Abstract
Contaminant biodegradation in unsaturated soils may reduce the risks of vapor intrusion. However, the reported rates show large variability and are often derived from slurry experiments that are not representative of unsaturated conditions. Here, different laboratory setups are used to derive the biodegradation capacity of an unsaturated soil layer through which gaseous toluene migrates from the water table upwards. Experiments in static unsaturated soil microcosms at 6–30 % water-filled porosity (WFP) and unsaturated soil columns at 9, 14, and 27 % WFP were compared with liquid batches containing the same culture of Alicycliphilus denitrificans. The biodegradation rates for the liquid batches were orders of magnitude lower than for the other setups. Hence, liquid batches do not necessarily reflect optimal conditions for bacteria; either oxygen or toluene mass transfer at the cell scale or the absence of soil–water–air interfaces seemed to be limiting bacterial activity. For the column setup, the rates were limited by mass supply. The microcosm results could be described by apparent first-order biodegradation constants that increased with WFP or through a numerical model that included biodegradation as a first-order process taking place in the liquid phase only. The model liquid phase first-order rates varied between 6.25 and 20 h−1 and were not related to the water content. Substrate availability was the primary factor limiting bioactivity, with evidence for physiological stress at the lowest water-filled porosity. The presented approach is useful to derive liquid phase biodegradation rates from experimental data and to include biodegradation in vapor intrusion models.
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References
Abreu L, Johnson PC (2005) Effect of vapor source-building separation and building construction on soil vapor intrusion as studied with a three-dimensional numerical model. Environ Sci Technol 39(12):4550–4561
Abreu L, Johnson PC (2006) Simulating the effect of aerobic biodegradation on soil vapor intrusion into buildings: influence of degradation rate, source concentration, and depth. Environ Sci Technol 40(7):2304–2315
Abreu L, Ettinger R, McAlary T (2009) Simulated soil vapor intrusion attenuation factors including biodegradation for petroleum hydrocarbons. Ground Water Monit Remediat 29(1):105–117
Allen-King RM, Gillham RW, Barker JF, Sudicky EA (1996) Fate of dissolved toluene during steady infiltration through unsaturated soil: II. Biotransformation under nutrient-limited conditions. J Environ Qual 25(2):287–295
Alvarez PJJ, Vogel TM (1991) Kinetics of aerobic biodegradation of benzene and toluene in sandy aquifer material. Biodegradation 2(1):43–51
Bastida F, Luis Moreno J, Hernandez T, Garcia C (2006) Microbiological degradation index of soils in a semiarid climate. Soil Biol Biochem 38(12):3463–3473
Bouwer EJ, Zehnder AJB (1993) Bioremediation of organic compounds—putting microbial metabolism to work. Trends Biotechnol 11(8):360–367
Chang MK, Voice TC, Criddle CS (1993) Kinetics of competitive inhibition and cometabolism in the biodegradation of benzene, toluene, and p-xylene by two Pseudomonas isolates. Biotechnol Bioeng 41(11):1057–1065
Dechesne A, Or D, Gülez G, Smets BF (2008) The porous surface model, a novel experimental system for online quantitative observation of microbial processes under unsaturated conditions. Appl Environ Microbiol 74(16):5195–5200
DeVaull GE (2007) Indoor vapor intrusion with oxygen-limited biodegradation for a subsurface gasoline source. Environ Sci Technol 41(9):3241–3248
DeVaull GE, Ettinger RA, Salanitro JP, Gustafson JB (1997) Benzene, toluene, ethylbenzene and xylenes [BTEX] degradation in vadose zone soils during vapor transport: first-order rate constants. Proceedings of the Petroleum Hydrocarbons and Organic Chemicals in Ground Water: Prevention, Detection and Remediation Conference, API/NGWA, Ground Water Publishing Company, Westerville, Ohio, pp 365–379
