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Bioremediation technologies for treatment of PAH-contaminated soil and strategies to enhance process efﬁciency
S. Venkata Mohan Æ Takuro Kisa Æ Takeru Ohkuma Æ Robert A. Kanaly Æ Yoshihisa Shimizu
Received: 23 February 2006 / Accepted: 19 May 2006 / Published online: 15 July 2006 Ó Springer Science+Business Media B.V. 2006
Abstract The complex and diverse structural conﬁgurations of polycyclic aromatic hydrocarbons (PAHs), combined with their low bioavailability, hydrophobic nature, strong sorption phenomena, and high persistence in soil makes the design of effective bioremediation methodologies a challenge. The multi-phasic nature of the bioremediation process, restricted mass transfer and non-availability of degrading soil microﬂora further compound the problem. In this direction, this communication presents a focused review of bioremediation technologies used recently for the treatment of PAH-contaminated soils. The speciﬁc roles of important factors affecting bioremediation process efﬁciency are discussed. Finally some of the recently used strategies to enhance bioremediation process efﬁciency,
S. V. Mohan (&) Bioengineering and Environmental Centre, Indian Institute of Chemical Technology, Hyderabad 500 007, India e-mail: firstname.lastname@example.org T. Kisa Æ T. Ohkuma Æ Y. Shimizu Æ S. V. Mohan Research Center for Environmental Quality Management, Kyoto University, Otsu, Shiga 520 0811, Japan R. A. Kanaly Department of Technology and Ecology, Graduate School of Global Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
including bioaugmentation, biostimulation, rhizoremediation, the use of chemotaxins, the biomimetic catalytic system approach, and integrated techniques, are reviewed. Keywords Polycyclic aromatic hydrocarbons (PAHs) Æ Bioremediation Æ Technologies Æ Bioavailability Æ Factors Æ Bioaugmentation Æ Biostimulation Æ Bacterial chemotaxins Æ Rhizoremediation Æ Biomimetic catalytic system
Introduction Polycyclic aromatic hydrocarbons (PAHs) represent a large and diverse group of organic molecules having a broad range of properties, differing in molecular weight, structural conﬁguration, water solubility, number of aromatic rings, volatility, sorption coefﬁcients, etc. (Harayama 1997; Kanaly and Harayama 2000; MaliszewskaKordybach and Smreczak 2000; Harmsen 2004). Anthropogenic sources like gasoline and diesel fuel combustion, oil spills, former gas plant facilities, etc., contribute PAHs to the environmental matrix (Juhasz and Naidu 2000; Kanaly and Harayama 2000; Meckenstock et al. 2004; Johnsen et al. 2005) and their ubiquitous distribution, environmental persistence and potentially deleterious effect on human health have resulted in an increasing interest by the research commu-
Rev Environ Sci Biotechnol (2006) 5:347–374
nity. In many cases, their non-environmentally friendly nature and cost of treatment offsets the application of commonly used remediation technologies such as land removal, incineration or land ﬁlling. Considering these circumstances, bioremediation is gaining wider approval as a feasible alternative treatment technology for the remediation of soils contaminated with PAHs. Indeed, bioremediation is considered to be a safe, efﬁcient, eco-friendly and economic means of removing pollutants from contaminated soil without simply enacting transfer to another medium. Reports pertaining to bioremediation studies of PAH-contaminated soils have increased over the last 5 years. Generally, biological degradation is the primary dissipation mechanism for most organic pollutants in the soil environment, but the activity of degrading microorganisms is dependent upon many factors, including contaminant uptake and bioavailability, concentration, toxicity, mobility, access to other nutrients, and activated enzymes (Cerniglia 1984, 1992). Low bioavailability and toxicity, non-uniform spatial distribution of microorganisms and pollutants, retardation of substrate diffusion by the soil matrix, capability of microbial metabolism, etc., are factors which control the bioremediation efﬁciency of PAHs in the soil matrix. In this realm, additional strategies are being integrated into the bioremediation process to enhance bioremediation process efﬁciency. The major aim of this communication is to review the bioremediation technologies used for PAH-contaminated soils while providing emphasis on the factors inﬂuencing the process efﬁciency. Finally the paper discusses some of the more recently used strategies to enhance bioremediation process efﬁciency.
Bioremediation technologies The scientiﬁc literature for the past half decade has documented a considerable number of bioremediation studies on PAH-contaminated soil employing various remediation technologies such as solid phase treatment, land treatment/farming, composting, bioreactors, phytoremediation, enzyme catalyzed bioremediation and combined
methods (chemical pre-treatment followed by bioremediation), in addition to the application of strategies such as biostimulation, microbial adaptation, bioaugmentation, bacterial chemotaxis, etc., for enhancing bioremediation rates. Biostimulation requires adjustments to the site (contaminated soil or water) in order to provide bacterial communities with a favorable environment in which they can effectively degrade contaminants. In cases where natural communities of degrading bacteria are present in low numbers or even absent, bioaugmentation, i.e., the addition of contaminant-degrading organisms, can speed up the degradation process (Van Limbergen et al. 1998; Cunningham et al. 2004). The property of bacterial mobility under the inﬂuence of a chemical gradient, either towards (positive) or away (negative) from the gradient to found optimum conditions for their growth and survival which is called as bacterial chemotaxis (Pandey and Jain 2002), can be positively applied to enhance bioremediation in soil matrix. The process of microbial adaptation is a process that enhance native microﬂora metabolic capability by preexposure of soils to contaminant concentrations greater than the background. Various technologies reported in the literature for the bioremediation of PAH-contaminated soil in the past ﬁve years are consolidated and shown in Table 1. Several researchers studied the efﬁciency of solid phase treatment for the remediation of PAH-contaminated soil employing natural attenuation (Guerin 2000; Taylor and Jones 2001; Chang et al. 2002; Gogi et al. 2003; Xu et al. 2005a, b; Trindade et al. 2005), ex situ methods (Chang et al. 2002; Boopathy 2003; Oleszczuk and Baran 2003; Gong et al. 2005; Ambrosoli et al. 2005; Coulon et al. 2005; Macleod and Semple 2005; Sabate et al. 2006) and land farming (Betancur-Galvis et al. 2006) at both laboratory and ﬁeld scales. Some of these studies also elucidated the effects of biostimulation (Taylor and Jones 2001; Chang et al. 2002; Delille et al. 2004; Xu et al. 2005a, b; Coulon et al. 2005; Gong et al. 2005; Trindade et al. 2005; Sabate et al. 2006), bioaugmentation (Zheng and Obbard 2002; Garon et al. 2004; Venkata Mohan et al. 2004b; Trindade et al. 2005; Heinaru et al. 2005), co-substrate addition (Chang et al. 2002; Gong
in vessel composting with green waste. (2005) In situ. biostimulation with nutrients. sunﬂower oil and nutrient addition In situ. b) Gong et al. bioaugmentation and biostimulation Ex situ Ex situ. (2005) Antizar-Ladislao et al. denitrifying conditions Aerobic Coulon et al. mixed electron acceptor conditions Aerobic Aircraft oil-contaminated soil Wood treatment facility soil PAH-contaminated saline alkaline soil Oil contaminated sediments Manufactured gas plant soil Oil-contaminated soil Biphenyl. (2006) Xu et al. (2004) Betancur-Galvis et al. composting with soot waste Ex situ. (2005) Liste and Alexander (2000) 349 Composting Phytoremediation/ Rhizoremediation Ex situ. biostimulation with aeration and soil water adjustment Ex situ composting with spent mushroom Ex situ. pyrene contaminated soil Ex situ using land treatment units In situ Oleszczuk and Baran (2003) Hansen et al. b and 2006) Haderlein et al. municipal sewage and reﬁnery oil sludge Chang et al. (2003) Moretto et al.Table 1 Bioremediation technologies for the bioremediation of PAH-contaminated soil Conditions Aerobic Aerobic Heavy vehicle maintained facility soil Coal tar-contaminated soil Source of contaminant Reference Guerin (2000) Taylor and Jones (2001) Process Method Solid phase treatment/ Natural attenuation/ Land farming/Land treatment PAHs-contaminated soil (synthetic) In situ In situ ﬁeld study. (2005) Ex situ. biostimulation with slow releasing fertilizer and chitosan Ex situ. adaptation Diesel contaminated sub-antractic soil (synthetic) Pyrene-contaminated soil Wood treatment facility soil PAH-contaminated soil PAH-contaminated alkaline soil Coal tar contaminated soil Pyrene and benzo[a]pyrene contaminated soil (synthetic) Pyrene-contaminated soil Macleod and Semple (2005) Sabate et al. pilot scale study Ex situ composting with maple leaves and alfalfa In situ. (2005a. phenanthrene. nine plant species 123 . ﬂuorene.and nitrate-reducing conditions Aerobic Anaerobic. (2005) Ambrosoli et al. (2005a. (2003) Boopathy (2003) In situ Aerobic Aerobic Aerobic Aerobic Aerobic Anaerobic. (2002) Rev Environ Sci Biotechnol (2006) 5:347–374 In situ Ex situ Oil ﬁeld-contaminated soil Diesel fuel-contaminated sediments Gogoi et al. (2005) Trindade et al. ﬁeld trial. (2006) Lau et al. sulphate. nutrients Aerobic Aerobic Aerobic Aerobic Aerobic Aerobic – Anaerobic. biostimulation with biodiesel and nitrogen and phosphorus source Ex situ. natural attenuation.
