Andrew R. Autry, Ph.D., Mark Shearon ENSITE Inc South Royal Atlanta Drive Tucker, Georgia 30084
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1 RAPID BIODEGRADATION OF POLYAROMATIC HYDROCARBONS IN CREOSOTE CONTAMINATED SOIL I -! pa/' Andrew R. Autry, Ph.D., Mark Shearon ENSITE Inc South Royal Atlanta Drive Tucker, Georgia Brian Archer Applied Ecologies Inc West Georgia Street Vancouver, British Columbia V6E 3V7 Introduction Bioremediation refers to the use of microorganisms, both bacteria and fungi, to degrade organic constituents in contaminated media that would otherwise need to be disposed of by more classical remediation/waste management techniques. The use of bioremediation applications has previously been heavily concentrated in the wastewater treatment industry. One exciting, fairly recent application of bioremediation technologies is the use of these technologies as remedial alternatives for the soil of a site contaminated with organic compounds. In fact, this application has been used with a great deal of success on petroleum fuel contaminated where the contaminants of interest included gasoline, diesel fuel, jet fuel and crude oil. Organic compounds that are treatable by bioremediation include polyaromatic hydrocarbons (PAHs). PAHs are the principal organic contaminants of concern in creosote contaminated soil. PAHs consist of two or more fused aromatic rings, and can be classified, with regard to chemical structure, based on either the number of rings present in the compound or on the molecular weight of the compounds. As is true with many other organic compounds, lower molecular weight PAHs, those that contain a smaller number of rings, are more readily biodegradable and are therefore biologically degraded faster than are heavier weight PAHs which contain a larger number of ring structures. For example, naphthalene, a 2 ring PAH, is more rapidly degraded than is benzo(a)pyrene, a 5 ring PAH.
2 PAH Biodemadation PAHs are biologically degraded by both bacteria and fungi in natural systems. The pathways for degradation are fairly complex, and are specific for each type of PAH compound. For example, naphthalene, a two ring PAH, is degraded in the following manner. An oxygenase enzyme inserts molecular oxygen into the naphthalene molecule; the ring that was initially attacked is then attacked again and opened, converting the parent compound to salicylate, which is then converted to catechol and oxidized to biomass by either the a-keto acid or /3-keto adipate pathwa?'. Phenanthrene, a three ring PAH, is sequentially attacked using oxygenase enzymes and converted to a naphthaldehyde intermediate, which is converted to an o-phthalic acid intermediate, which is in turn converted to protocatechuate; protocatechuate is then oxidized to biomass and C02 by the same pathways that are used to oxidize catechol6,'. Anthracene, an isomer of phenanthrene, is biologically degraded by a similar pathway'. The biochemistry of PAHs possessing more than 4 rings is not as well defined as it is for the lower molecular weight PAHs. Generally, the first steps in degradation involve ring sequential ring oxidation and cleavage by oxygenase enzymes, followed by a conversion to diol intermediates which are then biologically degradedg. It is well established that these higher order PAHs are usually cometabolized in nature'o*''*'2. Cometaboiism means that a microorganism will not grow or oxidize a specific compound unless a structurally similar, yet more readily utilizable compound (its cometabolite) is present, The cometabolite serves to induce the synthesis of "gratuitous" enzymes that, although synthesized to degrade the cometabolite, are unable to discern the difference between the cometabolite and the target compound, and attack each nonspedfically. Cometabolites for the higher order PAHs include biphenyl, naphthalene, fluoranthene, benzene, xylene, and toluene. Soil bacteria and fungi that can biologically degrade various PAHs are listed as follow^^^^'^. Naphthalene: Phenanthrene: Anthracene: Fluoranthene: Fluorene: Benzo (a)pyr ene : Pseudomonas putida, P. jluarescens, P. cepacia Flavobacterium sp., Beijerinckia sp., P. putida Flavobacterium sp., Beijerinckia sp. P. paucimobih, Alcaligenes denitri'cans P. versiculatis Beijerinckia sp., Cunninghamella elegans It should be noted that the species presented above are representative of those that have been documented to degrade PAHs; many other bacterial and fungal species are known to degrade PAHs. Furthermore, most of the PAH degrading organisms are common soil isolates and are likely present in any given soil sample. 4:4
