K., Montgomery, A. O., & Pritchard, P. H. (1988). Trichloroethylene metabolism by microorganisms that degrade aromatic compounds. Applied and Environmental Microbiology, 54, 604–606.
Oh, Y.-S., Shareefdeen, Z., Baltzis, B. C., & Bartha, R. (1994). Interactions between benzene, toluene, and p-xylene (BTX) during their biodegradation. Biotechnology and Bioengineering, 44, 533–538.
Oksanen, J., Blanchet, G. F., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, S. P., Stevens, M. H. H., & Wanger, H. (2015). Vegan: Community Ecology Package. R Package Version 2.3-0. http://CRAN.R-project.org/package=vegan
Osborn, A. M., Moore, E. R., & Timmis, K. N. (2000). An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environmental Microbiology, 2, 39–50.
Priya, V. S., & Philip, L. (2013). Biodegradation of dichloromethane along with other VOCs from pharmaceutical wastewater. Applied Biochemistry and Biotechnology, 169, 1197–1218.
Pruesse, E., Peplies, J., & Glöckner, F. O. (2012). SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics, 28, 1823–1829. http://www.arb-silva.de/.
Reardon, K. F., Mosteller, D. C., & Bull Rogers, J. D. (2000). Biodegradation kinetics of benzene, toluene, and phenol as single and mixed substrates for Pseudomonas putida F1. Biotechnology and Bioengineering, 69, 385–400.
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J., & Weber, C. F. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541. http://www.mothur.org/.
Schroeder, E. D., Eweis, J. B., Chang, D. P. Y., & Veir, J. K. (2000). Biodegradation of recalcitrant components of organic mixtures. Water, Air, and Soil Pollution, 123, 133–146.
Takada-Hoshino, Y., & Matsumoto, N. (2004). An improved DNA extraction method using skim milk from soils that strongly adsorb DNA. Microbes and Environments, 19, 13–19.
Tay, S. T., Hemond, H. F., Polz, M. F., Cavanaugh, C. M., Dejesus, I., & Krumholz, L. R. (1998). Two new Mycobacterium strains and their role in toluene degradation in a contaminated stream. Applied and Environmental Microbiology, 64, 1715–1720.
Vidali, M. (2001). Bioremediation. An overview. Pure and Applied Chemistry, 73, 1163–1172.
Widdel, F., & Pfennig, N. (1981). Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. I. Isolation of new sulfate-reducing bacteria enriched with acetate from saline environments. Description of Desulfobacter postgatei gen. nov., sp. nov. Archives of Microbiology, 129, 395–400.
Yokota, A., Tamura, T., Takeuchi, M., Weiss, N., & Stackebrandt, E. (1994). Transfer of Propionibacterium innocuum Pitcher and Collins 1991 to Propioniferax gen. nov. as Propioniferax innocua comb. nov. International Journal of Systematic Bacteriology, 44, 579–582.
Yu, C.-P., & Chu, K.-H. (2005). A quantitative assay for linking microbial community function and structure of a naphthalene-degrading microbial consortium. Environmental Science & Technology, 39, 9611–9619.
Zehraoui, A., Wendell, D., & Sorial, G. A. (2014). Biodegradation of a ternary mixture of hydrophobic and hydrophilic VOCs in trickle bed air biofilters. Water, Air, and Soil Pollution, 225, 2075.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Table S1
(DOCX 20 kb)
Rights and permissions
About this article
Cite this article
Yoshikawa, M., Zhang, M. & Toyota, K. Enhancement and Biological Characteristics Related to Aerobic Biodegradation of Toluene with Co-Existence of Benzene. Water Air Soil Pollut 227, 340 (2016). https://doi.org/10.1007/s11270-016-3050-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-016-3050-5