soil slurry bioreactor. (2003) Johnson et al. (2006) Former manufactured gas plant site soil Manufactured Gas Plant site soil Phenanthrene and pyrene contaminated soil Diesel oil-contaminated soil Coal tar-contaminated soil PAHs-contaminated soil Aerobic Aerobic Aerobic Kaimi et al. solvent pre-treatment . (2001) Source of contaminant Reference 123 – – Ortega-Calvo et al. (2005) – – – – Aerobic Aerobic Liste and Prutz (2006) Parrish et al. (2004) Parrish et al. (2006) Canet et al. (2005) – PAHs-contaminated soil Johnson et al. (2003) Verveke et al. plant root exudates of white mulberry (Morus alba) Mixed ryegrass (Lolium perenne) and white clover (Trifolium repens) sward together with a rhizobial inoculum (Rhizobium leguminosarum) Greenhouse pot Earthworm Enzyme-mediated treatment Rev Environ Sci Biotechnol (2006) 5:347–374 Bioreactors Three plant species (maize. ryegrass and white clover) Ryegrass White rot fungus and native soil microﬂora Soil slurry bioreactor (augmented with fungus Phanerochaete chrysosporium) Soil slurry bioreactor (augmented with fungus Absidia cylindrospora) Ex situ. (2005) Xu et al.h]nthracene contaminated soil PAHs-contaminated soil PAHs-contaminated soil Chrysene contaminated soil Creosote contaminated soil Manufactured gas plant site – Benzo[a]pyrene Rentz et al. (2004) Huang et al. (2001) Process Method Mixed sward of clover and ryegrass Bacterial chemotaxins Willo stands Mixed grass legume system with microbial inoculum Multiple process phytoremediation system Rhizodegradtion using Tall fescue (Festuca arundinacea Schreb) and yellow sweet clover (Melilotus ofﬁcinalis Lam) Plant root extracts of osage orange (Maclura pomifera). (2004) Fluorenecontaminated soil Anthracene-contaminated soil (synthetic) Coal tar-contaminated soil Venkata Mohan et al. (2004 and 2005) – Chyrene and dibenz [a.350 Table 1 continued Conditions – Joner et al. (2004b) Lee et al. hybrid willow (Salix albaXmatsydana). (2001) Zheng and Obbard (2002) Garon et al. kou (Cordia subcordata). augmented with laccase from Pleurotus ostreatus 1804 Ex situ.
(2004) Biswas et al. soil slurry bioreactor (augmented with fungus Absidia cylindrospora) Ex situ. soil slurry bioreactor. soil slurry bioreactor Ex situ. (2005) Wrenn et al. mixed electron acceptor conditions Anaerobic. soil column bioreactor Aerobic Aerobic Aerobic Anaerobic. soil column bioreactor Ex situ. soil slurry bioreactor Ex situ. pyrene and benzo[b] fluoranthene contaminated soil Diesel fuel-contaminated sediments Koran et al. continuous-ﬂow beach microcosm reactor 351 123 . biosurfactant addition Ex situ.contaminated soil Diesel oil-contaminated soil Garon et al.Table 1 continued Conditions Aerobic Aerobic Aerobic Aerobic PAHs-contaminated soil Phenanthrene-contaminated soil PAHs-contaminated soil PAHs-contaminated soil Kim et al. (2004) Woo et al. silicone oil Ex situ. (2005) Ex situ pilot scale study. mixed electron acceptor conditions Aerobic Diesel fuel-contaminated sediments Creosote-contaminated soil Phenanthrene-contaminated soil Fluorene-contaminated soil Aerobic Aerobic Rev Environ Sci Biotechnol (2006) 5:347–374 USEPA (2003) Seung et al. soil column bioreactor (ﬁxed) Ex situ. (2001) Ex situ. soil slurry bioreactor. sulphate reducing conditions Aerobic Coal derived hydrocarbons-contaminated soil Coal derived hydrocarbons-contaminated soil Crude oil-contaminated soil Pyrene-contaminated soil Crude oil-contaminated soil Kuwano and Shimizu (2006) Kumada et al. (2001) Zheng and Obbard (2002) Boopathy (2003) Source of contaminant Reference Process Method Ex situ. non-ionic surfactant (Brij30) addition Ex situ. using spill clean up sorbents (peat sorb and spill sorb) Ex situ. (2001a. soil slurry bioreactor Ex situ. (2005) Baptista et al. soil slurry bioreactor. b) Villemur et al. soil slurry bioreactor Anaerobic. soil slurry bioreactor Aerobic. addition of maltosyl cyclodextrin Ex situ. (2005) Bordas et al. (2004) Aerobic Aerobic Aerobic Fluorene-contaminated soil Phenanthrene. (2005) Naphthalene. sulfur oxidizing conditions Anaerobic PAHs-contaminated sediments Lei et al. soil column bioreactor. soil-solvent washing followed by anaerobic treatment of the extract by ﬂuidized bed conﬁguration Ex situ. (2004a. soil column bioreactor Boopathy (2004) Ex situ. (2000) Woo et al. soil slurry bioreactor. soil slurry bioreactor Ex situ. b) Garon et al. acenaphthene. (2006) Ex situ. soil slurry bioreactor (augmented with fungus Phanerochaete chrysosporium) Ex situ.
(2001) Source of contaminant Reference 123 Anaerobic Koran et al. (2006) Aerobic Aerobic aerobic PAHs-contaminated soil Diesel oil-contaminated soil Diesel oil-contaminated soil Johnson et al. bioremediation and Phytoremediation) Ex situ. acenaphthene. ozone oxidation integrated bioremediation Rev Environ Sci Biotechnol (2006) 5:347–374 . (2001) Lee et al.contaminated soil Huang et al. (2005) Ahn et al. using site spill clean up sorbents (peat sorb and spill sorb) along with soil slurry phase bioremediation Ex situ. (2005) Aerobic Phenanthrene-contaminated soil O’Mahony et al. soil-solvent washing and anaerobic treatment of the extract Multiple process integration (physical. (2001) Aerobic Naphthalene. ozone oxidation integrated bioremediation Ex situ. combined chemical oxidation (ozone and Fenton type treatment) integrated with bioremediation Ex situ combined treatment with ryegrass.352 Table 1 continued Conditions Aerobic Aerobic Coal tar-contaminated soil PAHs-contaminated sand Choi et al. white clover sword and rhizobial inoculum Ex situ. (2004) Aerobic Aerobic Creosote-contaminated soil PAHs-contaminated soil Goi and Trapido (2004) Kulik et al. and benzo(b)ﬂuoranthene contaminated soil Creosote. pyrene. pre-ozonation integrated with bioremediation Ex situ. (2006) Process Method Combined treatment Ex situ. photochemical. solvent pre-treatment integrated soil slurry phase bioremediation Ex situ. Fenton/ozone oxidation integrated bioremediation Ex situ. (2005) Biswas et al.
Composting has been demonstrated to be effective in biodegrading PAHs at both laboratory and ﬁeld scales using different types of compost bulking agents such as spent mushroom (Lau et al. 2005a). In contrast.h.i]perylene was observed in 48 h at 80°C. Composting Composting technology involves the addition of organic bulking agents to the compost mixture which facilitates an increase in porosity leading to effective air ﬂow and serves as a source of easyto-assimilate carbon for biomass growth (Eweis et al. 1998). 2004). Although different microbial populations developed in the two LF units.Rev Environ Sci Biotechnol (2006) 5:347–374 353 et al. Antizar-Ladislao and coworkers (2005b. Land farming Among solid phase treatment technologies. Normally. land farming (LF) has a distinctive advantage for stimulating the native soil microﬂora that are enriched in the soil by the presence of contaminants but that are constrained in their degradation capability by limiting factors such as inadequate aeration. 2006) used in-vessel composting technology for the remediation of coal tarcontaminated soil and optimized the soil composting temperature at 38°C for the most effective degradation. bulking) and to provide moisture (irrigation) and nutrients (fertilizer. 2003). Energy released during organic degradation results in temperature elevation facilitating that the system pass through four major microbiological phases (mesophilic. cooling and maturation) (Antizar-Ladislao et al. 1998. Microbial recolonisation during the cooling phase is characterized by the appearance of mesophilic fungi whose spores withstand the high temperatures of the thermophilic stage. In the ﬁnal compost stage (maturation). 2005a) and maple leaves and alfalfa (Haderlein et al. few solid phase bioremediation studies that focused on the anaerobic microenvironment by employing different electron acceptor conditions were reported (Chang et al. LF. benzo[a]pyrene and benzo[g. Boopathy 2003. It was reported that neither composting nor the addition of compost had any effect on benzo[a]pyrene mineralization. traditional agricultural procedures are used to create mixing and aeration (tilling. Haderlein and co-workers (2005) studied the effects of composting or simple addition of compost to soil during the mineralization of pyrene and benzo[a]pyrene by addition of maple leaves and alfalfa. the two strategies resulted in similar contaminant degradation proﬁles. 2004). 2005). 2005). green wastes (Antizar-Ladislao et al. Comparatively. 2005) and adaptation (Macleod and Semple 2005) on bioremediation process efﬁciency. 1998). Ambrosoli et al. Hansen and coworkers (2004) investigated the bioremediation of contaminated soil from a wood treatment facility using two pilot-scale land-treatment units (LTUs) and evaluated the efﬁcacy of different cultivation strategies (traditional LF practice compared with gas-phase composition (oxygen concentration) based cultivation) and maintenance schedules (intensive-treatment and nonintensive treatment). thermophilic. as with other solid-phase treatment technologies. poor contact of the microorganisms with the contaminants and insufﬁcient nutrients (Hansen et al. most digestible organic matter was found consumed by the microbial population and the composted material is considered stable (Sela et al. phenanthrene. the pyrene mineralization rate increased dramatically with the amount of time that the soil had been composted (more than 60% mineralization after 20 days). 2002. Complete degradation of individual naphthalene. often demonstrates a biphasic behavior in terms of contaminant degradation patterns: an initial rapid reduction followed by a slower rate of degradation (Hansen et al. Lau and co-workers (2003) used spent mushroom compost as a waste byproduct of the mushroom industry as a bulking agent (5%) to bioremediate PAH-contaminated soil. 2004). Antizar-Ladislao et al. soot waste (Moretto et al. FRTR. 2005). The mesophilic stage normally has the highest microbial diversity while the thermophilic stage is characterized by spore-forming bacteria and thermophilic fungi. The operation and management costs are a major portion of the overall costs of LF bioremediation. 123 . LF is one of the accepted remediation processes by the US EPA for the remediation of wood treatment facility sites (US EPA 1995).
