ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

Open Access

Okere and Semple. J Bioremed Biodegrad 2012, S:1 DOI: 10.4172/2155-6199.S1-006

Open Access

Research Article

Keywords: Bioavailability; Biodegradation; Deserts; Temperate;Tropical; Soils

Introduction

Polycyclic aromatic hydrocarbons (PAHs) are an important class of hydrophobic organic contaminants (HOCs) widely found in the environment. They have been studied with increasing interest for more than twenty years because of more findings about their toxicity, environmental persistence and prevalence [16,20,57,83,147,149].

PAHs are produced into the environment through natural and anthropogenic sources. Natural sources include their formation as biogenic precursors during early diagenesis [22,76,140] and production by plants and termites [15,75,140]. Production from anthropogenic activities such as petroleum oil refining, combustion, transportation and spillage and the use of domestic heaters are however more significant [51,147]. PAHs are widely distributed in the environment as products of incomplete combustion, and have been detected in various environmental samples including air [51], water [120], sediments [152] and soil [67,68].

The soil environment appears to be the ultimate sink for PAHs as, globally, soils store more than 90% of the total PAHs found in the environment [1,147]. PAHs are delivered into background soils mainly by atmospheric deposition [68,133,144], but the proximity to point sources and soil properties (mainly soil organic matter and total organic carbon) have been found to affect concentrations [21,69]. Moreover, high concentrations of PAHs have been found in urban and roadside soils [69,88], with even higher concentrations found at sites impacted by organic contamination [94,103]. PAHs have been shown to accumulate mainly in the organic layer in soils [126], with a positive correlation between soil PAHs and soil organic matter reported [94,146]. Knowledge of soil PAH concentrations can be used to estimate PAH sources to soil. Since soils may act both as a sink for high molecular weight (HMW) PAHs and as a source of low molecular (LMW) PAHs to the atmosphere, this knowledge is important [37,131,151]. In fact, PAH concentrations in soil have been reported to significantly correspond with levels in air [131], house dust [33] and urban street dust [124]. PAHs differ from other groups of organic compounds because of their unique physical and chemical properties. These properties control their transport and behaviour in the environment.

Physico-Chemical Properties of PAHs

Individual PAHs differ significantly in their physical and chemical properties (Table 1) and can be divided into low molecular weight (e.g., 2 to 3 ring PAHs like naphthalenes, fluorenes, phenanthrenes, and anthracenes) and high molecular weight PAHs (4 to 7 ring PAHs from chrysenes to coronenes). Generally, LMW PAHs are more soluble, and volatile and less hydrophobic [81,153]. As a result, they are more easily lost from the environment. Many HMW PAHs (e.g.benzo[a]pyrene and benzo[b]fluoranthene, benzo(e)pyrene and benzo(j)fluoranthene) are structural isomers with the same molecular weight but different structural formulae. Purified HMW PAHs (five benzene rings and above) are solids and generally do not volatilize because their melting points are greater than 100oC [81]. HMW PAHs also have large resonance energies which make them thermodynamically stable though they can be photo-oxidized at various aromatic positions to form quinones. An example is when benzo[a]pyrene undergoes photolysis. Increase in hydrophobicity endows these chemicals with high octanol: water partition coefficients (kow) as a result of which they tend to adsorb to soil organic matter, are less bioavailable and therefore are not easily degraded giving rise to greater persistence in soil. High molecular weight PAHs are therefore naturally recalcitrant in the soil environment [25,58].

Fate and Behaviour of PAHs in Soil

When PAHs enter soil, they can be lost or removed by a number of physical, chemical or biological processes. For example, photo-

*Corresponding author: Kirk T Semple, Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK, E-mail: k.semple@lancaster.ac.uk

Received November 10, 2011; Accepted December 23, 2011; Published December 26, 2011

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Copyright: © 2012 Okere UV, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

AbstractPolycyclic aromatic hydrocarbons (PAHs) are an important class of organic contaminants ubiquitously found in

soils globally. Their fate in soil varies depending on both soil properties and chemical structure; however, microbial degradation represents the most significant means of loss. It is therefore important to understand the factors that control PAH biodegradation in different soil environments. This review considers PAH biodegradation in “pristine” Antarctic, temperate, tropical and hot desert soils. Pre-exposure of indigenous microbes to PAHs is important for the development of the capacity to degrade PAHs so PAH sources to these soils are discussed. The role of PAH bioavailability in the biodegradation of PAHs in ‘pristine’ soils from the different climatic regions is also discussed as well as the factors that control it. Soil organic matter, water content and temperature are seen as the main environmental factors that control PAH bioavailability in these soils. With most studies focussing on temperate soils, there is need for more research on soils from other climatic zones.

Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic RegionsUchechukwu V Okere and Kirk T Semple*Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK

Journal of Bioremediation & BiodegradationJo

urna

l of B

iorem

ediation & Biodegradation

ISSN: 2155-6199

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 2 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

PAH Molecular Weight Structure Melting Point (oC) Water Solubility(mg litre-1) Log Kow

Naphthalene 128.2

79 – 82 320 3.5

Acenaphthene 152.2

95 5.3 3.95

Acenaphthylene 152.2

72-82 3.93 3.94

Fluorene 166.2

115 - 16 1.85 4.28

Phenanthrene 178.2

99 1.24 5.62

Anthracene 178.2

218 0.64 5.33

Fluoranthene 202.3

110 0.25 4.62

Pyrene 202.3

156 0.14 4.47

Banzo[a]anthracene 228.3

158 0.01 5.30

Chrysene 228.3

255 0,002 5.30

Benzo[b]fluoranthene 252.3

168 - 5.74

Benzo[k]fluoranthene 252.31

215 - 6.06

Benzo[a]pyrene 252.3

179 0.0038 5.74

Benzo[ghi]perylene 276.3

273 0.00026 6.20

Dibenzo[ah]anthracene 278.35

262 0.0005 6.84

Indeno[1,2,3-c,d]pyrene 276.3 163 Insoluble 6.20

Table 1: Physical and chemical properties of selvected PAHs.

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 3 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

oxidation and/or volatilization to the atmosphere, leaching to ground water, irreversible sorption to soil organic matter, uptake by plants and microbial degradation are some of these processes [109,122] (Figure 1). The rate at which these loss processes occur and the extent to which a PAH is affected is dependent on a number of factors including soil type (mineral and organic matter contents), the physico-chemical properties of the individual PAH, soil temperature and moisture, redox potential, nutrients availability, presence and activity of degrading microorganisms and bioavailability of the PAH to degrading microorganisms. [99,108].

