Bioremediation Potential in Recalcitrant Areas of PCE in Alluvial Fan Deposits

Authors: J. Herrero, D. Puigserver, I. Nijenhuis, K. Kuntze, J. M. Carmona

Abstract:

In the transition zone between aquifers and basal aquitards, the perchloroethene (PCE)-pools are more recalcitrant than those elsewhere in the aquifer. Although biodegradation of chloroethenes occur in this zone, it is a slow process and a remediation strategy is needed. The aim of this study is to demonstrate that combined strategy of biostimulation and in situ chemical reduction (ISCR) is more efficient than the two separated strategies. Four different microcosm experiments with sediment and groundwater of a selected field site where an aged pool exists at the bottom of a transition zone were designed under i) natural conditions, ii) biostimulation with lactic acid, iii) ISCR with zero-value iron (ZVI) and under iv) a combined strategy with lactic acid and ZVI. Biotic and abiotic dehalogenation, terminal electron acceptor processes and evolution of microbial communities were determined for each experiment. The main results were: i) reductive dehalogenation of PCE-pools occurs under sulfate-reducing conditions; ii) biostimulation with lactic acid supports more pronounced reductive dehalogenation of PCE and trichloroethene (TCE), but results in an accumulation of 1,2-cis-dichloroethene (cDCE); iii) ISCR with ZVI produces a sustained dehalogenation of PCE and its metabolites iv) combined strategy of biostimulation and ISCR results in a fast dehalogenation of PCE and TCE and a sustained dehalogenation of cisDCE. These findings suggest that biostimulation and ISCR with ZVI are the most suitable strategies for a complete reductive dehalogenation of PCE-pools in the transition zone and further to enable the dissolution of dense non-aqueous phase liquids.

Keywords: Aged PCE-pool, anaerobic microcosm experiment, biostimulation, in situ chemical reduction, natural attenuation.

Digital Object Identifier (DOI): doi.org/10.5281/zenodo.2643858

References:

[1] A. Tiehm and K. R. Schmidt, “Sequential anaerobic/aerobic biodegradation of chloroethenes--aspects of field application.,” Curr. Opin. Biotechnol., vol. 22, no. 3, pp. 415–21, Jun. 2011.
[2] M. J. Moran, J. S. Zogorski, and B. L. Rowe, “Approach to an assessment of volatile organic compounds in the nation’s ground water and drinking-water supply wells,” Open-File Rep., 2006.
[3] USEPA, “National Primary Drinking Water Regulations. U.S. Environmental Protection. EPA 816-F-09-004.,” in National Service Center for Environmental Publications, 2009.
[4] B. L. Parker, J. A. Cherry, S. W. Chapman, and M. A. Guilbeault, “Review and analysis of chlorinated solvent dense nonaqueous phase liquid distributions in five sandy aquifers,” Vadose Zo. J., vol. 2, no. 2, pp. 116–137, 2003.
[5] T. H. Wiedemeier et al., “Technical protocol for evaluating natural attenuation of chlorinated solvents in ground water,” Natl. Risk Manag. Res. Lab. EPA, no. September, p. EPA/600/R-98/128.pag, 1998.
[6] P. M. Bradley, “History and Ecology of Chloroethene Biodegradation: A Review,” Bioremediat. J., vol. 7, no. 2, pp. 81–109, Apr. 2003.
[7] P. M. Bradley and F. H. Chapelle, “Microbial Mineralization of Dichloroethene and Vinyl Chloride under Hypoxic Conditions,” Ground Water Monit. Remediat., vol. 31, no. 4, pp. 39–49, Nov. 2011.
[8] L. Adrian and F. E. Löffler, “Organohalide-Respiring Bacteria—An Introduction,” in Organohalide-Respiring Bacteria, Berlin, Heidelberg: Springer Berlin Heidelberg, 2016, pp. 3–6.
[9] E. Bouwer, “Bioremediation of chlorinated solvents using alternate electron acceptors,” Handb. bioremediation, 1994.
[10] T. M. Vogel, C. S. Criddle, and P. L. McCarty, “ES Critical Reviews: Transformations of halogenated aliphatic compounds,” Environ. Sci. Technol., vol. 21, no. 8, pp. 722–36, Aug. 1987.