2003). contributed to a reduction in the bioavailability of target PAHs (Parrish et al.354 Rev Environ Sci Biotechnol (2006) 5:347–374 Phyotremediation Several studies have showed the suitability of phytoremediation to soils polluted by PAHs (Liste and Alexander 2000. Ferro et al. 2003). (2006) studied the performance of three plant species (maize. The differences in PAH concentration between the unplanted and the planted soil indicated that the presence of plant roots. 2003. 1993. They concluded that the plants enhanced the biological availability of initially non-extractable molecules. Combined plant-cultivation (maize. Liste and Prutz 2006. 2002. Plants enhance the remediation of soils containing organic pollutants by various processes (Shimp et al. Joner et al. 2005). Phytoremediation. Johnson et al. According to Parrish et al. This technology is based on the catabolic potential of root-associated microorganisms. Phytoremediation may largely result from the enhanced degradation of organic compounds in the rhizosphere as a result of the higher densities and greater activities of microorganisms than in the surrounding soil (Cunningham et al. low-cost alternative for treating extensive areas of pollution by organic chemicals (Susrala et al. Liste and Prutz (2006) investigated the potential of 13 plant species in greenhouse pot experiments in a long-term contaminated soil from a former manufactured gas plant site. The advantages of phytoremediation compared with other approaches are that it preserves the natural structure and texture of the soil. 2005. Parrish et al. 1996. Haderlein et al. They concluded that the establishment of fast-growing willow stands on land can result in the revaluation of contaminants leading to the possibility for phytoremediation (Vervaeke et al. 2004. and/or (3) exuding compounds that increase the bioavailability of the contaminants. 2003. Cunningham et al. Xu et al. that high levels of microbial biomass in the soil can be achieved. Vervaeke et al. Bogan et al. (2) increasing the number of sites in the organic matrix available for PAH adsorption and eventual binding by contributing root matter to the soil organic matter (SOM). 2005. that energy is derived primarily from sunlight. Plants enhance the bioavailability of contaminants due to the function of root growth and their subsequent penetration through the soil exposing entrapped contaminants that may have been previously inaccessible. (2005). in addition to the passage of time. 2005).and root-associated microorganisms have been shown to secrete enzymes and exudates that act as surfactants and increase the available contaminant concentration in soil (Fava et al. Huang et al. 2004). 2006). 2005). Plant. Ortega-Calvo et al. Verveke et al. ‘Orm’) on the dissipation of PAHs in dredged sediment and observed most pronounced degradation in the root zone of the stand. Liste and Alexander (2000) studied the capability of nine plant species to promote the degradation of pyrene in soil and reported higher degradation rates in vegetated soil. Root exudates are found to enhance the desorption of contaminants from the soil matrix. ryegrass and white clover) for phenanthrene and pyrene removal and concluded that the presence of vegetation signiﬁcantly enhanced the dissipation of phenanthrene and pyrene in the soil environment. Xu et al. 2004. 123 . Approximately 92% of phenanthrene and 88% of pyrene was found to be removed from soils planted with maize. (2003) made a ﬁeld trial to assess the impact of planting a willow stand (Salix viminalis L. 1996. plants may serve multiple roles inﬂuencing the fate of organic contaminants in soil by (1) simultaneously promoting the degradation of the available fractions via stimulation of microbial activity. that it is low in cost and that it has the potential to be rapid (Huang et al. which are supported by the organic substrates in root excretions and by a favorable microenvironment in the rhizosphere. 98% and pyrene. 2004. is the use of plants and/or the associated rhizosphere to decontaminate polluted sites. 95%) in soils. Liste and Alexander 2000). and is considered today to be a realistic. 2005. Parrish et al. ryegrass and white clover) showed signiﬁcantly enhanced degradation rates (phenanthrene. or rhizoremediation. 2001. 2004. thereby increasing their availability to degradation (Parrish et al. to promote the proliferation of total and aromatic ring dioxygenase-expressing bacteria (ARDB) in the root zone and to foster the biodegradation of PAHs. 1994).
Two reactor conﬁgurations. three-. Recent studies suggest that the pump and. which carries nutrients. 2004. 2004). 2001a. particularly in systems with different mass transfer properties. Remediation of contaminated soil therefore may be enhanced by plants because they function like a solar driven pump that has degradative activity in the rhizosphere (Cunningham et al. The soil content in the slurry signiﬁcantly alters the distribution of target compounds between the water and soil. Soil column bioreactors bring about effective degradation of soil bound contaminants by facilitating increased contact with the water phase. 2005). Biswas et al. calcium and iron). the soil slurry phase system uses a liquid slurry treatment mechanism facilitating effective contact of the contaminant with the microﬂora (Venkata Mohan et al.treat concept that has been hypothesized applies even to hydrophobic compounds such as PAHs (Liste and Alexander 2000). bioreactors facilitate effective degradation of contaminants in less time. 2005) and anaerobic (Boopathy 2003. 1994). 2005). biostimulation with the addition of carbon sources (Garon et al. Reactors utilize naturally occurring bacteria (native soil microﬂora) or inoculated strains having speciﬁc metabolic capabilities to metabolize contaminants present either in the solid or liquid phases under optimum environmental conditions. b). four-. In contrast. 2004a. 2004a and 2006). 2005. namely soil column bioreactors and a soil slurry phase bioreactor were mostly studied. Lei et al. US EPA 2003. Seung et al. Once the oxygen depletion and acidiﬁcation problems were solved. while the complete denitriﬁcation of 123 .Rev Environ Sci Biotechnol (2006) 5:347–374 355 Phytoremediation may largely result from the enhanced degradation of organic compounds in the rhizosphere as a result of the higher densities and greater activities of microorganisms than in the surrounding soil (Cunningham et al. in situ treatment. 2001a. though the extent of degradation was smaller than what was reported for freshly spiked PAHs. 2004. 2005) and the use of sulfur-oxidizing conditions (Lei et al. and nutrients (potassium. 1999. In addition. Kuwano and Shimizu 2006) microenvironments. indigenous soil microbiota. substantial removal of two-. Bioreactors Comparatively extensive work was documented in the literature pertaining to the application of bioreactor technology for the remediation of PAH-contaminated soil (Table 1). bioaugmentation with fungal strains (Garon et al. 1996). plant transpiration may result in the transport of contaminants dissolved in the water from areas outside the root zone towards the root (Ferro et al. additional carbon sources and oxygen under controlled and optimized conditions (Kumada et al. b. Soil slurry has shown to signiﬁcantly enhance both the initial rates and overall extents of mineralization (White et al. 1996). b. magnesium. Reduced sulfur compounds present in the sediment caused rapid oxygen depletion due to the extensive activities of sulfur-oxidizing bacteria and resulted in a dramatic pH drop. evaluated the performance of soil slurry phase reactors for the treatment of creosote contaminated soil at the pilot scale level employing a 30% soil slurry. (2005) revealed the importance of indigenous bacteria involved in natural sulfur cycling by determining the degradation behavior of PAHs under sulfate oxidizing conditions. The main advantage of the slurry system as per the EPA includes on-site treatment and often. PAH degradation was not observed. nitrogen supplementation in the form of ammonia. Several research studies reported application of soil slurry phase bioremediation for the remediation of PAH-contaminated soil by adopting various process variations under aerobic (Kim et al. The process variations integrated in slurry phase operation include: the use of prior solvent pre-treatment (Lee et al. 2005). Lee et al. under denitrifying conditions. the use of non-ionic surfactants (Kim et al. Woo et al. 2001. Compared to solid phase systems. Doick and Semple 2003). 2001). the use of adsorbents (Biswas et al. and ﬁvering PAHs were achieved aerobically. The study demonstrated the effectiveness of slurry phase bioreactor technology in treating PAH-contaminated soil to levels below regulatory standards. The US EPA (2003) under the superfund innovative technology evaluation (SITE) program. phosphate. Garon et al. However. Lei et al.