Figure 2 shows the possible fate of a PAH in soil [122]. Compounds with low Kow, high water solubility and volatility are more mobile and degradable. As a result, they are lost rapidly when they enter the soil (A). Many contaminants however, show a biphasic behaviour where though losses are clearly occurring, the rate and extent of the losses decrease as contact time between the soil and contaminant(s) increase (B). This process has been termed ageing [59,117]. C represents the loss pattern of a recalcitrant PAH in soil [122]. The major biotic means by which PAHs are lost from soils is through degradation by bacteria and bioavailability is crucial to PAH biodegradation in soil [23,30,100,123].

Bioavailability/Bioaccessibility and Biodegradation of PAHs in Soil

Bioavailability/bioaccessibility

Two steps are involved in the biodegradation of PAHs in soil. The first is the physical uptake of the PAH by the microbial cell and the second is the biological metabolism of the PAH [84]. The second step is a function of the intrinsic biological ability of the microorganism to degrade the PAH but the first is a function of the physical availability of the compound to the cell. Assuming the presence of an adequate metabolic pathway, the degradation of a PAH can only proceed rapidly if the PAH is available to the microorganism in a form (usually in the aqueous phase) that the organism can utilise it [93,115]. Where this is non-existent, the biodegradation of the PAH will be limited by the bioavailability of the PAH to the microorganism. Despite its importance to biodegradation (and by extension to contaminated land assessment), the concept of bioavailability has struggled to progress from a mere research topic to a practical tool for the assessment and management of risks associated with contaminated land. This difficulty is due mainly to confusing and disagreeing definitions (arising from the varied use of the term in different fields) and the absence of a fast and cost effective tool for measuring bioavailability [44,56,107,113]. Semple et al. [113] proposed the use of two definitions, rather than a single term: “bioavailable” and “bioaccessible”. The authors defined the bioavailable compound as “that which is freely available to cross an organism’s cellular membrane from the medium the organism inhabits at a given time” [113]. By contrast, the bioaccessible compound is “that which is available to cross an organism’s cellular membrane from the environment, if the organism has access to the chemical” [113]. The difference between the bioavailable and bioaccessible fractions according to their definition is that whereas the bioavailable compound is available to cross the organisms’ cellular membrane (for degradation, transformation or exertion of a toxic effect) now, the bioaccessible compound can only do so when a restraint in time and/or space has been removed. In other words, the bioaccessible compound comprises that which is actually bioavailable now and that which is potentially bioavailable. Figure 3 conceptualises the bioavailable and bioaccessible fractions of a contaminant in soil [113]. Both of these definitions are important because bioavailability is a descriptor for potential

rates of biodegradation; whereas, bioaccessibility describes realistic biodegradation endpoints [107,114]. The significance of defining bioavailability by the terms suggested by the authors lies in the fact that it raises questions about what is actually being measured by current methods that claim to measure the bioavailable fraction.

The concept of ageing (Figure 2) is important to the bioavailability of PAHs in soil [9]. Decreased bioavailability of PAHs to degrading microbes due to sequestration/ageing in soil has been reported and two processes have been proposed to be responsible for this. The first is the diffusion of PAHs through dissolution sites present in the rubbery and glassy phases of soil organic matter. Contaminants that diffuse through the glassy phase interact more with soil organic matter because of the presence of more rigid cavities [150]. The second process occurs when surfaces within the nano- and micro-pores in soils adsorb contaminants diffusing through them [102]. Since soils contain many pores with diameters less than 20 nm [9], any PAHs that diffuse into such pores become unreachable by degrading bacteria, resulting in their reduced bioavailability.

Biodegradation

Biodegradation of PAHs by microorganisms and the pathways involved have been extensively reviewed elsewhere [13,30,55,70,101,117,155]. Several bacteria capable of degrading PAHs in soils have also been isolated and identified [49,60-62,128]. Biodegradation of PAHs in soil does not depend on the PAH properties alone [40] but also on environmental conditions [86], soil properties [85], bioavailability of the PAH [97] and the degradation potential of the indigenous microorganisms [82].

PATHS(natural and abthropogenic sources)

De

Deposition or spoilage

Soil-PAH interactions

Soil organic matter

Sequestration

Sorptionand di�usion

Persistence

Volatilisation,photo-oxidation,chemical oxidation, leaching

Microbial biotransformation,accumulation and assimilation

Removal from Soil

Figure 1: Fate of PAHs in soil.

[Con

tam

inat

ion]

Contaminant type C

Contaminant type B

Contaminant type A

TimeFigure 2: Theoretical loss curves for three classes of contaminants [122].

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 4 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

that optimum ratios for PAH biodegradation is approximately 100:10:1 [123].

PAH biodegradation in soil is inducible [79] but the processes through which indigenous soil microbes develop the capacity or “learn” to degrade PAHs are not fully understood [63]. However, the pre-exposure of soils to PAH concentrations higher than background PAH levels [65,121] and a change in the genetic composition of the indigenous soil microbial community are thought to be important factors affecting the process [130]. A change in the genetic composition of the indigenous soil microbial community is necessary where the indigenous microbes have not been exposed to either naturally occurring or anthropogenic compounds similar to the PAH of interest. In a study to investigate the relationship between pre exposure and metabolism of PAHs in soil, all 14C PAHs, studied except 14C benzo[a]pyrene, were readily mineralized in most of the pre exposed soils, whereas in the uncontaminated soil, less than 5% of each 14C PAH was mineralized [28]. In a similar study to assess the development of pyrene catabolic activity in two similar soils (pasture and woodland), significant decreases in the lag times and significant increases in the maximum rates and extents of 14C-pyrene mineralised were observed with increasing soil-pyrene contact time [83]. The workers also found that the microbial community in the pasture soil (with lower soil organic