[11] S. Atashgahi, Y. Lu, and H. Smidt, “Overview of Known Organohalide-Respiring Bacteria—Phylogenetic Diversity and Environmental Distribution,” in Organohalide-Respiring Bacteria, Berlin, Heidelberg: Springer Berlin Heidelberg, 2016, pp. 63–105.
[12] I. Nijenhuis and K. Kuntze, “Anaerobic microbial dehalogenation of organohalides — state of the art and remediation strategies,” Curr. Opin. Biotechnol., vol. 38, pp. 33–38, Apr. 2016.
[13] S. H. Zinder, “The Genus Dehalococcoides,” in Organohalide-Respiring Bacteria, Berlin, Heidelberg: Springer Berlin Heidelberg, 2016, pp. 107–136.
[14] X. Maymó-Gatell, Y. Chien, J. M. Gossett, and S. H. Zinder, “Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene,” Science (80-.)., vol. 276, no. 5318, pp. 1568–1571, 1997.
[15] B. van der Zaan et al., “Correlation of Dehalococcoides 16S rRNA and chloroethene-reductive dehalogenase genes with geochemical conditions in chloroethene-contaminated groundwater.,” Appl. Environ. Microbiol., vol. 76, no. 3, pp. 843–50, Feb. 2010.
[16] P. M. Bradley and F. H. Chapelle, “Anaerobic mineralization of vinyl chloride in Fe (III) -Reducing , aquifer sediments,” Env. Sci Technol., vol. 30, no. 6, pp. 2084–2086, 1996.
[17] F. Aulenta, A. Pera, S. Rossetti, M. Petrangeli Papini, and M. Majone, “Relevance of side reactions in anaerobic reductive dechlorination microcosms amended with different electron donors.,” Water Res., vol. 41, no. 1, pp. 27–38, Jan. 2007.
[18] N. Wei and K. T. Finneran, “Influence of ferric iron on complete dechlorination of trichloroethylene (TCE) to ethene: Fe (III) reduction does not always inhibit complete dechlorination,” Environ. Sci. Technol., vol. 45, no. 17, pp. 7422–7430, 2011.
[19] National Research Council, “Improving management of persistent of contaminants. Groundwater and soil cleanup,” Natl. Acad. Press., pp. 113–174, 1999.
[20] J. Philips, P. J. Haest, D. Springael, and E. Smolders, “Inhibition of Geobacter Dechlorinators at Elevated Trichloroethene Concentrations Is Explained by a Reduced Activity Rather than by an Enhanced Cell Decay,” Environ. Sci. Technol., p. 130115145641003, Jan. 2013.
[21] S. K. Haack and B. A. Bekins, “Microbial populations in contaminant plumes,” Hydrogeol. J., vol. 8, no. 1, pp. 63–76, Mar. 2000.
[22] B. E. Sleep et al., “Biological enhancement of tetrachloroethene dissolution and associated microbial community changes,” Environ. Sci. Technol., vol. Environmen, no. 40, pp. 3623–3633, 2006.
[23] C. Holliger et al., “Dehalobacter restrictus gen. nov. and sp. nov., a strictly anaerobic bacterium that reductively dechlorinates tetra-and trichloroethene in an anaerobic respiration,” Arch. Microbiol., vol. 169, no. 4, pp. 313–321, 1998.
[24] L. R. Krumholz, “Desulfuromonas chloroethenica sp. nov. uses tetrachloroethylene and trichloroethylene as electron acceptors,” Int. J. Syst. Bacteriol., vol. 47, no. 4, pp. 1262–1263, 1997.
[25] M. L. G. C. Luijten et al., “Description of Sulfurospirillum halorespirans sp. nov., an anaerobic, tetrachloroethene-respiring bacterium, and transfer of Dehalospirillum multivorans to the genus Sulfurospirillum as Sulfurospirillum multivorans comb. nov.,” Int. J. Syst. Evol. Microbiol., vol. 53, no. 3, pp. 787–793, 2003.
[26] X. Maymó-Gatell, I. Nijenhuis, and S. H. Zinder, “Reductive dechlorination of cis-1,2-dichloroethene and vinyl chloride by ‘Dehalococcoides ethenogenes’.,” Environ. Sci. Technol., vol. 35, no. 3, pp. 516–21, Feb. 2001.