composition. Sijm et al. They in turn carried out studies to investigate ways to optimize such factors for enhancing PAH bioremediation efﬁciency in soil by employing the published degradation data using a multiple linear regression approach. The proceeding section of the review discusses some of the strategies applied to enhance bioremediation process efﬁciency for decontaminating PAHcontaminated soil. its mass transfer rate and subsequent metabolism by the microﬂora. Major factors that have a signiﬁcant inﬂuence on bioremediation process efﬁciency are presented in the Table 2. 2005. (2004a. microbial associated and bioremediation system associated (Fig. It is well known that the bioavailability of contaminants is inﬂuenced by many factors including chemical structure. a number of studies that employed soil column bioreactors conﬁgured for the bioremediation of PAH-contaminated soils under aerobic (Baptista et al. soil associated. Problems associated with the bioremediation process Bioremediation of PAHs in contaminated soil is considered to be a complex phenomenon due to the toxic and hydrophobic nature of the contaminants. Ohkuma et al. Conventional slurry phase bioreactors use impellers to suspend soil particles and their mixing is more rigorous than shaking. Doick and Semple 2003. Additionally. According to Semple and co-workers (2004). 1997. The ﬁndings from their study suggest that mild operating conditions could be of beneﬁt to the treatment of contaminated soils with the advantages of low energy cost and rapid biodegradation. Furthermore. soil composition. 2005. Seung et al. Such mild conditions can be achieved by rotating a drum bioreactor (Woo and Park 1999). 2005. 1). 2005. indicating the dominance of autotrophic denitriﬁers. Sartoros et al. Ultimate bioremediation efﬁciency will depend on the extent of the bioavailability of the contaminant. the effectiveness of the system with low shear stress was increased when the soil content was increased. Bioavailability of contaminants followed by contaminant mass transfer and subsequent metabolism are the factors believed to control the overall bioremediation efﬁciency in the soil matrix especially in regard to hydrophobic contaminants such as PAHs. 2005). which might be more favorable for cell growth and subsequent biodegradation. 2005. 2006. 2006) and anaerobic (Boopathy 2004. Tang et al. 2006). 2000. Additionally. the multi phasic nature of the bioremediation process and the environmental factors governing the process. Kumada et al. Semple et al. physico-chemical interactions of PAHs with soil and environmental factors. such as temperature and moisture inﬂuence the rate and extent of biodegradation (Guerin 1999. Tang et al. Johnsen et al. a proper optimization of factors is essential to advance its efﬁciency. 2005). b) proposed that a high mass transfer rate with a high input of energy might not always be an effective condition for rapid biodegradation when using the technology of slurry-phase bioremediation and indicated the requirement of a lower mass transfer rate. Johnsen et al. Bordas et al. Tang et al. 2005. bioavailability actually describes two distinct fractions: (i) ‘bio-available’ (that compound which is interacting with biota at a given moment in time) plus and (ii) ‘bioaccessible’ (encompasses what is bio-available now plus what is potentially bio-available). including soil texture. The role of bioavailability on the microbial metabolism and mass transfer with respect to PAH bioremediation in soils was reported (Juhasz and Naidu 2000. 123 . Some factors will alter the rate of microbial uptake and metabolism (the intrinsic activity of the cell) and other factors change the rate of contaminant transport to the microorganisms (bioavailability) (Bosma et al. especially in the soil matrix. Ohkuma et al. microbial environment heterogeneity. The problems associated with PAH-bioremediation in soil microcosms can be broadly segregated into four interrelated categories: contaminant associated. or shear stress. Kuwano and Shimizu 2006) conditions have been reported. molecular weight and toxicity. pH and physical structure. (2005) suggested that in view of the complex nature of the bioremediation process. Sabate et al. 2006.356 Rev Environ Sci Biotechnol (2006) 5:347–374 nitrate to nitrogen occurred stoichiometrically with a concomitant increase in sulfate concentration. and soil properties. water content.
molecular stability is also important (Guerin 1999). (2006). Stability is indicated by the ring arrangement. Lau et al. Johnsen et al. Kuwano and Shimizu (2006). Tang et al. Johnsen et al. They possess physical properties. Juhasz and Naidu (2000). (2005). (2005). (2005). Tang et al. Semple et al. Sabate et al. This stability can be quantiﬁed by the parameters of bond localization energy (BLE). and covalent binding (Bollag 1992) between PAHs and SOM 123 . Meckenstock et al. Chang et al. Canet et al. Samanta et al. such as low aqueous solubility and high solid–water distribution ratios. Tang et al. (2002). biotic mechanisms are responsible for removal of PAHs containing more than 3-rings and volatilization is important only for 2-ring compounds such as naphthalene and 1-methylnaphthalene (Park et al. (2005). (2005a. (2005). which stand against their ready microbial utilization. and the ionization potential. Moretto et al. (2002). Coulon et al. dissolution (Ehlers and Luthy 2003). Antizar-Ladislao et al. Moretto et al. (2005) Johnsen et al. aromatic rings whose biochemical persistence arises from dense clouds of p electrons on the ring structures which makes them resistant to nucleophilic attack (Johnsen et al. Boopathy (2003 and 2004). Betancur-Galvis et al. (2002). (2004). (2005) Namkoong et al. Doick and Semple (2003). (2006) Juhasz and Naidu (2000). Tang et al. (2005a and 2006). (2005). Taylor and Jones (2001). (2005). (2003). Chang et al. Bioremediation rates of PAHs in soil have been shown to decrease with increase in PAH residence time (aging) (Hatzinger and Alexander 1995). In general.Rev Environ Sci Biotechnol (2006) 5:347–374 Table 2 Factors inﬂuencing the bioremediation of PAHs in contaminated soils Factors pH Inﬂuence Bioavailability Mass transfer Microbial metabolism rate Bioavailability Mass transfer Microbial metabolism rate Bioavailability Microbial metabolism rate Bioavailability Microbial metabolism rate References Tang et al. (2005). (2005). (2006) 357 Temperature Microﬂora Electron acceptor Juhasz and Naidu (2000). (2005) Microenvironment Microbial metabolism rate Nutrients Microbial metabolism rate Co-substrate Microbial metabolism rate Soil properties Contaminant characteristics Bioavailability Mass transfer Bioavailability Mass transfer Microbial metabolism rate Contaminated associated PAHs are composed of fused. 2005). (2005). Pan et al. Ambrosoli et al. Gong et al. While aqueous solubility is a main structural determinant in the biodegradation of PAHs. Wrenn et al. Johnsen et al. Tang et al. Haderlein et al. Feitkenhauer et al. The aqueous solubility. adsorption (Weber and Huang 1996). (2005). Ohkuma et al. (2006). (2006) Juhasz and Naidu (2000). Sartoros et al. (2006). Sartoros et al. Semple et al. (2006) Kanaly and Harayama (2000). (2002). BLE effects ring opening. (2004) Taylor and Jones (2001). b). diffusion. Coulon et al. (2005). (2005). 1996). linear being the most unstable and angular the most stable. Tang et al. (2003). the bioavailability of PAHs decrease almost logarithmically with increasing molecular mass (Johnsen et al. and as a consequence. (2002). (2005). The partitioning (Pignatello and Xing 1996). (2005) Maliszewska-Kordybach and Smreczak (2000). Garon et al. 1990). chemisorption (Maruya et al. (2006). Betancur-Galvis et al. (2005). dictates where on the molecule oxidation is likely to occur. Johnsen et al. Semple et al. 2005). Xu et al. (2006). (2005). (2005). (2005). Taylor and Jones (2001). Johnsen et al.