Temperature, soil moisture content, alkalinity, soil nutrient content and pre exposure to PAHs are some of the environmental and soil properties affecting PAH biodegradation in soil. Generally, bacterial metabolic activity and PAH biodegradation increases with increasing temperature up to an optimum temperature reported to be around 30˚C to 40˚C [78,156]. Hydrocarbon utilizing bacteria can also adapt to temperature extremes to maintain metabolic activity. Hydrocarbon degradation has therefore been reported at temperatures close to freezing and above 30˚C [5,10]. The optimum moisture level for the biodegradation of oil sludge reported in literature is between 30% - 90% of the soil’s water holding capacity [129]. At higher water contents, there is a risk of the onset of anaerobic conditions arising from the slow rate of oxygen diffusion through water. At lower water contents, water availability becomes a limiting factor to microbial activity or PAH bioavailability. PAH degradation has also been shown to be favoured in slightly alkaline soils, as PAH-degrading bacteria become less competitive with increasing acidic conditions [84]. Bacteria require nutrient elements, such as nitrogen and phosphorus for incorporation into biomass and the synthesis of cellular components. The presence of these nutrient elements in soil is therefore critical for the biodegradation of PAHs [14]. The optimisation of the C:N:P ratio is thought to be one of the most important amendments enhancing the rates and extents of PAH biodegradation in soil. It is generally accepted

Sorbed compound(rapidly reversible)[bioavailable or bioaccessible:temporally constrained]

Sorbed compound(slowly/very slowly reversible)[bioaccessible:temporally constrained]

Occluded compound[non-bioaccessible] Earthworm

compound[physically constained]

Plant root

Bioaccessible

Bioavailablecompound

Figure 3: A conceptual diagram illustrating the bioavailable and bioaccessible fractions of a contaminant in soil as defined by physical location [113].

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 5 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

matter) adapted to use pyrene before the community in the woodland soil. This observation was attributed to decreased bioavailability of pyrene in the woodland soil due to a higher soil organic matter content.

Having noted the importance of pre-exposure to the development of PAH degrading capacity and the dependence of PAH bioavailability and biodegradation on soil and environmental factors, this review aims to consider existing knowledge on PAH levels, bioavailability and indigenous biodegradation in background soils from extreme temperature environments, temperate environments and tropical environments.

Biodegradation of PAHs in Soils from Different Cli-matic Zones

Antarctic soils

Although Antarctic soils are diverse, they have all been generally described as cold, sandy, desert soils, with minimal effective annual precipitation, high pH, low organic matter and nutrient contents and rare occurrences of vegetation, mostly lichens and mosses [5,27]. Mean monthly temperatures in the continental Antarctic region where the most extreme conditions are found are below -15˚C all year round, falling to below -30˚C in winter [135]. Less than 0.35% of the entire terrestrial Antarctic continent is ice free, the remainder is permanently under the cover of ice [45]. Despite this tiny proportion of the continent being ice-free and exposed to weathering processes, there is significant microbial diversity in Antarctic soils. Different PAH degrading microorganisms have been found [29]: up to 13 MPN g-1 [5], 230 MPN g-1 [4] and 7×104 CFU g−1 [112] of hydrocarbon degrading bacteria have been reported to be present in uncontaminated Antarctic soils. Most of these PAH degraders were identified as bacteria rather than fungi [71], e.g. Flavobacterium spp., Corynebacterium spp., Bacillus spp. an isolate from the family of Enterobacteriaceae [71], Pseudomonas spp. or Sphingomonas spp. related to PAH degradative strains from lower latitudes [3,17] and Acinetobacter [80] are some of those isolated from Antarctic soils. These degraders were psychrotolerant, able to tolerate temperatures >20˚C and capable of growing at or near 0°C. They were also able to degrade monoaromatic hydrocarbons, naphthalene as well as its methyl derivatives [3,71].

The presence of PAH-degrading bacteria in background soils is a good indicator that the soils have been exposed to PAHs [26], even at low concentrations. Long range atmospheric transport of low molecular weight PAHS and increased human presence and activity in the Antarctic represent the main sources of PAHs in these soils. Human activities require hydrocarbons for heating, power generation and to power land and air transport vehicles. Elevated levels of PAHs in Antarctic soils have therefore been found mostly in soils with close proximity to current or former scientific bases, fuel stores or automobile or aircraft fuelling stations [8,125]. Accidental discharge of petroleum products during storage and distribution from drums and pipelines is also a significant source [53]. PAHs in uncontaminated Antarctic soils have either been undetectable or detected at background levels [4,5]. For instance, a study was carried out to compare PAH concentrations at fuel spill sites to uncontaminated control sites in three Antarctic locations: Scott Base, Marble Point and Wright Valley. The study found PAH concentrations in the contaminated sites to range from 41 – 8,105 ng g-1 of dry soil. PAHs were, however, undetectable at the control soils [2]. PAH concentrations of up to 27,000 mg kg-1 have also been detected in contaminated soils at McMurdo Station, Antarctica; the highest concentrations were found in soils from unpaved roadbeds and gasoline pumps [89]. Where PAHs have been found in uncontaminated

Antarctic soils, low molecular weight PAHs (phenanthrene and fluoranthene) are usually prevalent and are present at levels consistent with pre-industrial times [137]. This is an indication that while local sources are responsible for high levels of PAHs in contaminated soils, long range atmospheric transport from populated areas of Africa, South America, and Australia is the most likely source of PAHs to background Antarctic soils [72].

The fate of PAHs in Antarctic soils includes volatilisation, dispersal, transformation or degradation as a result of physical, chemical and biological processes. Lighter PAHs volatise readily from Antarctic soils and can migrate through soil layers [53]. Less volatile fractions tend not to migrate far from their point of deposition [42]. Lighter molecular weight PAHs are expected to be available for microbial degradation in Antarctic soils [7] because these soils are typically dry and have low organic matter contents. Since the sequestration of organic compounds in dry soils with < 4% moisture is controlled by adsorption onto mineral surfaces and not organic matter [18,134], PAH biodegradation in Antarctic soils should not be limited by sequestration to soil organic matter. PAH bioavailability may however, be limited by poor water activity [78]. Because of the low moisture contents of Antarctic soils, PAHs and microbes may not be able to move around sufficiently enough to come in contact for biodegradation. Microbial degradation of PAHs in Antarctic soils has been measured in microcosms [5] and mesocosms [36]. Low moisture content, alkaline soil pH [5], and low temperature [6,41] have been identified as the limiting factors for PAH biodegradation in Antarctic soils; however, nutrient availability and temperature fluctuations are considered to be the most important [36,132].

When high concentrations of PAHs are introduced into Antarctic soils, they have the potential to further deplete the already low amounts of N and P present in the soils when they are used up by microorganisms during biodegradation [4]. Enhanced biodegradation of PAHs has been achieved in Antarctic soils by the addition of fertilizers containing N and P. For instance 14C-naphthalene was mineralised to a greater extent when N was added as nitrate or ammonium [5]. The addition of nutrients to the coarse-textured, low-moisture soils prevalent in continental Antarctica has the potential to inhibit PAH biodegradation by decreasing soil water potentials, care must therefore be taken to add the right amount of nutrients and there is no consensus on what that right amount is because of the varying soil and environmental conditions prevalent in Antarctica [6].