[27] A. Suyama, R. Iwakiri, K. Kai, T. Tokunaga, N. Sera, and K. Furukawa, “Isolation and characterization of Desulfitobacterium sp. strain Y51 capable of efficient dehalogenation of tetrachloroethene and polychloroethanes.,” Biosci. Biotechnol. Biochem., vol. 65, no. 7, pp. 1474–81, Jul. 2001.
[28] Y. C. Chang, M. Hatsu, K. Jung, Y. S. Yoo, and K. Takamizawa, “Isolation and characterization of a tetrachloroethylene dechlorinating bacterium, Clostridium bifermentans DPH-1,” J. Biosci. Bioeng., vol. 89, no. 5, pp. 489–491, 2000.
[29] P. K. Sharma and P. L. McCarty, “Isolation and characterization of a facultatively aerobic bacterium that reductively dehalogenates tetrachloroethene to cis-1, 2-dichloroethene.,” Appl. Environ. Microbiol., vol. 62, no. 3, pp. 761–765, 1996.
[30] Y. Sung et al., “Characterization of two tetrachloroethene-reducing, acetate-oxidizing anaerobic bacteria and their description as Desulfuromonas michiganensis sp. nov.,” Appl. Environ. Microbiol., vol. 69, no. 5, pp. 2964–2974, 2003.
[31] Y. Yang and P. L. McCarty, “Comparison between donor substrates for biologically enhanced tetrachloroethene DNAPL dissolution,” Environ. Sci. Technol., vol. 36, pp. 3400–3404, 2002.
[32] R. Gillham and S. O’Hannesin, “Enhanced degradation of halogenated aliphatics by zero‐valent iron,” Ground Water, vol. 32, pp. 958–967, 1994.
[33] W. S. Orth and R. W. Gillham, “Dechlorination of trichloroethene in aqueous solution using Fe 0,” Env. Sci Technol., vol. 30, no. 1, pp. 66–71, 1996.
[34] T. J. Campbell, D. R. Burris, A. L. Roberts, and J. R. Wells, “Trichloroethylene and tetrachloroethylene reduction in a metallic iron-water-vapor batch system,” Environ. Toxicol. Chem., vol. 16, no. 4, pp. 625–630, 1997.
[35] R. A. Brown, “Chemical oxidation and resuction for chlorinated solvent remediation,” in In situ Remediation of Chlorinated Solvent Plumes, no. 1, 2010.
[36] B. M. Henry, “Biostimulation for anaerobic bioremediation of chlorinated solvents,” in In situ Remediation of Chlorinated Solvent Plumesemediation of chlorinated solvent plume, 2010.
[37] M. M. Lorah, E. H. Majcher, E. J. Jones, and M. a Voytek, “Microbial consortia development and microcosm and column experiments for enhanced bioremediation of chlorinated volatile organic compounds, West Branch Canal Creek wetland area, Aberdeen Proving Ground, Maryland.,” 2008.
[38] D. E. Ellis et al., “Bioaugmentation for accelerated in situ anaerobic bioremediation,” Environ. Sci. Technol., vol. 34, no. 11, pp. 2254–2260, Jun. 2000.
[39] D. Puigserver et al., “Temporal hydrochemical and microbial variations in microcosm experiments from sites contaminated with chloromethanes under biostimulation with lactic acid,” Bioremediat. J., vol. 20, no. 1, pp. 54–70, Jan. 2016.
[40] D. Hunkeler and R. Aravena, “Investigating the origin and fate of organic contaminant in groundwater using stable isotope analysis,” in Environmental isotopes in biodegradation and bioremediation, no. 8, C. M. Aelion, P. Höhener, D. Hunkeler, and R. Aravena, Eds. Boca Raton, Fla.: CRC Press, 2010, p. 450.
[41] D. Hunkeler, R. U. Meckenstock, B. Sherwood Lollar, T. C. Schmidt, and J. T. Wilson, “A guide for assessing biodegradation and source identification of organic ground water contaminants using compound specific isotope analysis ( CSIA ),” PA 600/R-08/148, no. December. 2008.
[42] S. J. Flynn, F. E. Löffler, and J. M. Tiedje, “Microbial community changes associated with a shift from reductive dechlorination of PCE to reductive dechlorination of cis-DCE and VC,” Environ. Sci. Technol., vol. 34, no. 6, pp. 1056–1061, 2000.