3 Rate Limiting Factors for Bioremediation Amlications While it is well established that PAHs are biologically degraded in highly controlled, optimized, laboratory conditions, frequently, in the field, rate limiting factors can lower the rate of biodegradation to the extent that bioremediation will not be a viable option for site remediation. These rate limiting factors can be either biochemical/microbiological or environmental in nature. Microbiological and biochemical limiting factors exert the most direct effect on the biodegradation rate. The principal limiting factors that are biochemical in nature for field-scale applications include a lack of any organisms possessing the metabolic pathways required for degradation, and, for compounds that are cometabolized, a lack of cometabolites to induce the synthesis of degradative enzymes. Owing to the large numbers of bacterial species capable of oxidizing organic contaminants, including PAHs, and their wide distribution in nature, absence of a bacterial or fungal species capable of degradation would likely never occur in a soil system. Environmental factors limiting aerobic biodegradation rates include temperature, oxygen supply, contaminant bioavailability, contaminant chemical structure, and soil chemistry. Optimal temperature for biodegradation is 27 C? In ex-situ applications, seasonality is therefore a factor. Because the fastest biodegradation rates are noted for aerobic biological processes, oxygen supply to soil bacteria becomes a critical limiting factor. If there is not an adequate supply of oxygen, the aerobic respiratory processes responsible for contaminant mineralization will cease to function, and degradation of organic contaminants will halt. In fact, oxygen limitation has been cited as the critical rate limiting factor for high rate bioremediation applications16. Soil nutrient status, primarily as nitrogen and phosphorus (N and P) content, can influence the biodegradation rate also. Frequently these inorganic nutrients are present in growth limiting concentrations in soil systems, and they influence biodegradation by directly impacting on the microbial growth rates. The availability of the contaminant for biodegradation is governed by the soil chemistry of the site and can also be a major rate limiting factor. For example, soils with large amounts of clay can adsorb contaminants, thus effectively removing them from the potentially biodegradable pool. Furthermore, many of the higher molecular weight PAHs (e.g.-benzo(a)pyrene) are extremely water insoluble and must be solubilized before effective biological degradation can occur. Unmitigated, lack of contaminant bioavailability will likely be the critical rate limiting factor for PAH biodegradation in a soil ecosystem. The use of a surfactant has proven very successful in enhancing the biodegradation of heavier PAHs. Additionally, bacterial cells themselves are frequently adsorbed onto clay and other soil material. Adsorbed bacteria are incapable of mediating organic contaminant degradation. These cells must be desorbed if biodegradation of organic contaminants in soil is to occur. The chemical structure of the contaminant can directly affect the biodegradation rate. While all organic compounds will be biodegraded to some extent in a soil system, the rate and final concentration are partially dependent on the structure of the molecule. Generally, the more complex the contaminant, the more difficult the degradation, and, therefore, longer time periods are required for degradation to occur.
4 PrinciDles of SafeSoil Control of Limiting Factors The commercial success of any field-scale bioremediation project will depend on the rate of biodegradation. As previously stated, all organic compounds will be degraded to a certain extent in soil systems. The key to successful bioremediation projects involves controlling the natural limiting factors so that the desirable rate is obtained. The speed of any bioremediation process is dependent on natural biodegradation rates. Increasing these rates will lower the time requirement for biological degradation. These natural rates are in turn dependent on natural rate limiting factors, both biochemical and environmental. SafeSoil evolved as a solution to controlling these rate limiting factors as a means to maximize biodegradation rates and yield the fastest, most reliable biologically mediated remedial alternative. The issue of inorganic nutrient (N and P) limitation is overcome by the inclusion of excess quantities of nitrogen and phosphorus (as both organic molecules and inorganic salts) in the SafeSoil additive. The issue of contaminant toxicity to indigenous microflora is partially overcome by the inclusion of readily utilizable C sources (as simple sugars) in the SafeSoil additive. The issue of efficient soil aeration is overcome by the proprietary treatment process, which physically encapsulates air in the treated soil matrix, thus maintaining aerobic conditions. The issue of contaminant and microbial cell mobility is accounted for by the inclusion of mild, naturally-occurring surfactants in the additive, which serve to make the hydrophobic compounds present in the soil more water soluble and more biologically available. The speed of the process is therefore controlled through manipulation of the rate limiting factors. The issue of cometabolite limitation is partially compensated for by the presence of preformed enzymes whose synthesis need not be induced by the presence of a cometabolite. Development of the SafeSoil Biotreatment Process In any given soil system, a variety of biological, chemical, and physical parameters interact to mediate contaminant removal and oxidation. The nature and relative proportion of contaminants removed by each type of process (biological, chemical, and