El-Farhan YH, Scow KM, De Jonge LW, Rolston DE, Moldrup P (1998) Coupling transport and biodegradation of toluene and trichloroethylene in unsaturated soils. Water Resour Res 34(3):437–445
Hansen KC, Zhou Z, Yaws CL, Aminabhavi TM (1993) Determination of Henry’s law constants of organics in dilute aqueous solutions. J Chem Eng Data 38(4):546–550
Harms H, Zehnder AJB (1994) Influence of substrate diffusion on degradation of dibenzofuran and 3-chlorodibenzofuran by attached and suspended bacteria. Appl Environ Microbiol 60(8):2736–2745
Heijthuijsen JHFG, Hansen TA (1986) Interspecies hydrogen transfer in co-cultures of methanol-utilizing acidogens and sulfate-reducing or methanogenic bacteria. FEMS Microbiol Lett 38(1):57–64
Hendrickx B, Junca H, Vosahlova J, Lindner A, Rüegg I, Bucheli-Witschel M, Faber F, Egli T, Mau M, Schlömann M, Brennerova M, Brenner V, Pieper DH, Top EM, Dejonghe W, Bastiaens L, Springael D (2006) Alternative primer sets for PCR detection of genotypes involved in bacterial aerobic BTEX degradation: distribution of the genes in BTEX degrading isolates and in subsurface soils of a BTEX contaminated industrial site. J Microbiol Meth 64(2):250–265
Hers I, Atwater J, Li L, Zapf-Gilje R (2000) Evaluation of vadose zone biodegradation of BTX vapours. J Contam Hydrol 46(3–4):233–264
Höhener P, Duwig C, Pasteris G, Kaufmann K, Dakhel N, Harms H (2003) Biodegradation of petroleum hydrocarbon vapors: laboratory studies on rates and kinetics in unsaturated alluvial sand. J Contam Hydrol 66(1–2):93–115
Höhener P, Dakhel N, Christophersen M, Broholm M, Kjeldsen P (2006) Biodegradation of hydrocarbons vapors: comparison of laboratory studies and field investigations in the vadose zone at the emplaced fuel source experiment, Airbase Værløse, Denmark. J Contam Hydrol 88(3–4):337–358
Holden PA, Hersman LE, Firestone MK (2001) Water content mediated microaerophilic toluene biodegradation in arid vadose zone materials. Microbial Ecol 42(3):256–266
Ilstedt U, Nordgren A, Malmer A (2000) Optimum soil water for soil respiration before and after amendment with glucose in humid tropical acrisols and a boreal mor layer. Soil Biol Biochem 32:1591–1599
Jin Y, Streck T, Jury WA (1994) Transport and biodegradation of toluene in unsaturated soil. J Contam Hydrol 17(2):111–127
Johnson PC, Ettinger R (1991) Heuristic model for predicting the intrusion rate of contaminant vapors into buildings. Environ Sci Technol 25(8):1445–1452
Kelly WR, Hornberger GM, Herman JS, Mills AL (1996) Kinetics of BTX biodegradation and mineralization in batch and column systems. J Contam Hydrol 23(1–2):113–132
Khan KS, Joergensen RG (2006) Microbial C, N, and P relationships in moisture-stressed soils of Potohar, Pakistan. J Plant Nutr Soil Sc 169(4):494–500
Lahvis MA, Baehr AL, Baker RJ (1999) Quantification of aerobic biodegradation and volatilization rates of gasoline hydrocarbons near the water table under natural attenuation conditions. Water Resour Res 35(3):753–765
Linn DM, Doran JW (1984) Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and not tilled soils. Soil Sci Soc Am J 48(6):1267–1272
Maier RM, Pepper IL, Gerba CP (2000) Environmental microbiology. Academic, San Diego
Malina G, Grotenhuis JTC, Rulkens WH, Mous SLJ, De Wit JCM (1998) Soil vapour extraction versus bioventing of toluene and decane in bench-scale soil columns. EnvironTechnol 19(10):977–991
McAlary T, Provoost J, Dawson HE (2011) Vapor intrusion. In: Swartjes FA (ed) Dealing with contaminated sites. From theory towards practical application. Springer, Dordrecht, pp 409–454
Mercer JW, Cohen RM (1990) A review of immiscible fluids in the subsurface: properties, models, characterization and remediation. J Contam Hydrol 6(2):107–163
Molins S, Mayer KU, Amos RT, Bekins BA (2010) Vadose zone attenuation of organic compounds at a crude oil spill site—interactions between biogeochemical reactions and multicomponent gas transport. J Contam Hydrol 112(1–4):15–29
Ostendorf DW, Kampbell DH (1991) Biodegradation of hydrocarbon vapors in the unsaturated zone. Water Resour Res 27(4):453–462