electron acceptor. Low proportions of clay and silt in soil have been correlated to higher PAH bioavailability. partitioning of PAHs into organic matter in soil has been suggested as a mechanism of sequestration by which the PAHs adsorb rapidly to the external surfaces of the soil and then slowly partition into the interior regions of the solid organic matter particles. nutrients. efficiency to degrade contaminants Bioremediation system associated System configuration. Hatzinger and Alexander 1999). operation conditions such as temperature. etc. making them inaccessible to microorganisms. 1997. 2005). This process limits the release of PAHs into the bulk liquid phase. toxicity Mass Transfer Soil associated Physical and chemical characteristics. PAHs may be strongly adsorbed onto soil particles. they become potentially unavailable for microbial degradation due to their limited bioavailability as only small fractions of these compounds occur in the bioavailable water-dissolved state (Johnsen et al. 2004). but also by the biological. 1 Factors associated with the bioremediation efﬁciency of PAH-contaminated soil are believed to be responsible for the decline in their degradation over time. 2006). thus decreasing biodegradation rates (Willumsen and Karlson 1997. Soil associated The biodegradation potential of hydrocarbons is not only deﬁned by their chemical composition. soil composition. Bioavailability Fig. native soil microflora availability and its efficiency to degrade contaminants Microbial metabolism Microbial associated Native soil microflora availability. Additionally. moisture content. Furthermore. White et al. contaminant concentration. operation microenvironment. 123 . Aging facilitates movement of a contaminant into soil micropores or into the SOM leading to the transformation and/or incorporation of pollutants into stable soil solid phases (Ehlers and Luthy 2003).358 Rev Environ Sci Biotechnol (2006) 5:347–374 Contaminant associated Physical and chemical characteristics. composition. 1997) and desorption of PAHs from soil is considered to be a controlling factor in their biodegradation (Hansen et al. physical and chemical characteristics of the soil environment (BetancurGalvis et al. survival in presence of contaminant. The interactions are considered to be the major rate-limiting factors in ﬁeld scale applications. the rate of degradation of hydrocarbons and the total amount mineralized will vary depending upon the soil type (Davis and Madsen 1996). PAHs tend to interact with non-aqueous phases and SOM. especially clays (Luthy et al. As a consequence. co-substrate. Due to high hydrophobicity and soil water distribution ratios. pH.
Contrary to studies suggesting that adsorbed contaminants are not bioavailable. Harms and Bosma 1997). 1998). Bioavailability is driven by mass transfer of the contaminant from the soil phase to the solution phase (Cuypers et al. Mixing does not occur well in soil and the effective diffusion of molecules in soil may be orders of magnitude lower than in water. the turnover times are long (slow rates). 2005). Park et al. located in small pores that are inaccessible for bacteria. thereby restricting bacterial mobility (Postma and van Veen 1990. Therefore PAH-degrading populations in soil are probably mostly not growing. 2002. PAHs are poorly water soluble and heterogeneously distributed on soils and may be absorbed inside of organic particles. while the rates are in general faster for studies in which the liquid phase is well-mixed (Tang et al. recent studies indicate that soil microorganisms may be capable of degrading non-desorbable compounds (Guerin et al. and the high tortuosity of the system. 123 . but rather are in a pseudo-stationary phase where transient growth only replaces decaying cells until the habitat’s mass transfer-controlled carrying capacity is reached again (Johnsen et al. Tang et al. process operation conditions (microenvironment and conﬁguration) and the presence/absence of indigenous activity will signiﬁcantly govern the overall bioremediation process efﬁciency. Some microbial species may be capable of overcoming the binding that results in contaminant sequestration or they may produce compounds. (2001) evaluated the substrate depletion of non-desorbable naphthalene and found that this fraction. 2005). was bioavailable to bacteria. the thinner is the boundary layer and the higher the PAH-ﬂux from solid form to the bulk liquid (Johnsen et al. Mass transfer phenomena depend on diffusion. giving them an advantage over those without these abilities (Alexander 2000). 2001. predation is believed to reduce bacterial biomass in pores. increased microbial conversion capacities do not necessarily lead to higher biotransformation rates when mass transfer is the limiting factor (Bosma et al. Studies have shown that bacterial degradation is altered greatly by the physical and chemical features of the heterogeneous microbial environment (Tang et al. surfactants. 1997). The efﬁciency of degradation is often seriously impeded by two factors: poor accessibility of lipophilic compounds to microorganisms and the toxic effects of substrates upon the microorganism (Garon et al. that can enhance desorption. In studies resembling in situ degradation. genetics of the relevant organisms and enzyme stability and activity). dead-end pores. system microbiology (presence of co-substrates.8 lm. and emulsiﬁers. In soil. such as enzymes. though unable to be extracted using exhaustive aqueous solutions. 2005). It is evident from the literature that using reactors for the bioremediation of PAHs in a soil matrix supports effective degradation rates by counteracting the consequence of mass transfer and thus facilitating an increase in bioavailability by using optimized conditions. Ortega-Calvo and Saiz-Jimenez 1998. as opposed to well mixed aqueous systems. substrate consumption leads much faster to mass transferlimited conditions as the number of cells increases. which further links with the thickness of the boundary layer related to the size and shape of the molecule and the shaking velocity (Mulder et al. 2004). 2005). 1997). or otherwise occluded by the multitude of solid soil constituents (Johnsen et al. Remediation system associated Additionally. Microbial ecology. 1998). 2005). 2000). 1992. Consequently. Bacterial cells are generally excluded from pores smaller than about 0.2–0. Guerin and Boyd 1997. Park et al. a large fraction of PAH-degrading bacteria in soil are expected to be physically separated from PAH sources and therefore will depend on diffusive transport of PAHs from the sources to the cells (Harms and Bosma 1997). and in addition.Rev Environ Sci Biotechnol (2006) 5:347–374 359 Microbial associated The rate at which microbial cells can convert chemicals during bioremediation processes depends on the rate of uptake and metabolism (the intrinsic activity of the cell) and the rate of transfer to the cell (mass transfer) (Bosma et al. Reid et al. The smaller the crystals and the higher the shaking velocity. since diffusion is retarded by the solid phases.
2005). (2006) Garon et al. (2005). Johnson cost et al. Trindade et al. 2001. Goi and Trapido et al. (2005). (2005). 2005. (2004). including that contaminant sensitivity may retard the establishment of sufﬁcient biomass to facilitate degradation (Huang et al. (2004). (2005) Relatively costly Canet et al. Zhao et al. Macleod process and Semple (2005) Relatively costly compared to natural attenuation process Large land requirement Unpredictable Bacterial chemotaxins Cheaper technology and low capital cost Can be used in in situ remediation process Unpredictable Kim et al. (2004 (multiple process High maintenance integration). Kumada et al. Lee et al. (2005). Johnson et al. Bento et al. (2004). (2006) Rhizoremediation Low capital and operating associated cost phytoremediation Effective Biostimulation Low capital cost Can be used in in situ or ex situ remediation process Effective Bioaugmentation Can be used in ex situ or in situ remediation process Effective and rapid Can be used in ex situ or in situ remediation process Effective and rapid Other process integration with bioremediation Adaptation Addition of surfactants Can be used in in situ or ex situ remediation process Cheaper and simple technology Low capital and operating cost Enhances bioavalibility Relatively costly process Can be used in in situ or ex situ remediation process Zheng and Obbard (2002). Koran process et al. b). Kaimi et al. Rentz et al. Taylor and Jones (2001). Choi et al. co-metabolism. (2004 and 2005). (2005) Relatively Slow Bento et al. Venkata Mohan et al. (2006). (2006). Bordas et al. Garon et al. Xu (2005a. (2004). Garon et al. (2001a. Huang et al. (2005). (2006).360 Rev Environ Sci Biotechnol (2006) 5:347–374 Strategies to enhance bioremediation efﬁciency For bioremediation to be effective. (2006). The literature has documented various strategies. biostimulation. (2005). Trindade et al. (2005). O’Mahay et al. Sabate et al. Tang et al. chemical pre-treatment followed by bioremediation. Sartoros et al. Biswas et al. such as the addition of rhizobacteria associated with phytoremediation (rhizoremediation). bacterial chemotaxis. (2004). (2003) 123 . Ahn et al. adaptation. (2005). bioaugmentation. many limitations exist for large-scale application. Another main potential obstacle that needs to be overcome to improve the phytoremediation system is to increase the low bioavailability Table 3 Strategies used to enhance the bioremediation of PAH in contaminated soils Strategy Advantages Limitations Large land requirement Reference Huang et al. (2005). the overall rate of PAH removal and degradation must be accelerated above naturally occurring microbial processes and the key factor inﬂuencing the bioremediation rate is the bioavailability of the PAHs to the microorganisms (Johnsen et al. Gong et al. (2001). (2006). multiple process integration. Kulik et al. Huang et al. b). (2004). Rhizoremediation Although using plants for remediation of persistent contaminants may have advantages over other methods. (2001). (2001). (2005). (2004). (2005). Ohkuma et al. Wrenn et al. (2001). (2006) Ortega-Calvo et al. Suthersan 2002). Betancur-Galvis et al. Johnsen et al. (2005). enzyme mediated remediation and addition of surfactants to enhance and/or improve the degradation rate of the PAHs from contaminated soils (Table 3). Bento et al.