[43] S. Révész et al., “Bacterial community changes in TCE biodegradation detected in microcosm experiments,” Int. Biodeterior. Biodegradation, vol. 58, no. 3, pp. 239–247, 2006.
[44] É. Mészáros, R. Sipos, R. Pál, C. Romsics, and K. Márialigeti, “Stimulation of trichloroethene biodegradation in anaerobic three-phase microcosms,” Int. Biodeterior. Biodegradation, vol. 84, pp. 126–133, Oct. 2013.
[45] R. E. Richardson, V. K. Bhupathiraju, D. L. Song, T. A. Goulet, and L. Alvarez-Cohen, “Phylogenetic characterization of microbial communities that reductively dechlorinate TCE based upon a combination of molecular techniques,” Environ. Sci. Technol., vol. 36, no. 12, pp. 2652–2662, 2002.
[46] J. M. Lendvay et al., “Bioreactive barriers: a comparison of bioaugmentation and biostimulation for chlorinated solvent remediation,” Environ. Sci. Technol., vol. 37, no. 7, pp. 1422–1431, 2003.
[47] T. W. Macbeth, D. E. Cummings, S. Spring, L. M. Petzke, and K. S. Sorenson, “Molecular characterization of a dechlorinating community resulting from in situ biostimulation in a trichloroethene-contaminated deep, fractured basalt aquifer and comparison to a derivative laboratory culture,” Appl. Environ. Microbiol., vol. 70, no. 12, pp. 7329–7341, 2004.
[48] ITRC, Strategies for Monitoring the Performance of DNAPL Source Zone Remedies, Technical/Regulatory Guidelines, Interstate Technology and Regulatory Council, 206 pages, August 2004, Washington, DC.
[49] J. J. Morse et al., “A treatability test for evaluating the potential applicability of the reductive anaerobic biological in situ treatment technology (RABITT) to remediate chloroethenes,” Draft Tech. Protoc. Environ. Secur. Technol. Certif. Program. Arlington, VA Environ. Secur. Technol. Program., 1998.
[50] X. Lu, J. T. Wilson, and D. H. Kampbell, “Comparison of an assay for Dehalococcoides DNA and a microcosm study in predicting reductive dechlorination of chlorinated ethenes in the field.,” Environ. Pollut., vol. 157, no. 3, pp. 809–15, Mar. 2009.
[51] D. Puigserver et al., “Reductive dechlorination in recalcitrant sources of chloroethenes in the transition zone between aquifers and aquitards,” Environ. Sci. Pollut. Res., vol. 23, no. 18, pp. 18724–18741, Sep. 2016.
[52] J. T. Trevors, “Sterilization and inhibition of microbial activity in soil,” J. Microbiol. Methods, vol. 26, pp. 53–59, 1996.
[53] . Herrero, D. Puigserver, I. Nijenhuis, K. Kuntze, and J. M. Carmona, “Evolution of degradation of chloroethenes as a function of the biogeochemical interactions taking place in the source zone-plume zone,” unpublished.
[54] Y. D. Chen, J. F. Barker, and L. Gui, “A strategy for aromatic hydrocarbon bioremediation under anaerobic conditions and the impacts of ethanol: a microcosm study.,” J. Contam. Hydrol., vol. 96, no. 1–4, pp. 17–31, Feb. 2008.
[55] J. Palau, A. Soler, P. Teixidor, and R. Aravena, “Compound-specific carbon isotope analysis of volatile organic compounds in water using solid-phase microextraction,” J. Chromatogr. A, vol. 1163, no. 1, pp. 260–268, 2007.
[56] D. J. Lane, “16S/23S rRNA Sequencing,” in Nucleic acid techniques in bacterial systematics, E. Stackebrandt and M. Goodfellow, Eds. New York: Wiley, 1991.
[57] H. Heuer, M. Krsek, P. Baker, K. Smalla, and E. Wellington, “Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients,” Appl. Envir. Microbiol., vol. 63, no. 8, pp. 3233–3241, Aug. 1997.
[58] G. Imfeld et al., “Characterization of microbial communities in the aqueous phase of a constructed model wetland treating 1,2-dichloroethene-contaminated groundwater.,” FEMS Microbiol. Ecol., vol. 72, no. 1, pp. 74–88, Apr. 2010.