Ostendorf DW, Schoenberg TH, Hinlein ES, Long SH (2007) Monod kinetics for aerobic biodegradation of petroleum hydrocarbons in unsaturated soil microcosms. Environ Sci Technol 41(7):2343–2349
Pasteris G, Werner D, Kaufmann K, Höhener P (2002) Vapor phase transport and biodegradation of volatile fuel compounds in the unsaturated zone: a large scale lysimeter experiment. Environ Sci Technol 36(1):30–39
Patterson BM, Davis GB (2009) Quantification of vapor intrusion pathways into a slab-on-ground building under varying environmental conditions. Environ Sci Technol 43(3):650–656
Picone S, Valstar J, Grotenhuis T, van Gaans P, Rijnaarts H (2012) Sensitivity analysis on parameters and processes affecting vapor intrusion risks. Environ Toxicol Chem 31(5):1042–1052
Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58(4):755–805
Poulsen M, Lemon L, Barker JF (1992) Dissolution of monoaromatic hydrocarbons into groundwater from gasoline–oxygenate mixtures. Environ Sci Technol 26(12):2483–2489
Rathfelder KM, Lang JR, Abriola LM (2000) A numerical model (MISER) for the simulation of coupled physical, chemical and biological processes in soil vapor extraction and bioventing systems. J Contam Hydrol 43(3–4):239–270
Reardon KF, Mosteller DC, Bull Rogers JD (2000) Biodegradation kinetics of benzene, toluene, and phenol as single and mixed substrates for Pseudomonas putida F1. Biotechnol Bioeng 69(4):385–400
Rijnaarts HHM, Norde W, Bouwer EJ, Lyklema J, Zehnder AJB (1993) Bacterial adhesion under static and dynamic conditions. Appl Environ Microbiol 59(10):3255–3265
Roels JA, Kossen NWF (1978) On the modelling of microbial metabolism. In: Bull MJ (ed) Progress in industrial microbiology. Elsevier, Amsterdam, pp 95–203
Sanders PF, Hers I (2006) Vapor intrusion in homes over gasoline-contaminated ground water in Stafford, New Jersey. Ground Water Monit R 26(1):63–72
Schaefer A, Harms H, Zehnder AJB (1998) Bacterial accumulation at the air–water interface. Environ Sci Technol 32:3704–3712
Schoefs O, Perrier M, Samson R (2004) Estimation of contaminant depletion in unsaturated soils using a reduced-order biodegradation model and carbon dioxide measurement. Appl Microbiol Biot 64:53–61
Shaler TA, Klečka GM (1986) Effect of dissolved oxygen concentration on biodegradation of 2,4-dichlorophenoxyacetic acid. Appl Environ Microbiol 51(5):950–955
Skopp J, Jawson D, Doran JW (1990) Steady-state aerobic microbial activity as a function of soil water content. Soil Sci Soc Am J 54:1619–1625
Smith JA, Chiou CT, Kammer JA, Kile DE (1990) Effect of soil moisture on the sorption of trichloroethene vapor to vadose-zone soil at Picatinny arsenal, New Jersey. Environ Sci Technol 24(5):676–683
Suarez M, Rifai H (1999) Biodegradation rates for fuel hydrocarbons and chlorinated solvents in groundwater. Bioremediat J 3(4):337–362
Tindall JA, Friedel MJ, Szmajter RJ, Cuffin SM (2005) Part 1: Vadose-zone column studies of toluene (enhanced bioremediation) in a shallow unconfined aquifer. Water Air Soil Pollut 168(1–4):325–357
USEPA (2004) User’s guide for evaluating vapor intrusion into buildings. Office of Emergency and Remedial Response, Washington, DC
Weelink SA, Tan NC, ten Broeke H, van Doesburg W, Langenhoff A, Gerritse J, Stams AJ (2007) Physiological and phylogenetic characterization of a stable benzene-degrading, chlorate-reducing microbial community. FEMS Microbiol Ecol 60(2):312–321
Weelink SA, Tan NC, ten Broeke H, van den Kieboom C, van Doesburg W, Langenhoff A, Gerritse J, Junca H, Stams AJ (2008) Isolation and characterization of Alicycliphilus denitrificans strain BC, which grows on benzene with chlorate as the electron acceptor. Appl Environ Microbiol 74(21):6672–6681
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Picone, S., Grotenhuis, T., van Gaans, P. et al. Toluene biodegradation rates in unsaturated soil systems versus liquid batches and their relevance to field conditions. Appl Microbiol Biotechnol 97, 7887–7898 (2013). https://doi.org/10.1007/s00253-012-4480-7
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DOI: https://doi.org/10.1007/s00253-012-4480-7