Temperature limits the biodegradation of PAHs in Antarctic soils by affecting the physical nature of the PAHs and the metabolic activity of the degrading microbes [36]. At low temperatures, PAHs are more viscous, less volatile and less soluble resulting in reduced bioavailability and subsequent biodegradation [78]. Metabolic activity of PAH-degrading microbes at low temperatures are reduced because they follow the Arrhenius relationship, increasing with increasing temperature [78], usually doubling for each 10oC increase in temperature from 10˚C to 40oC [24,36]. As a result, though PAH biodegradation has been reported at low temperatures [46], increasing the temperature has often resulted in increased rates and extents of PAHs degradation [73,136].

Temperate soils

Temperate environments are characterised by their general mildness and four distinct seasons with summer and winter roughly of equal length. 35% - 40% of the global human population live in the hospitable temperate environment comprising roughly 7% of the

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 6 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

Earth’s surface area [38]. Temperate and tropical soils share many soil types, making the distinction between them artificial; however, characteristics like soil temperature and soil moisture are often different between the two across all soil types [118]. Temperate soils are different from tropical soils firstly because during a significant portion of the year (winter), they are exposed to sub-optimal or freezing temperatures resulting in reduced biological activity and changes in the physical and chemical properties of the soils. Secondly, agricultural soils in temperate environments are generally younger than soils from the tropics [110]. It is also generally believed that the residence times of organic matter/carbon is longer in temperate soils than in tropical soils due mainly to reduced rates of decomposition arising from lower temperatures and moisture levels in temperate regions [127].

In soils throughout the temperate zone, PAH profiles are similar [137], showing correlations between individual PAH concentrations [143] and a quantitative dominance of higher molecular weight PAHs (e.g. chrysene, pyrene, fluoranthene) produced mainly due to anthropogenic activities [43,94,138]. This similarity in PAH profiles has been explained by the “weathering” of emissions from different sources in the atmosphere, resulting from the transformation of PAHs from different sources during atmospheric transport [66].

Levels of PAHs in background soils from Western Europe have been found to cover a wide range of concentrations from 8.6 to 11,200 μg kg-1 [94]. Land use plays an important role in PAH concentrations in temperate soils. For instance, PAHs in agricultural soils amended with sewage sludge have been reviewed [19], showing the effects the introduction of sewage sludge can have on PAH concentrations. Sewage sludge may enhance the removal of PAHs from soils, either by the introduction of microorganisms adapted to PAH degradation or by increasing the leachability of PAHs through the movement of dissolved organic matter. Conversely, the application of sewage sludge can introduce more organic matter into the soil, resulting in greater sorption of PAHs and subsequent retention in the soils [145]. Long term studies of archived UK agricultural soils amended with sewage sludge revealed PAH levels were three times higher than unamended control soils, particularly with higher molecular weight PAHs [145,148]. The implication may be that the addition of sewage sludge to temperate agricultural soil does more to enhance the retention of PAHs than their losses.

PAH concentrations in temperate soils also differ according to soil type. In most cases, concentrations of persistent organic pollutants are lower in grassland soils than in woodland/forest soils because of the greater ability of the forest canopy to scavenge for persistent organic pollutants [90]. Selected Norwegian grassland soils have been found to have generally lower PAH levels than neighbouring forest systems [94].

Urban temperate soils are often associated with increased human activity resulting in high PAH levels relative to soils from less populated rural areas [69,74]. Distance from point sources, climatic conditions and soil organic matter are other factors that influence levels of PAHs in urban soils. Positive correlations have been drawn between PAH concentrations in temperate soils and soil organic matter [67,94,147].

PAH degraders have been found in pristine soil samples from Norway (up to 2.4 x106 CFU g-1 soil) and Denmark (up to 6.6 x 106 CFU g-1 soil), agricultural soils (up to 9.9 x106 CFU g-1 soil), diffusely polluted (up to 1.1 x 108 CFU g-1 soil) and industrially polluted (up to 1.7 x 107 CFU g-1 soil) soils from Denmark. This shows the ubiquitous presence of PAH degraders following the ubiquitous presence of PAHs in temperate soils. In fact, a correlation has been found between the

total PAHs in a temperate soil and the potential for PAH mineralisation in the soil suggesting the dependence of PAH degradation potential on the level of PAH contamination [65]. While studying the total and bioaccessible amounts of PAHs present at a motorway site north of Copenhagen and the prevalence of microbial PAH degraders as well as the potential for PAH degradation, the highest levels of PAH contamination were found in samples closest to the motorway. The highest numbers of bacterial PAH degraders and the greatest potential for PAH biodegradation were also found in the same soils. The fact that the highest levels of PAH contamination was found in the soil with the highest numbers of bacterial PAH degraders appear contradictory and raises questions about PAH persistence. The authors suggested that low bioavailability of PAHs and not a limitation in the bacterial population was responsible for the accumulation of PAHs in the soil with a high number of bacterial PAH degraders. A measurement of the bioaccessible PAH fractions showed that only 1-5 % of the PAHs were actually accessible to the soil microorganisms for degradation. Adsorption of PAHs to soot particles released from diesel engines was given as a possible reason for the reduced bioavailability and consequent reduced biodegradation of the PAHs [64]. Higher soil organic matter content in temperate soils has also been found to result in slower adaptation of indigenous soil microorganisms to PAH degradation [83]. In a study, two similar temperate soils (pasture and woodland) were amended with 100 mg pyrene kg-1 and significant mineralisation of 14C pyrene was observed after 8 and 76 weeks soil pyrene contact time respectively. The addition of microbial inocula led to the mineralisation of the previously added 14C pyrene implying that it was bioavailable but the indigenous microflora had not adapted to its degradation. As the only difference between the two soils was a higher organic matter content in the woodland soil, the authors suggest that the rate of pyrene organic matter content in the woodland soil, the authors suggest that the rate of pyrene transfer from the soil to the microorganisms was slower in the woodland soil due to its higher organic matter content leading to slower adaptation of the microorganisms and subsequent biodegradation. Despite PAH-degrading microorganisms being ubiquitously distributed through temperate soils, the major limiting factor for PAH degradation appears to be bioavailability as controlled by soil type and soil organic matter content.