[59] W.-T. Liu, T. L. Marsh, H. Cheng, and L. J. Forney, “Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA.,” Appl. Environ. Microbiol., vol. 63, no. 11, pp. 4516–4522, 1997.
[60] T. L. Marsh, P. Saxman, J. Cole, and J. Tiedje, “Terminal restriction fragment length polymorphism analysis program, a web-based research tool for microbial community analysis,” Appl. Environ. Microbiol., vol. 66, no. 8, pp. 3616–3620, 2000.
[61] http://www.ncbi.nlm.nih.gov/blast/.
[62] D. H. Huson, S. Mitra, H. J. Ruscheweyh, N. Weber, and S. C. Schuster, “Integrative analysis of environmental sequences using MEGAN 4,” Genome Res., vol. 21, pp. 1552–1560, 2011.
[63] D. Hunkeler and B. Morasch, “Isotope fractionation during transformation processes,” in Environmental isotopes in biodegradation and bioremediation, C. M. Aelion, P. Höhener, D. Hunkeler, and R. Aravena, Eds. CRC Press, 2010, pp. 79–125.
[64] S. S. Patil, E. M. Adetutu, A. Aburto-Medina, I. R. Menz, and A. S. Ball, “Biostimulation of indigenous communities for the successful dechlorination of tetrachloroethene (perchloroethylene)-contaminated groundwater.,” Biotechnol. Lett., vol. 36, no. 1, pp. 75–83, Jan. 2014.
[65] H. I. Boga, R. Ji, W. Ludwig, and A. Brune, “Sporotalea propionica gen. nov. sp. nov., a hydrogen-oxidizing, oxygen-reducing, propionigenic firmicute from the intestinal tract of a soil-feeding termite,” Arch. Microbiol., vol. 187, pp. 15–27, 2007.
[66] E. S. Shelobolina et al., “Geobacter pickeringii sp. nov., Geobacter argillaceus sp. nov. and Pelosinus fermentans gen. nov., sp. nov., isolated from subsurface kaolin lenses,” Int. J. Syst. Evol. Microbiol., vol. 57, pp. 126–135, 2007.
[67] W. Robertson, J. Bowman, P. Franzmann, and B. Mee, “Desulfosporosinus meridiei sp. nov., a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwater,” Int J Syst Evol Microbiol, vol. 51, no. 1, pp. 133–140, Jan. 2001.
[68] L. Hallbeck and K. Pedersen, “Autotrophic and mixotrophic growth of Gallionella ferruginea,” Journal of General Microbiology, vol. 137. pp. 2657–2661, 1991.
[69] B. Sercu et al., “The influence of in situ chemical oxidation on microbial community composition in groundwater contaminated with chlorinated solvents,” Microb. Ecol., vol. 65, no. 1, pp. 39–49, 2013.
[70] W. W. Mohn and K. J. Kennedy, “Reductive dehalogenation of chlorophenols by Desulfomonile tiedjei DCB-1.,” Appl. Environ. Microbiol., vol. 58, no. 4, pp. 1367–1370, 1992.
[71] F. Löffler, J. Cole, K. Ritalahti, and J. Tiedje, “Diversity of dechlorinating bacteria,” in Dehalogenation: microbial processes and environmental application, M. Haggblom and I. Bossert, Eds. 2003, pp. 53–87.
[72] D. M. Bagley and J. M. Gossett, “Tetrachloroethene transformation to trichloroethene and cis-1,2-dichloroethene by sulfate-reducing enrichment cultures,” Appl. Environ. Microbiol., vol. 56, pp. 2511–2516, 1990.
[73] N. Yoshida, K. Asahi, Y. Sakakibara, K. Miyake, and A. Katayama, “Isolation and quantitative detection of tetrachloroethene (PCE)-dechlorinating bacteria in unsaturated subsurface soils contaminated with chloroethenes,” J. Biosci. Bioeng., vol. 104, no. 2, pp. 91–97, 2007.
[74] K. Dowideit et al., “Spatial heterogeneity of dechlorinating bacteria and limiting factors for in situ trichloroethene dechlorination revealed by analyses of sediment cores from a polluted field site,” FEMS Microbiol. Ecol., vol. 71, pp. 444–459, 2010.
[75] J. F. Heidelberg et al., “The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough.,” Nat. Biotechnol., vol. 22, no. 5, pp. 554–9, May 2004.