physical) will be site-specific and will depend on a variety of factors, including indigenous bacterial population sizes, soil chemistry, and the chemistry of the pollutants under consideration. The most effective bioremediation technology is one which enhances biologically mediated degradation by maximizing the capacity of other effects (chemical and physical) for contaminant removal. Consistent with this idea, SafeSoil represents the first truly integrated approach to on-site remediation, combining the most effective biological components with the most effective physical/chemical treatments for the best and fastest possible removal of contaminants. The nature and relative proportion of contaminants remedied by each component of the process (biological or physical/chemical) will be site-specific. The biological component of the 416
5 approach is the portion mediating the majority of the contaminant removal and has for that reason been considered in extreme depth. SafeSoil evolved by extracting the best elements of various other forms of bioremediation. For example, composting adds organic nutrients (in the form of wood chips); SafeSoil adds them as simple sugars and proteins. The addition of inorganic nutrients and water is a common practice in landfarming; SafeSoil has some inorganic nutrients included in the additive. Bioreactors offer effective mixing and hence more efficient mass transfer of contaminants; SafeSoil accomplishes this task, and SafeSoil does so without generating the high liquid: solids ratios observed with bioreactors. With the advent of modern molecular biology, many other biological processes are capable of being applied to ecological problems. These include the use of preformed, immobilized enzymes to mediate biochemical transformations and the use of monoclonal antibodies and genetic engineering techniques to indicate whether a bacterial population is actively degrading hydrocarbons in nature. SafeSoil also adds preformed oxygenase enzyme to mediate the initial oxidation of various compounds. Figure 1 summarizes the various components of the SafeSoil treatment process. Technology Description SafeSoil is a rapid ex-situ bioremediation process that involves excavation of contaminated soil, power screening for the removal of debris and break-up of larger soil aggregates, transport of the screened soil to a paddle shaft mixer (2.5 cubic yard capacity), mixing the contaminated soil with a proprietary, nutrient-enriched additive in the mixer, placement of the treated soil in "curing" piles on site, and "curing", during which time biodegradation by naturally occurring microorganisms utilizing biochemical pathways mediated by enzymes, will occur. Safesoil, in contrast to most other ex-situ bioremediation technologies, does not
6 require any further soil processing. All nutrients and initial oxygen requirements are supplied during initial processing. The air entrainment feature of SafeSoil creates a honeycomb-like lattice throughout the soil through which air can freely diffuse, thus enabling aerobic conditions to persist in the treated soil throughout the curing period. Safesoil adds a proprietary, nutrient-enriched additive to the soil to mediate and enhance biodegradation of organic contaminants. This additive contains the following components: Nitrogen sources Phosphorus sources Preformed enzymes Surfactants + Simple sugars Safesoil adds both nitrogen and phosphorus in an inorganic form to supply immediately available nitrogen and phosphorus to bacterial populations deficient in that nutrient. SafeSoil also adds organic nitrogen in the form of protein to provide a time-released source of N for long-term bacterial N requirements. The first step in most aerobic biodegradation reactions is mediated by an oxygenase enzyme. SafeSoil includes a preformed oxygenase enzyme in the additive to preclude the need for de novo microbial enzyme synthesis, frequently a time-consuming process. Surfactants are added to solubilize hydrophobic compounds and make them more biologically available. Simple sugars are added to provide compromised microbial populations with an immediately utilizable carbon source, in order to restore these populations to full health and metabolic capability. Preformed enzymes mediate initial rapid biodegradation of contaminants. Later, during the curing portion of treatment process, nutrients applied during initial processing encourage the growth of indigenous microflora, which degrade organic molecules during the process of growth. The latter mechanism is the more conventional route of bioremediation. The route for destruction of organic contaminants, including PAHs, by aerobic biological processes, is oxidation of the organic molecules to C02 and structural carbon (as microbial biomass). SafeSoil relies solely on the indigenous microorganisms of the site to mediate biological degradation of organic compounds and does not add exogenous microbial populations to enhance biodegradation. Case Study Project History A bench-scale treatability test was conducted to test the effectiveness of the Safesoil Biotreatment Process on soil of a former wood preserving facility in southern Florida. Soil of this site had become contaminated with creosote as a consequence of previous wood treatment operations. Soil of this site was sandy silt, and no metals were present to interfere with biological activity. The property owner and consulting engineering firm 418