Tropical soils

Geographically, the tropics can be defined as that part of the world located between 23.5 degrees north and south of the equator, representing the land mass between the Tropic of Cancer and the Tropic of Capricorn. Tropical environments are largely warmer than temperate environments with much less temperature variations between seasons. Approximately 87% of the global tropical areas are usually above 25˚C. Differences in amounts of precipitation and solar radiation further distinguish between tropical and temperate climates [12,32].

The generalisations that can be drawn from the characteristics of tropical soils have been reviewed as follows: (i) the types and properties of clay minerals are much more varied in the tropics than in glaciated temperate areas; (ii) many tropical soils exhibit significant anion exchange capacity; (iii) organic matter contents in the tropics are similar to those of the temperate region; (v) although the annual addition of organic carbon to the soil is five times greater in tropical udic environments than temperate udic environments, the rate of organic decomposition is also five times greater in the tropics; (v) in ustic environments, lack of soil moisture during the dry season decreases organic carbon decomposition just as low temperatures do

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 7 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

in temperate regions; (vi) the vast majority of the soils of the humid tropics are acidic, and (vii) the vast majority of the cultivated soils of the humid tropics are not acidic [34].

Soil-PAH fingerprints are often defined by soil type and PAH sources into the soil. PAHs enter tropical environments mostly through on-going biomass burning and vehicular traffic [137]. By contrast, fossil fuel combustion (known to release higher molecular weight four and five ring PAHs) dominate PAH sources of PAHs into temperate soils [139]. Also, a longer history of industrialisation in the temperate region implies historical PAH sources. This suggest that over time, the more volatile, biodegradable lower molecular weight PAHs would have been removed from temperate soils [68]. Biologically derived PAH sources known to produce low molecular weight PAHs have also been identified as sources of low molecular weight PAHs into tropical soils [139-141].

Microbial diversity in soils is determined by vegetation type, carbon and nutrient availability, soil moisture and soil pH. Soils with similar environmental characteristics will therefore have similar bacterial communities irrespective of geographical location [48]. Studies where indigenous PAH degraders are enumerated in tropical soils are rare but tropical soils with similar properties as temperate soils can be expected to contain similar microbial communities. The presence of microorganisms with the necessary genes for PAH degradation in contaminated tropical soils have been reported [54]. For example, thirty three distinct species of bacteria, fungi and yeast capable of degrading PAHs were collected from petroleum polluted soils and cyanobacteria mats from Indonesia [31]. Also, three Pseudomonas species LP1, LP2 and LP3 were isolated from an oil polluted soil in Lagos, Nigeria. They were able to degrade a broad range of PAHs including up to 67.79%, 66.61% and 47.09% of pyrene respectively [95].

Moisture and temperature are the main factors that influence microbial activities in which tropical and temperate soils differ. Tropical soils have higher temperatures all year round [77]. Rates of PAHs degradation in tropical soils are therefore generally expected to be higher than in temperate soils. The higher rates of organic matter turn over observed in tropical soils support this argument [34]. Moisture should therefore be the controlling/limiting factor of microbial activity in tropical soil [98]. PAH biodegradation can be controlled by moisture

either directly because microbial activity can be inhibited by poor soil moisture or indirectly by affecting PAH transport and bioavailability [116].

Hot deserts

Desert soils can be found globally except in Europe. They are characterised by poor organic matter and water levels, are usually subjected to rather high temperatures (up to 50˚C) and extensive light [104]. There is a paucity of data relating to the sources and levels of PAHs in background hot desert soils because most studies on background soils have been conducted using temperate soils [87]. However, both short and long range atmospheric transport of PAHs and proximity of hot deserts to PAH point sources play significant roles in the background concentration of PAHs in desert soils [52].

Temperature is significant to the fate of PAHs in desert soils. Because of the hydrophobic nature of PAHs and their consequently reduced solubility, PAH volatilisation, solubility and bioavailability are controlled by temperature. At high temperatures, PAHs are less viscous, more easily distributed and can diffuse faster. Bioavailability of some PAHs can therefore be enhanced at elevated temperatures [47]. On the other hand, bioavailability and biodegradation of PAHs can be inhibited by the poor moisture content of the soils. Increased bioavailability and subsequent biodegradation has been achieved by repeated irrigation of polluted desert soils [105,106]. Biodegradation of PAHs in extremely hot desert soils requires the activity of thermophilic bacteria but not much is known about PAH degradation by thermophiles in soil [86,96]. A few microbes capable of degrading PAHs at very hot temperatures have been isolated. For example, Bacillus thermoleovorans, which grows at 60˚C, has been isolated from a compost consisting of wooden ties treated with lignite tar and was able to utilise naphthalene as a sole carbon source [11]. Nocardia otitidiscaviarum which grows optimally at 50˚C has also been shown to possess PAH degrading capabilities [154]. Other microorganisms able to degrade naphthalene, phenanthrene and anthracene under thermophilic conditions have also been isolated [47,92]. Some of these microbes were found to produce metabolites that were different from those produced during the biodegradation of PAHs by mesophilic bacteria [92]. A new pathway was also identified when Bacillus thermoleovorans degraded naphthalene at 60˚C [11]. For some time, it was assumed that at elevated temperatures, reduced oxygen solubility limited effective aerobic degradation of PAHs but more recent discoveries have shown that at elevated temperatures, the oxygen transfer coefficient rises thereby compensating for the reduction in oxygen solubility [86].

Conclusion

PAHs are an important class of environmental contaminants produced by both natural and anthropogenic processes. The importance of soil as a reservoir of organic pollutants means that PAHs can now be found in virtually all global soils irrespective of nature or location. When PAHs enter a soil, they interact with the soil in different ways leading to either retention or loss depending on the physical, chemical and biological characteristics of the soil. Since global soils differ in their characteristics, the fate of PAHs in soils also differ and it may not always be correct to extrapolate the fate of a PAH in one soil type to another. This makes understanding the interactions between PAHs and soils from different environments important. The weight of available information on these interactions leans heavily in favour of temperate soils. More research is therefore needed into PAH-soil interactions in tropical and desert soils.