the number of aerobic bacteria and the amount of soil dehydrogenase activity were higher than in the root-free soil and also showed a correlation with the growth of roots. Johnson and co-workers (2004) also reported improved remediation of chrysene spiked soil by employing mixed grass–legume systems.e. Several studies have documented the application of a bioaugmentation strategy for PAH degradation in soil by augmenting with speciﬁc isolates of bacteria or fungus (Zheng and Obbard 2002. The dissipation rate of diesel oil showed a correlation with soil dehydrogenase activity in both the rhizosphere and the root-free soil. Joner et al. Bioaugmentation Irrespective of rhizobacterial addition in the phytoremediation process. 1996. the addition of contaminant-degrading organisms. 2005). Cylindrospora). This. i. Johnson et al. reported enhanced degradation of ﬂuorene in a soil slurry system by augmenting with a fungi isolate (A.and 4-ring PAHs from soil was unaffected by phytoremediation but desorption of 5and 6. 2004 and 2005. There is evidence that microbial activity in the rhizosphere or addition of microbial strains to the rhizosphere resulted in enhanced degradation of PAHs by carefully managing the complex plant– microbe–pollutant interactions (Reilley et al. Trindade et al. due to their ability to alleviate nutrient limitations and thus increase plant and root growth by increasing exudation from host roots which in turn facilitates the growth of microbial degraders or inﬂuences pollutant availability (Phillips and Streit 1996. Huang et al. In the cases where natural communities of degrading bacteria are present in low numbers or even absent. Catabolic pathways operating in natural communities reﬂect interactions between microbial species under mixed culture conditions where extensive sharing of nutritional resources is common and interaction of two or several strains is often a pre-requisite for growth and biodegradation (Heinaru et al.Rev Environ Sci Biotechnol (2006) 5:347–374 361 of pollutants due to adsorption to soil particles (Johnsen et al. bioaugmentation. while a non-fungal system required 576 h of contact time. 2005. one way of tackling low biomass availability and a lack of required contaminant degraders during bioremediation is to apply a bioaugmentation strategy. may speed up the degradation process (Van Limbergen et al. 2004. Heinaru et al. Johnson et al. The release of 3. In the rhizosphere. In a fungi-augmented system. Venkata Mohan et al. It is known that plants support microﬂora growth in the rhizosphere with much greater adaptability for different carbon sources (including pollutants) (Siciliano and Germida 1998). more than 90% of the ﬂuorene was found to be removed within 288 h of contact time. Ryegrass growth showed the dissipation threshold of diesel oil contaminated soil by 55% compared to corresponding root-free soil and the threshold reduction occurred after the development of plant roots (Kaimi et al. when the 123 . These problems can be efﬁciently counteracted by facilitating phytoremediation through judicious use of both plant growth promoting rhizobacteria and speciﬁc contaminantdegrading bacteria. (2006) examined the role of mycorrhiza during the remediation of PAHs in a mixed sward of clover and ryegrass and found enhanced loss of chrysene and dibenz[a. 2004b). 2006).ring constituents was increased by two orders of magnitude. Rhizobia play an important role in the mixed cropping system (where two or more types of plants are utilized). 2001. 2005 studied a phytoremediation system that consisted of a mixed ryegrass (Lolium perenne) and white clover (Trifolium repens) sward together with a rhizobial inoculum (Rhizobium leguminosarum) for the remediation of PAH-contaminated soil and reported enhanced PAH degradation in planted treatments that received a rhizobial inoculum. 2005. 2005). 2004).. together with microbial inoculants (symbiotic rhizobia) and they attributed this to the symbiotic association which improved plant vigor and growth thereby stimulating the rhizospheric microﬂora to degrade chrysene. 1998). (2004). Bioavailability of pollutants and survival and catabolic activity of introduced microorganisms play important roles in bioaugmentation (Heinaru et al. Bioaugmentation is believed to not only augment metabolic function but also inﬂuence the bioavailability of pollutants. Garon et al.h]anthracene in a planted soil containing a mycorrhizal inoculum. Joner et al. 2002). Garon et al. Damaj and Ahmad 1996).
2005). Co-metabolism can be deﬁned as a nonspeciﬁc enzymatic reaction. 2004. maintenance requirements. (2003) have shown the positive role of adaptation on bioremediation efﬁciency. Leahy and Colwell 1990). BetancurGalvis et al. It is evident that the longer the contaminant is in the soil. there will not necessarily be a threshold concentration of PAH. 2000. Ambrosoli et al. below which biodegradation stops (Boonchan et al. Gong et al. Bouchez et al. although possessing the capacity to mineralize each of ﬁve PAHs. 2005). 2006. Garon et al. As a consequence. 2005. or ability to produce biosurfactants and to ingest surfactant solubilized chemicals (Johnsen et al. which helps to utilize PAHs not only as electron donors. 1980. Chang et al. It has been suggested that pre-exposure of soils to concentrations greater than background are needed for adaptation to a contaminant (Spain and Van Veld 1983). an enrichment from a PAH-contaminated soil readily mineralized the ﬁve-PAH mixture. Delille et al. or when the bacteria added.362 Rev Environ Sci Biotechnol (2006) 5:347–374 application methods involve homogenization. Gong et al. Sabate et al. Macleod and Semple (2005) demonstrated considerable improvement in the derivative abilities of a soil microbial community over a range of pyrene concentrations and applications. Trindade et al. differ from the indigenous population with respect to their speciﬁc afﬁnity for the contaminant. Chang et al. but also as acceptors (Ambrosoli et al. Garon et al. Several studies have shown that the presence of co-substrates enhanced PAH degradation (Kanaly et al. 2000. b). thus leading to an increased rate of degradation. Biostimulation Biostimulation is one important strategy which has been used extensively for enhancing the bioremediation of PAHs in soil (Gijs and Sparrevik 2000. The formation of enzymes catalyzing the degradation of organic pollutants may be repressed when the cells grows on other substrates. 2004). By supplementing soil slurry systems with maltosyl-cyclodextrin (branched cyclodextrin) enhanced bioavailability of ﬂuorene resulting in effective degradation was shown (Garon et al. or intensive ﬂushing of the system. Adaptation was shown through the development of the catabolic activity of pyrene-degrading bacteria in the soil. where different carbon sources enhanced PAH degradation due to the growth of methanogens. It involves adjustments to the site by the addition of nutrients (nitrogen. Yuan et al. Recent studies by Macleod and Semple (2002). (1999) showed that augmenting with mixed cultures of two or three strains. 2004. but rather co-utilize a number of available carbon compounds (Egli 2002). phosphorus and trace minerals) while also making appropriate 123 . 2004. slurrying. Chang et al. 2005. if the cells concomitantly take up several carbon sources to maintain their biomass. Kanaly and Bartha 1999. 2005). Adaptation Adaptation is another strategy or process which facilitates increases in the oxidizing potential of the native community (Spain et al. Xu et al. ability to co-utilize natural substrates. Adaptation can occur either through the induction and/or depression of speciﬁc enzymes or by the development of new metabolic capabilities through genetic changes or by the selective enrichment of organisms able to transform the target contaminant (Spain et al. 1997. 2005). 2005. 2005. Taylor and Jones 2001. Reid et al. 1980). Taylor and Jones 2001. the greater is the level of the catabolic activity. Co-metabolism Under soil conditions. In contrast. (2002) have shown analogous results in their anaerobic experiments. Enhanced PAH degradation in the presence of acetate might be attributed to the effect of co-metabolic fermentation activities by the inoculum. but the constitutive background level of expression is often sufﬁcient for immediate consumption of the pollutant if it becomes available in low amounts (Egli 2002). with a substrate competing with the structurally similar primary substrate for the enzyme’s active site. active or passive mobility. 2002. (2002) and Lee et al. Coulon et al. adhesion behavior. 2002. 2005a. Johnsen et al. 2006. achieved limited degradation of a ﬁve-PAH mixture. bacteria may not utilize a single carbon source.