7 agreed that bioremediation would be an ideal remedial technology for site closure. A bench-scale test was conducted to determine the length of time that would be required for remediation to occur, as well as the endpoint PAH concentrations that could be achieved within that time frame. The test consisted of the treatment of approximately 10 kg of soil in a small scale mixer with the SafeSoil additives in a manner and concentration consistent with that of anticipated full-scale operations. The mixed, treated soil was placed on stainless steel pans for the curing portion of this project. Composite samples were collected and analyzed for PAH content by EPA Method 8270 and for soil bacterial population density by the standard plate count technique. This sampling was conducted prior to treatment (n=3), in order to establish baseline PAH and biomass levels, and on various days posttreatment (n=2), in order to establish changes in each parameter as a function of posttreatment curing time. Treatment Results For the purposes of data analysis, PAHs were classified based on the number of rings present in each compound. The PAH classification scheme for this project is summarized by Table 1. Table 1. Rinp Number Two Ring Three Ring Four Ring Five Ring Classification of creosote-derived PAHs based on ring number Specific Compounds Naphthalene, a-methyl naphthalene Acenaphthylene, acenaphthene, dibenzofuran, phenanthrene, anthracene Fluoranthene, pyrene, benzo(a)a.nthracene, chrysene Benzo@)fluoranthene, benzo(k)fluoranthene, benzo(a)pyrene Treatment Results SafeSoil was effective at mediating the biodegradation of creosote derived PAHs for soil of this site. Two ring PAHs were the lightest molecular weight organic contaminants present in the soil and these were reduced 85% within a time frame of 30 days, from an initial level of 218 ppm to a day 30 level of 34 ppm (Figure 2). This concentration was further reduced, albeit at a lower degradation rate, to 30 ppm by day 100 (Figure 2). 4i9
8 Figure 2. SafeSoil Enhanced Biodegradation of Two Ring PAHs Curing time (days) - 2 ring PAH With regard to three ring PAHs, rapid degradation was also observed, with removal of 92% of the 3 ring PAHs present initially, from a pretreatment level of 688 ppm to a day 44 level of 61 ppm (Figure 3). This level was not significantly reduced after 100 days curing time. Figure 3. SafeSoil Enhanced Biodegradation of Three Ring PAHs PAH Concentration (ppm) _....._ _ c Curing time (days) ring PAH
9 A similar statement can be made for the four ring PAHs, which were reduced 75% in concentration after 74 days curing time (Figure 4). Initial levels of four ring PAHs were approximately 385 ppm (Figure 4). Figure 4. SafeSoil Enhanced Biodegradation of Four Ring PAHs PAH Concentration (ppm) 600 ' * Curing time (days) -e 4 rlng PAH For the five ring PAHs, there was some degradation initially occurring, and by day 100,88% of the initial levels of five ring PAHs had been removed (Figure 5). Initial levels of five ring PAHs were approximately 34 ppm (Figure 5). Figure 5. SafeSoil Enhanced Biodegradation of Five Ring PAHs PAH Concentratlon (mm) ""I a Curing time (days) 5 rlng PAH 421
10 PAHs were biologically degraded in a sequential manner for this study. That is, two ring PAHs were rapidly degraded to below a threshold concentration first. Once that threshold concentration had been reached, rapid degradation of three ring PAHs was initiated. The threshold concentration is the concentration of specific compounds below which biodegradation of these compounds proceeds at a very low rate. Below this concentration, indigenous microflora are no longer using these specific compounds as their principal carbon and energy source. Once the three ring PAHs had been biologically degraded to below the threshold concentration specific for three ring PAHs, rapid biodegradation of four ring PAHs was initiated. After the four ring PAHs had been reduced in concentration to below the threshold concentration specific for four ring PAHs, rapid biodegradation of five ring PAHs was initiated. This phenomenon is an example of diauxic growth, often noted for bacteria. Bacteria will preferentially utilize more easily degradable compounds (primary substrates) first; once these primary substrates have been depleted to a concentration below which their degradation occurs at a rapid rate, degradation and utilization of more recalcitrant compounds (secondary substrates) will occur. This effect has previously been noted for many organic compounds, and is confirmed by results of the current study in that all types of PAHs exhibited approximately the same removal on a percentage basis, but each required different lengths of time for removal to occur. For two ring PAHs, bacteria required only 30 days to effect this removal; for three ring PAHs, bacteria required 44 days to effect a similar removal; for four ring PAHs, 74 days were required, and for five ring PAHs, 100 days were required. There is some overlap in this sequential oxidation scheme, in that there was some oxidation of three, four, and five ring PAHs that occurred concurrently with two ring PAH biodegradation. This is largely due to the presence of some microorganisms that lack enzymes specific for two ring PAH (e.g.