In comparison to temperate soils, published data on the PAH levels of tropical soils is considerably less [35]. Available data show that generally, PAH levels in most tropical soils are lower than in temperate soils. For instance, PAH levels in soils from Lahore, Pakistan were considerably lower than those in soils collected from Birmingham, UK (which were representative of UK PAH levels) even though atmospheric levels were higher [119]. PAH levels of 5 ng g-1 dry weight have been reported for Costa Rican soil [39]. ∑20PAHs in 30 hydromorphic soils of the tropical metropolis of Bangkok was found to range between 12 and 380 μg kg−1 [142]. Higher PAH levels have been found in temperate UK (42 and 11,200 μg kg−1) and Norway (8.6 and 1,050 μg kg−1) background soils [69,94]. Shorter PAH accumulation time in tropical soils and enhanced PAH losses through biodegradation, volatilisation, photo-oxidation, and leaching into groundwater have been proposed as the reason why PAHs levels are lower in tropical soils [142]. Although the ∑PAHs in tropical soils is often less than in temperate soils, low molecular weight PAHs (naphthalene and phenanthrene) are most prevalent and are present at levels comparable to those in temperate soils [39].

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 8 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

References

1. Agarwal T, Khillare PS, Shridhar V, Ray S (2009) Pattern, sources and toxic potential of PAHs in the agricultural soils of Delhi, India. J Hazard Mater 163: 1033-1039.

2. Aislabie J, Balks M, Astori N, Stevenson G, Symons R (1999) Polycyclic aromatic hydrocarbons in fuel-oil contaminated soils, Antarctica. Chemosphere 39: 2201-2207.

3. Aislabie J, Foght J, Saul D (2000) Aromatic hydrocarbon-degrading bacteria from soil near scott base, Antarctica. Polar Biology 23: 183-188.

4. Aislabie J, Fraser R, Duncan S, Farrell RL (2001) Effects of oil spills on microbial heterotrophs in Antarctic soils. Polar Biology 24: 308-313.

5. Aislabie J, McLeod M, Fraser R (1998) Potential for biodegradation of hydrocarbons in soil from the ross dependency, Antarctica. Applied Microbiology and Biotechnology 49: 210-214.

6. Aislabie J, Saul DJ, Foght JM (2006) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10: 171-179.

7. Aislabie JM, Balks MR, Foght JM, Waterhouse EJ (2004) Hydrocarbon spills on Antarctic soils: effects and management. Environ Sci Technol 38: 1265-1274.

8. Aislabie JM, Ryburn J, Gutierrez-Zamora ML, Rhodes P, Hunter D, et al. (2012) Hexadecane mineralization activity in hydrocarbon-contaminated soils of Ross Sea region, Antarctica may require nutrients and inoculation. Soil Biology & Biochemistry 45: 49-60.

9. Alexander M (1995) How toxic are toxic chemicals in soil?, Environmental Science & Technology 29: 2713-2717.

10. Alvarez PJJ, Illman WA (2006) Bioremediation and natural attenuation. Wiley Interscience New Jersey.

11. Annweiler E, Richnow HH, Antranikian G, Hebenbrock S, Garms C, et al. (2000) Naphthalene degradation and incorporation of naphthalene-derived carbon into biomass by the thermophile Bacillus thermoleovorans. Appl Environ Microbiol 66: 518-523.

12. Arbeli Z, Fuentes CL (2010) Microbial degradation of pesticides in tropical soils, in Soil biology and agriculture in the tropics. P. Dion (eds) Springer Berlin Heidelberg 251-274.

13. Atlas RM (1981) Microbial degradation of petroleum hydrocarbons: an environmental perspective. Microbiol Rev 45: 180-209.

14. Atlas RM, Bartha R (1992) Hydrocarbon biodegradation and oil-spill bioremediation. Advances in Microbial Ecology 12: 287-338.

15. Azuma H, Toyota M, Asakawa Y, Kawano S (1996) Naphthalene--a constituent of magnolia flowers. Phytochemistry 42: 999-1004.

16. Baek SO, Field RA, Goldstone ME, Kirk PW, Lester JN, et al. (1991) A review of atmospheric polycyclic aromatic hydrocarbons: sources, fate and behavior. Water, Air, & Soil Pollution 60: 279-300.

17. Baraniecki CA, Aislabie J, Foght JM (2002) Characterization of Sphingomonas sp. Ant 17, an aromatic hydrocarbon-degrading bacterium isolated from Antarctic soil. Microb Ecol 43: 44-54.

18. Batterman S, Kulshrestha A, Cheng HY (1995) Hydrocarbon vapor transport in low moisture soils. Environmental Science & Technology 29: 171-180.

19. Beck AJ, Johnson DL, Jones KC (1996) The form and bioavailability of non-ionic organic chemicals in sewage sludge-amended agricultural soils. Sci Total Environ 185: 125-149.

20. Bispo A, Jourdain MJ, Jauzein M (1999) Toxicity and genotoxicity of industrial soils polluted by polycyclic aromatic hydrocarbons (PAHs). Organic Geochemistry 30: 947-952.

21. Blumer M (1976) Polycyclic aromatic compounds in nature. Scientific American (United States) 234:3: 35-45.

22. Blumer M (1976) Polycyclic aromatic compounds in nature. Sci Am 234: 35-45.

23. Boldrin B, Tiehm A, Fritzsche C (1993) Degradation of phenanthrene, fluorene, fluoranthene, and pyrene by a Mycobacterium sp. Appl Environ Microbiol 59: 1927-1930.

24. Bossert I, Bartha R (1984) The fate of petroleum in soil ecosystems, in Petroleum Microbiology, R.M. Atlas (eds) MacMillan Publishing Co: New York. 434–476.

25. Bossert ID, Bartha R (1986) Structure-biodegradability relationships of polycyclic aromatic hydrocarbons in soil. Bull Environ Contam Toxicol 37: 490-495.

26. Braddock JF, Lindstrom JE, Brown EJ (1995) Distribution of hydrocarbon-degrading microorganisms in sediments from Prince William Sound, Alaska, following the Exxon Valdez oil spill. Marine Pollution Bulletin 30: 125-132.

27. Campbell IB, Claridge GGC (2009) Antarctic permafrost soils, in Permafrost soils, R. Margesin (eds) 17-31.

28. Carmichael LM, Pfaender FK (1997) Polynuclear aromatic hydrocarbon metabolism in soils: relationship to soil characteristics and preexposure. Environmental Toxicology & Chemistry 16; 666-675.

29. Cavanagh JE, Nichols PD, Franzmann PD, McMeekin TA (1998) Hydrocarbon degradation by Antarctic coastal bacteria. Antarctic Science 10: 386-397.

30. Bryant DW, McCalla DR, Lultschik P, Quilliam MA, McCarry BE (1984) Metabolism of 1,8-dinitropyrene by Salmonella typhimurium. Chem Biol Interact 49: 351-368.