ring PAHs were degraded at 65°C by a mixed culture when hexadecane was included as a degradable solvent. 2000) and the bioavailability of soluble hydrophobic substances (Coulon et al. 2005). Zhao et al. b. Tang et al. many of the components in crude oil and diesel were reported to be degraded by psychrophilic and psychrotrophic microorganisms (Delille and Delille 2000. 2000). which facilitate or improve pollutant transfer into the water phase by decreasing the interfacial tension between water and hydrophobic pollutants. 2005). 1998. 2005. Increases in temperature lead to increases in diffusion rates of organic compounds by a decrease in their viscosity which lead to increases in the bioavailability of hydrophobic pollutants by increasing solubility. 2006. 2005. 2002). 2006) these potential co-substrates showed positive inﬂuence on bioremediation rates. 1999) and such an increase in toxicity may delay the onset of degradation (Leahy and Colwell 1990. the physical nature and chemical composition of hydrocarbons (Whyte et al. 2001a. Chung and Alexander 1999. soil moisture content. In addition to supplementing with nutrients. Niehaus et al. 2005). Eckford et al. However. Addition of surfactant can improve PAH transport to the degraders by inﬂuencing the dissolution or desorption process by attaching to the PAH-water interface (Park et al. 2002. Xu and Obbard 2003). Indeed. Betancur-Galvis et al.Rev Environ Sci Biotechnol (2006) 5:347–374 363 pH adjustments. Johnsen et al. Kim et al. b) as potential co-substrates has been tried. Field tests revealed that soil coverage with plastic sheets induced a small but permanent increase in the temperature of the surface soil and favored the degradation of alkanes over aromatics (Delille et al. Biostimulation agents are commonly used to overcome limitations in microbial growth and activity. 2005. and aeration for the proliferation of indigenous microorganisms in order to provide bacterial communities with a favorable environment by which they can effectively degrade contaminants (Salanitro et al. homogenization and dispersion of the contaminants may enhance the biodegradation rates. higher molecular reaction rates due to smaller boundary layers are expected at elevated temperatures. Johnsen et al. (2005) pointed out that the biodegradation rate was enhanced only by the addition of nitrate and phosphate in sites when the background nutrients are insufﬁcient. 2004). 2006). Bordes et al. Itavaara et al. municipal sewage (Chang et al. Feitkenhauer et al. 2005a. Baraniecki et al. Tang et al. sunﬂower oil (Gong et al. By facilitating aeration and adjusting soil water content (Sabate et al. (2005) showed the positive effect of mixed anionic–nonionic surfactants on the remediation 123 . Temperature plays a signiﬁcant role in controlling the nature and extent of microbial hydrocarbon metabolism (Nedwell 1999). Gibb et al. 2001). 2000. relatively little attention has been given to the effects of macronutrients on the biodegradation of PAHs (Betancur-Galvis et al. However. 1997). A way to disperse pollutants is by the addition of surface active compounds such as surfactants. biosolids (Betancur-Galvis et al. 2005) and chitosan (Xu et al. 2001. the increased volatilization and solubility of some hydrocarbons at elevated temperature may enhance their toxicity (Whyte et al. 2005. Zhao et al. In contrary. Stimulation with the addition of fertilizers has been shown to increase the number and activity of microbial populations. 2002). diffusion and reaction rates (Northcott and Jones 2001).to 5. Tang et al. Surfactant addition It is evident that PAH bioavailability is limited by low solubility and strong sorption/sequestration in micropores or organic matter. thus enhancing degradation in soils (Breedveld and Sparrevik 2000. 2002. Although microbial activity is generally reduced at low temperatures. (2003) showed that a mixture of 3. 2006). Rowland et al. When mass transfer is the limiting factor. 1998. 2004). and the retardation of substrate diffusion by the soil matrix (Harms and Bosma 1997. addition of agents such as bio-diesel (Taylor and Jones 2001). the use of biopile systems seems to be the most economic way to reach large increases in temperature (Delille et al. oil reﬁnery sludge (Chang et al. Careful evaluation of the temperature effects on biodegradation rates in laboratory scale experiments may give more insight into the process before going to applications in the ﬁeld. non-uniform spatial distribution of microorganisms and pollutants. Eriksson et al.
2001. Lee et al. 2005. (2005) investigated the PAH degradative potential of indigenous microorganisms in ozonated soil. Combined chemical and biological treatment for PAH-contaminated soils has been investigated (O’Mahony et al. The important merits of ozone include that it can be used either in gaseous or liquid form and after a short period of application the un-reacted ozone reverts back to atmospheric oxygen without leaving toxic residues in the soil (KasprzykHordern et al. detergent-like molecules with a hydrophilic head and a lipophilic tail which form spherical or lamellar micelles when the surfactant concentration exceeds a compound-speciﬁc. 2001). Villemur et al. pH and microbial concentrations in the soils were found to decrease with increases in ozonation time and the greatest reduction was observed in soil that was ozonated for 900 min. Ahn et al. 2001) and chemical oxidation (Choi et al. 2006. Comparatively air-dried soils showed the greatest removal of phenanthrene and presence of clay showed retarded treatment 123 . Kulik et al. non-biodegradable and biocompatible silicon oil showed enhanced efﬁciency over the corresponding control system without the oil. 2004. 2006) or in the combination with Fenton’s treatment (Kulik et al. O’Mahony et al. (2006) studied the potential of using ozone treatment with bioremediation for the removal of phenanthrene from different types of soils. Johnsen et al. 2006). 2005). Biosurfactants are small. The addition of water immiscible. 2006). 2006) with different degrees of success. 2003. However. O’Mahony et al. On contrary. O’Mahony et al. studied the inﬂuence of addition of silicone oil in soil slurry systems to promote desorption of PAHs from soil to increase their bioavailability. Goi and Trapido et al. and the initial oxidation step is biologically slow and metabolically expensive (Alexander 1999. Ahn et al. 2001. Moreover. Goi and Trapido 2004. (2000). Chemical methods offer a relatively rapid and aggressive alternative to overcome some of the problems associated with bioremediation and such methods are not sensitive to the type and concentration of contaminant (Kim and Choi 2002). ozone transforms PAHs into intermediates that are more soluble in the aqueous phase and therefore more available to microbes for biodegradation. highest removal after bioremediation was observed in 180 min-ozonated soil while a negligible removal was shown in 900 min-ozonated soil. critical micelle concentration (Johnsen et al. liquid. Hydrophobic compounds become solubilized in the hydrophobic cores of the micelles. 2005. Integration of chemical treatment prior to bioremediation was reported to be an efﬁcient strategy to enhance the degradation rates of PAH-contaminated soil. (2001) showed the reduced bioavailability of sorbed contaminants after addition of surfactant due to the rate-limiting intraparticle diffusion of contaminants that remained uninﬂuenced by the surfactant and the reduction of the water-dissolved contaminant concentration by solubilization into micelles. Ahn et al. (2006) studied the ability of pre-oxidation using ozonation and Fenton-like treatment to overcome PAH recalcitrance to biodegradation and concluded that combined chemical and biological treatment was more efﬁcient in PAH elimination in creosote-contaminated soil than in either one alone.364 Rev Environ Sci Biotechnol (2006) 5:347–374 of PAH contaminated soils and the degree of solubility enhancements by the mixed surfactants followed the order of SDS–TW80 > SDS– Brij35 > SDS–TX100. 2001. Moisture content of the soil and the presence of clay showed signiﬁcant inﬂuence on the degradation efﬁciency. Kulik et al. 2001. Kulik et al. or sorbed PAH-pools into the water phase. 2006) prior to bioremediation was reported (Table 1). Integration of solvent pre-treatment (Koran et al. Chemical pre-treatment PAHs are stable compounds. which lead to a transfer of PAH from solid. Another way to biologically increase the effective diffusion of PAH molecules would be the excretion of biosurfactants as carriers (Garcia et al. Garcia et al. They concluded that appropriate ozonation time combined with the activity of the indigenous microorganisms that survived after ozonation could enhance remediation. Kulik et al. Huang et al. 2004) where the micelles of the surfactant facilitate the diffusive transfer of contaminant through the boundary layer. 2006. More stress was observed in the application of ozone oxidation alone (Choi et al.
Anaerobic and anoxic microenvironment Strategies involving microenvironment/metabolic function in bioremediation processes signiﬁcantly inﬂuence the degradation rates and efﬁciency of degradation of PAHs. (2001) developed an integrated system to remediate soils contaminated with pentachlorophenol and PAHs by the coupling of two treatment technologies. and 4ring PAHs was observed at optimal incubation conditions of pH 8. Extensive research is being conducted in the laboratories of Dr. 2000. Y. Chang et al. 2005) were also reported to be effective. soil-solvent washing and anaerobic biotreatment (ﬂuidized bed) of the extract. and combined treatment with rye grass and rhizobacterium (Johnson et al.0 and 30°C. Koran et al. Boopathy (2003 and 2004) used anaerobic environments in soil slurry phase systems under mixed electron acceptor conditions with a good degree of success for the bioremediation of diesel fuel sediments. however appropriate precautions should be taken to optimize the conditions such that effective chemical treatment will result without inhibiting the native soil microﬂora. Shimizu. In more recent times. The experimental data revealed the effectiveness of SRC in transforming higher molecular weight PAHs to low molecular weight PAHs and suggested that the integration of aerobic processes after anaerobic operations would result in further remediation of low molecular weight PAHs. bioremediation and phytoremediation (Huang et al. 2005. (2005) elucidated the role of adsorbents such as peat-sorb and spill-sorb in adsorbing diesel oil-contaminated soil by integration with soil slurry phase bioremediation. Kuwono and Shimizu 2006) has been relatively less investigated in the case of soil bound PAH bioremediation. Johnsen et al. Boopathy 2003 and 2004. 2004). provided that suitable terminal electron acceptors (nitrate. Koran et al.Rev Environ Sci Biotechnol (2006) 5:347–374 365 efﬁciency. Among the three anaerobic conditions studied. Anaerobic degradation of 2-. application of anaerobic process for the degradation of PAHcontaminated soils has been documented (Kanaly and Harayama. on the remediation of coal-derived hydrocarbon contaminated soil under both aerobic and anaerobic conditions employing soil column bioreactors. 3-. 2002. Cassidy and Irvine (1997) showed the potential advantage of SBR operation in the degradation of diesel fuelcontaminated soil compared to continuous mode operation. The potential advent of anoxic microenvironment engineering capabilties with the arrival of sequencing batch reactors (SBR) may provide effective microenvironments for transforming soil bound PAHs. (2002) investigated the anaerobic degradation of PAHs in different types of soils under nutrient enrichment conditions and their research indicated that rapid individual PAH degradation rates were observed in a mixture of PAH substrates compared to the presence of a single substrate. 2001. sulfate. 2005). Kyoto University. Samanta et al. Biswas et al. the anaerobic microenvironment (Koran et al. The SBR process operation. The reactor achieved a removal efﬁciency of approximately 86% (naphthalene) and 93% (acenaphthene). They concluded that pre-ozonation did not enhance the subsequent biodegradation of phenanthrene in the soils and this was attributed to the release of toxic by-products in this soil during ozonation. 2005). 2000. or ferric iron) are present (Meckenstock et al. Compared to aerobic metabolic function. Ambrosoli et al. anaerobic biodegradation of PAHs is possible both through fermentative and respiratory metabolism. Meckenstock et al.reducing conditions (SRC) showed the highest efﬁciency compared to methanogenic conditions and nitrate-reducing conditions (NRC). anoxic conditions which normally exist in the soil environment have not so far been studied in the remediation of PAHs. multiple process integration. sulfate. 2002. Kuwano and Shimizu (2006) reported bioremediation of coal-derived hydrocarbon contaminated soil under SRC in soil column bioreactors. Application of adsorption as pre-treatment to bioremediation (Biswas et al. such as physical. However. 2005). 2000. otherwise 123 . It is evident from the literature that integrating chemical treatment prior to biological treatment is encouraging. Ambrosoli et al. Chang et al. photochemical. In the soil environment. (2001) studied the integration of soil solvent washing prior to anaerobic treatment in a ﬂuidized bed reactor with GAC as biomass supporting material with a good degree of success.