- naphthalene, a-methyl naphthalene) degradation that initially utilized the next most readily utilizable organic compounds (e.g.-three and four ring PAHs). It should be noted that the residual PAH concentration still present in the soil after 100 days will eventually be biologically degraded; the sampling frequency employed for this study was based on the achievement of a specified action limit, and once that limit had been achieved, no further sampling was required. When total PAH concentration, defined as the sum of the two, three, four and five ring PAH concentrations, is considered, a consistent decline was noted. Initial levels of total PAHs were 1323 ppm;' day 74 levels were 195 ppm, reflecting an 85% reduction in total PAH concentration over a 74 day time period (Figure 6). Total PAH concentration did not significantly change between days 74 and 100, and this is largely due to the fact that five ring PAHs, which were the principal contaminants being degraded during this time, comprised such a small percentage of the total PAH level that reductions in five ring PAH concentration did not significantly change the total PAH concentration. 422
11 Figure 6. SafeSoil Enhanced Biodegradation of Total Creosote Derived PAHs PAH Concentration (ppm) _ _......_. _._ Curing time (days) + Total PAH Total PAH Is the sum of the and 5 fin&! M Hs Soil aerobic bacterial population sizes, an indicator of soil biological activity, increased greatly in size (up to 80 fold) following SafeSoil treatment (Figure 7), and then declined in a manner coincident with PAH removal, confirming the biological nature of SafeSoil mediated PAH removal. Figure 7. Effect of SafeSoil on Soil Bacterial Population Density Soil Bacteria (CFUlp) 1.000E* E* Curing time (days) Aerobic Bacteria 423
12 Summary The data confirm that SafeSoil was effective at mediating PAH removal from creosote contaminated soil. Sequential degradation of various types of PAHs was noted and this is a variation of bacterial diauxic growth. Large increases in soil bacterial biomass were noted concomitant with PAH biodegradation, and these confirm the biological nature of the process. SafeSoil was proven effective as a remedial alternative for creosote contaminated soil, and this technology is ready for field applications on creosote contaminated sites. References 'Autry, A.R., Shearon, M.S., and Archer, B Development, testing, and field implementation of Safesoil": a rapid ex-situ bioremediation technology. In: Proceedings of the National Research and Development Conference on the Control of Hazardous Materials, H. Bernard (ed), pp *Compeau, G.C., Mahaffey, W.D., and Patras, L Full-scale bioremediation of contaminated soil and water. In: Environmental Biotechnology for Waste Treatment, G. Sayler, R. Fox, and J.W. Blackbum (eds), pp Autry, A.R., Shearon, M.S., and Archer, B Bioremediation of petroleum hydrocarbon contaminated soil by the Safesoil treatment process. In: Proceedings of Hazmacon '91, T. Bursztynsky (ed), pp Cerniglia, C.E Microbial transformation of aromatic hydrocarbons. In: Petroleum Microbiology, R. Atlas (ed), pp 'Smith, M.R The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation 1: Cerniglia, Smith, 'Cerniglia, 'Gibson, D.T. and Subramanian, V Microbial degradation of aromatic hydrocarbons. In: Microbial Degradation of Organic Compounds, D.T. Gibson (ed), pp "Smith,
13 USE OF ABOVEGROUND BIOREACTORS FOR THE TREATMENT OF CONTAMINATED GROUNDWATER / / / ABSTRACT Biological treatment is currently in us 0 sites in the United States, primarily for the innocuous end chemical addition costs. Accordingly, if the biological treatment can be the most cost-e long-term liability perspectives. Aboveground bioremediation systems can b to treat contaminated groundwater. T which the biomass grows as a biofilm, system requires minimal operator atte inants in a given water stream are biodegradable, echnology from both the low operating cost and with attached growth fixed-film bioreactors e influent streams. Many applications of the installation compounds, such as phenol and a1 is often cost-effective when air emis system have involve be limited, in contr ng highly soluble biodegradable of volatile contaminants INTRODUCTION Biological treatment is environment. For abo advantage over mass a standard technology for treating organi treatment of contaminated groundwater, bi 426
14 "Cerniglia, C.E. and Heitkamp, M.A Microbial degradation of polycyclic compounds (PAH) in the aquatic environment. In: Metabolism of PAHs in the Aquatic Environment, V. Varanasi (ed), pp '*Cerniglia, Cerniglia, Smith, %chneider, D.R. and Billingsley, R.J Bioremediation: a desk manual for the environmental profmsional. Pudvan Publishing, Northbome IL. 16Devinny, J.S. and Islander, R.L Oxygen limitation in land treatment of concentrated waste. Hazardous Wastes and Hazardous Matenah 6: Smith,
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