31. Chaillan F, Le Flèche A, Bury E, Phantavong YH, Grimont P, et al. (2004) Identification and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res Microbiol 155: 587-595.

32. Cheesman EE (1978) An introduction to the botany of tropical crops, London: Longmans 371,

33. Chuang JC, Callahan PJ, Menton RG, Gordon SM, Lewis RG, et al. (1995) Monitoring methods for polycyclic aromatic hydrocarbons and their distribution in house dust and track-in soil. Environmental Science & Technology 29: 494-500.

34. Cobley LS, Steele WM (1984) An introduction to the botany of tropical crops. Longman, New York.

35. Connell DW, Miller GJ, Mortimer MR, Shaw GR, Anderson SM (1999) Persistent lipophilic contaminants and other chemical residues in the Southern Hemisphere. Critical Reviews in Environmental Science and Technology 29: 47-82.

36. Coulon F, Pelletier E, Gourhant L, Delille D (2005) Effects of nutrient and temperature on degradation of petroleum hydrocarbons in contaminated sub-Antarctic soil. Chemosphere 58: 1439-1448.

37. Cousins IT, Jones KC (1998) Air-soil exchange of semi-volatile organic compounds (socs) in the uk. Environmental Pollution 102: 105-118.

38. Crutzen PJ (2002) Geology of mankind. Nature 415: 23.

39. Daly GL, Lei YD, Castillo LE, Muir DCG, Wania F (2007) Polycyclic aromatic hydrocarbons in costa rican air and soil: a tropical/temperate comparison. Atmospheric Environment 41: 7339-7350.

40. Davis JW, Madsen S (1996) Factors affecting the biodegradation of toluene in soil. Chemosphere 33: 107-130.

41. Delille D, Coulon F, Pelletier E (2004) Effects of temperature warming during a bioremediation study of natural and nutrient-amended hydrocarbon-contaminated sub-Antarctic soils. Cold Regions Science & Technology 40: 61-70.

42. Deprez PD, Arens M, Locher H (1999) Identification and assessment of contaminated sites at Casey Station, Wilkes Land, Antarctica. Polar Record 35: 299-316.at Casey Station, Wilkes Land, Antarctica. Polar Record 35: 299-316.

43. Edwards NT (1983) Polycyclic aromatic hydrocarbons (PAHs) in the terrestrial environment—a review1. Journal of Environmental Quality 12: 427-441.

44. Ehlers LJ, Luthy RG (2003) Contaminant bioavailability in soil and sediment. Environ Sci Technol 37: 295A-302A.

45. Engelen A, Convey P, Hodgson D, Roger Worland M, Ott S (2008) Soil properties of an antarctic inland site: Implications for ecosystem development. Polar Biology 31: 1453-1460.

46. Eriksson M, Sodersten E, Yu Z, Dalhammar G, Mohn WW (2003) Degradation of polycyclic aromatic hydrocarbons at low temperature under aerobic and nitrate-reducing conditions in enrichment cultures from northern soils. Appl Environ Microbiol 69: 275-284.

47. Feitkenhauer H, Müller R, Märkl H (2003) Degradation of polycyclic aromatic hydrocarbons and long chain alkanes at 60-70 degrees C by Thermus and Bacillus spp [corrected]. Biodegradation 14: 367-372.

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 9 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

48. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103: 626-631.

49. Foght JM, Westlake DW (1988) Degradation of polycyclic aromatic hydrocarbons and aromatic heterocycles by a Pseudomonas species. Can J Microbiol 34: 1135-1141.

50. Freckman DW, Virginia RA (1989) Plant-feeding nematodes in deep-rooting desert ecosystems. Ecology 70: 1665-1678.

51. Freeman DJ, Cattell FCR (1990) Woodburning as a source of atmospheric polycyclic aromatic hydrocarbons. Environmental Science & Technology 24: 1581-1585.

52. Garrison VH, Shinn EA, Foreman WT, Griffin DW, Holmes CW, et al. (2003) African and Asian dust: From desert soils to coral reefs. BioScience 53: 469-480.

53. Gore DB, Revill AT, Guille D (1999) Petroleum hydrocarbons ten years after spillage at a helipad in Bunger Hills, east Antarctica. Antarctic Science 11: 427-429.

54. Hamann C, Hegemann J, Hildebrandt A (1999) Detection of polycyclic aromatic hydrocarbon degradation genes in different soil bacteria by polymerase chain reaction and DNA hybridization. FEMS Microbiol Lett 173: 255-263.

55. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169: 1-15.

56. Harmsen J (2007) Measuring bioavailability: from a scientific approach to standard methods. J Environ Qual 36: 1420-1428.

57. Harvey R (1991) Polycyclic Aromatic Hydrocarbons: Chemistry and Carcinogenicity. Cambridge monographs on cancer research, Cambridge University Press: Cambridge, UK.

58. Harvey RG (1997) Polycyclic aromatic hydrocarbons. Wiley-VCH New Yok, N.Y.

59. Hatzinger PB, Alexander M (1995) Effect of aging of chemicals in soil on their biodegradability and extractability. Environmental Science & Technology 29: 537-545.

60. Heitkamp MA, Cerniglia CE (1988) Mineralization of polycyclic aromatic hydrocarbons by a bacterium isolated from sediment below an oil field. Appl Environ Microbiol 54: 1612-1614.

61. Heitkamp MA, Franklin W, Cerniglia CE (1988) Microbial metabolism of polycyclic aromatic hydrocarbons: isolation and characterization of a pyrene-degrading bacterium. Appl Environ Microbiol 54: 2549-2555.

62. Ho Y, M Jackson Y Yang, Mueller JG, Pritchard PH (2000) Characterization of fluoranthene- and pyrene-degrading bacteria isolated from PAH-contaminated soils and sediments. Journal of Industrial Microbiology & Biotechnology 24: 100-112.

63. Holden PA, Firestone MK (1997) Soil microorganisms in soil cleanup: How can we improve our understanding? J Env Quality 26: 32-40.

64. Johnsen AR, De Lipthay JR, Reichenberg F, Sørensen SJ, Andersen O, et al. (2006) Biodegradation, bioaccessibility, and genotoxicity of diffuse polycyclic aromatic hydrocarbon (PAH) pollution at a motorway site. Environ Sci Technol 40: 3293-3298.

65. Johnsen AR, Karlson U (2005) PAH degradation capacity of soil microbial communities--does it depend on PAH exposure? Microb Ecol 50: 488-495.