Garon et al. It is a complex process in which bacterial cells detect temporal changes in the concentration of speciﬁc chemicals. Fungi are generally found in aquatic sediments. SBR systems have high substrate uptake capability due to the alternation between high carbon source and starvation conditions and the systems are generally more robust to withstand the shock loads (Wilderer et al. in conjugation with soil indigenous microorganisms in the oxidation of PAHs. considerable interest is occurring in regard to the application of bacterial chemotaxis as potential tool to enhance bioremediation. fungi have extracellular enzymes involved in the degradation of a wide range of pollutants (Garon et al. which are relatively less studied. Moreover. (2004) studied the applicability of fungus (Absidia cylindrospora) as a bioaugmentation supplement in soil slurry systems to enhance ﬂuorene bioremediation in contaminated soil. either toward (positive chemotaxis) or away (negative chemotaxis) from the gradient which helps bacteria to ﬁnd optimum conditions for their growth and survival (Pandey and Jain 2002). milder reaction conditions. Application of enzyme biocatalyst treatment in the remediation of PAHcontaminated soil is recently ﬁnding its place (Table 1). dibenz[a. respond behaviorally to these changes and then adapt to the new concentration of the chemical stimuli (Samanta et al. 2002). Results showed enzymatic transformation of anthracene in the soil matrix to a less toxic intermediate (anthraquinone) indicating the applicability of fungus oxidation. 2001). Chemotaxis is deﬁned as the phenomena of bacterial movement under the inﬂuence of a chemical gradient. 2004). They observed an enhanced oxidation by 43% in the presence of fungus while limited oxidation occurred for high molecular weight PAHs (chrysene. and could thus play an important role in the biodegradation process (Parales and Harwood 2002). may have signiﬁcant advantages over bacterial systems for soil bioremediation and in particular for PAH transformation. nitrogen and energy. 2003) used white rot fungus (Phanerochaete chrysosporium) synergistically. 2002). The application of SBR operation to PAH bioremediation may have the advantage of providing an anoxic microenvironment integrated with an aerobic microenvironment in single reactor system (Venkata Mohan et al. benzo[a]pyrene. with respect to the composition and metabolic properties of the microbial population by controlling the distribution and physiological state of the microorganisms (Wilderer et al. terrestrial habitats and surface waters and they have speciﬁc advantages over bacteria where fungal hyphal growth may penetrate throughout the contaminated soil to reach PAHs (Aprill and Sims 1990). Several studies showed evidence that motile bacteria are chemotactically attracted to environmental pollutants that they subsequently degraded. 2001). Bacterial chemotaxis Recently.h]anthracene and benzo[g. microorganisms have developed effective mechanisms that help them to regulate their cellular function in response to changes in their environment (Hoch 2000).366 Rev Environ Sci Biotechnol (2006) 5:347–374 called periodic discontinuous operation. greater stereospeciﬁcity and the capability to catalyze reactions at relatively low temperature and in the entire pH range (Venkata Mohan et al.h. Through evolution. Zheng and Obbard (2002. Laccases and phenoloxidases catalyze the oxidation of PAHs in the presence of mediator compounds that act as ‘‘electron shuttles’’ between the free enzyme and the substrate. may have potential to inﬂuence the microbial system by enforcement of controlled short-term unsteady state conditions leading in the long run to stable steady state conditions.2azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) as mediator (Venkata Mohan et al. 2004a and 2006) and also have the advantage of integrating two metabolic functions.i]perylene). Enzyme-mediated bioremediation The catalytic action of enzymes is extremely efﬁcient and selective compared to chemical catalysts due to higher reaction rates. In conjunction with their biodegrada- 123 . Laccase from Pleurotus ostreatus1804 was studied to evaluate its potential to oxidize anthracene-contaminated soil in a sole-substrate system in the presence of 2. Chemotaxis can increase an organism’s chances of locating useful sources of carbon. Fungi biocatalyst systems. 2004b).
3 representative Pseudomonas strains were used for chemotaxis studies with PAHs (naphthalene. Fenton. research addressing the possibility of a role for chemotaxis in the biodegradation of PAHs was documented (Ortega-Calvo et al. Because the chemotaxis of bacteria seems to aid in the degradation of toxic compounds. When land farming was carried out prior to phytoremediation so that a new layer of soil was exposed to sunlight. potentially improving the growth of aerobic soil bacteria. bacterial chemotaxis towards pollutants might contribute to the ability of bacteria to compete with other organisms in the environment and to be efﬁcient agents for bioremediation (Parales and Haddock 2004). including solubilization and electron transfer (Fukushima et al. which contain a variety of functional groups and structural moieties and the chemical characteristics vary by soil type (Gaffney et al. and pyrene) along with bacterial lipopolysaccharide and root exudates. Recently. Fukushima et al. the molecular basis of this phenomenon is a fertile and useful area for future research. Such enhancement was attributed to the coupling of radical species from organic pollutants with humic substances and in contrast. biomimetic catalytic systems were investigated recently for remediation of soilbound contaminants by mimicking the transformations of xenobiotics (Marimoto and Tatsumi 1997. 1997). Over a 4-month period. Land farming may also oxygenate the soil. Taking advantage of this phenomenon. especially in humic soils.g.. Due to the presence of p-orbital structures in intact PAHs. In radical-based oxidative reactions (e. 2003). Multiple process integration One of the major challenges for organisms to degrade intact PAHs is the initial oxidation step. Huang and co workers (2004) developed a multiple process technique. particularly in regard to soil contaminated with PAHs. Fukushima et al. Humic substances are heterogeneous polyelectrolytes. a large thermodynamic barrier to the initial biological oxidation step is created (Huang et al. thereby resulting in faster degradation of contaminants. inhibition was attributed to humic substances serving as scavengers of active oxygen species. 2003). 2003). the PAHs brought to the surface were photooxidized (Huang et al. 1996). microbial remediation and phytoremediation for the remediation of creosote-contaminated soil. coordinated regulation of bacterial chemotaxis toward almost all toxic compounds and their respective mineralization and/or transformation indicate that this phenomenon might be an integral feature of degradation (Pandey and Jain 2002). integrating a phytoremediation system composed of physical (volatilization). the biomimetic catalytic systems may also be evaluated for the remediation of PAH-contaminated soil. 2000). introduction of contaminant degrading bacteria. plant growth promoting rhizobacteria and plant growth of a contaminant-tolerant tall fescue (Festuca arundinacea). Due to its speciﬁc advantages. The applied techniques were land-farming (aeration and light exposure). 2003. Fukushima and Tatsumi 2001. Thus. Out of 20 motile strains capable of degrading different PAHs. which may have acted as strong oxidants to organic pollutants (Klausen et al. In this direction. anthracene. 2003). 2001). humic substances also inﬂuence the removal of organic pollutants via biomimetic catalytic systems (Fukushima et al. photochemical (photooxidation). In such cases photochemical pretreatment of contaminated soil may facilitate the bioremediation of PAHs because they can be readily photooxidized by sunlight to quinones and hydroxy quinones (Mallakin et al. phenanthrene. the average efﬁciency of removal of 16 123 . enzymatic. 2004). OrtegaCalvo and co-workers (2003) for the ﬁrst time evaluated chemotaxis as a bioavailability-promoting trait in PAH-degrading bacteria from the soil rhizosphere. Fukushima and Tatsumi 2001. Indeed. The results indicated that chemotaxis is a relevant mobilizing factor for PAH-degrading rhizosphere bacteria. the removal of organic pollutants may be enhanced or inhibited in the presence of humic substances (Morimoto and Tatsumi 1997. humic substances play important roles in the remedial process via a variety of interactions. and MnO2 oxidations).Rev Environ Sci Biotechnol (2006) 5:347–374 367 tive capacities. Biomimetic catalysis In the soil environment. Parales and Haddock 2004).
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