66. Jones KC, Grimmer G, Jacob J, Johnston AE (1989) Changes in the polynuclear aromatic hydrocarbon content of wheat grain and pasture grassland over the last century from one site in the U.K. Sci Total Environ 78: 117-130.

67. Jones KC, Stratford JA, Tidridge P, Waterhouse KS, Johnston AE (1989) Polynuclear aromatic hydrocarbons in an agricultural soil: long-term changes in profile distribution. Environ Pollut 56: 337-351.

68. Jones KC, Stratford JA, Waterhouse KS, Furlong ET, Giger W, et al. (1989) Increases in the polynuclear aromatic hydrocarbon content of an agricultural soil over the last century. Environmental Science & Technology 23: 95-101.

69. Jones KC, Stratford JA, Waterhouse KS, Vogt NB (1989) Organic contaminants in Welsh soils: Polynuclear aromatic hydrocarbons. Environmental Science & Technology 23: 540-550.

70. Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182: 2059-2067.

71. Kerry E (1990) Microorganisms colonizing plants and soil subjected to different degrees of human activity, including petroleum contamination, in the Vestfold Hills and Macrobertson Land, Antarctica. Polar Biology 10: 423-430.

72. Klánová J, Matykiewiczová N, Mácka Z, Prosek P, Láska K, et al. (2008) Persistent organic pollutants in soils and sediments from James Ross Island, Antarctica. Environ Pollut 152: 416-423.

73. Knapp JS, Whytell AJ (1990) The biodegradation of morpholine in river water and activated sludge. Environ Pollut 68: 67-79.

74. Krauss M, Wilcke W (2003) Polychlorinated naphthalenes in urban soils: analysis, concentrations, and relation to other persistent organic pollutants. Environ Pollut 122: 75-89.

75. Krauss M, Wilcke W, Martius C, Bandeira AG, Garcia MV, et al. (2005) Atmospheric versus biological sources of polycyclic aromatic hydrocarbons (PAHs) in a tropical rain forest environment. Environ Pollut 135: 143-154.

76. Laflamme RE, Hites RA (1978) The global distribution of polycyclic aromatic hydrocarbons in recent sediments. Geochimica et Cosmochimica Acta 42: 289-303.

77. Lavelle P, Blanchart E, Martin A, Martin S, Spain A (1993) A hierarchical model for decomposition in terrestrial ecosystems: Application to soils of the humid tropics. Biotropica 25: 130-150.

78. Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54: 305-315.

79. Lee PH, Doick KJ, Semple KT (2003) The development of phenanthrene catabolism in soil amended with transformer oil. FEMS Microbiol Lett 228: 217-223.

80. Mac Cormack WP, Fraile ER (1997) Characterization of a hydrocarbon degrading psychrotrophic Antarctic bacterium. Antarctic Science 9: 150-155.

81. Mackay D, Shui WY, Ma KC (1992) Illustated hand book of physical-chemical properties and environmental fate of organic chemicals. Lewis, Boca Raton, FL.

82. MacLeod CJ, Morriss AW, Semple KT (2001) The role of microorganisms in ecological risk assessment of hydrophobic organic contaminants in soils. Adv Appl Microbiol 48: 171-212.

83. Macleod CJ, Semple KT (2002) The adaptation of two similar soils to pyrene catabolism. Environ Pollut 119: 357-364.

84. Maeir RM, Pepper IL, Gerba PC (2000) A textbook of environmental microbiology. Academic press San Diego, CA.

85. Manilal VB, Alexander M (1991) Factors affecting the microbial degradation of phenanthrene in soil. Applied Microbiology & Biotechnology 35: 401-405.

86. Margesin R, Schinner F (2001) Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl Microbiol Biotechnol 56: 650-663.

87. Marusenko Y, Herckes P, Hall S (2011) Distribution of polycyclic aromatic hydrocarbons in soils of an arid urban ecosystem. Water, Air, & Soil Pollution 219: 473-487.

88. Masih A, Taneja A (2006) Polycyclic aromatic hydrocarbons (PAHs) concentrations and related carcinogenic potencies in soil at a semi-arid region of India. Chemosphere 65: 449-456.

89. Mazzera D, Hayes T, Lowenthal D, Zielinska B (1999) Quantification of polycyclic aromatic hydrocarbons in soil at McMurdo Station, Antarctica. Sci Total Environ 229: 65-71.

90. Meijer SN, Steinnes E, Ockenden WA, Jones KC (2002) Influence of environmental variables on the spatial distribution of PCBs in Norwegian and U.K. soils: implications for global cycling. Environ Sci Technol 36: 2146-2153.

91. Motelay-Massei A, Ollivon D, Garban B, Teil MJ, Blanchard M, et al. (2004) Distribution and spatial trends of PAHs and PCBs in soils in the Seine River basin, France. Chemosphere 55: 555-565.

92. Müller R, Antranikian G, Maloney S, Sharp R (1998) Thermophilic degradation of environmental pollutants, in Biotechnology of Extremophiles, Springer Berlin / Heidelberg, 155-169.

93. Nakahara T, Erickson LE, Gutierrez JR (1977) Characteristics of hydrocarbon uptake in cultures with two liquid phases. Biotechnol Bioeng 19: 9-25.

94. Nam JJ, Thomas GO, Jaward FM, Steinnes E, Gustafsson O, et al. (2008) PAHs in background soils from Western Europe: influence of atmospheric deposition and soil organic matter. Chemosphere 70: 1596-1602.

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 10 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

95. Obayor O, M. Ilori, S Adebusoye, G Oyetibo, O Amund (2008) Pyrene-degradation potentials of Pseudomonas species isolated from polluted tropical soils. World Journal of Microbiology & Biotechnology 24: 2639-2646.

96. Obuekwe CO, Hourani G, Radwan SS (2001) High-temperature hydrocarbon biodegradation activities in Kuwaiti desert soil samples. Folia Microbiol (Praha) 46: 535-539.

97. Ogram AV, Jessup RE, Ou LT, Rao PS (1985) Effects of sorption on biological degradation rates of (2,4-dichlorophenoxy) acetic acid in soils. Appl Environ Microbiol 49: 582-587.

98. Orchard VA, FJ Cook (1983) Relationship between soil respiration and soil moisture. Soil Biology & Biochemistry 15: 447-453.

99. Park KS, RC Sims, RR Dupont, WJ Doucette, JE Matthews (1990) Fate of PAH compounds in two soil types: influence of volatilization, abiotic loss and biological activity. Environmental Toxicology and Chemistry 9: 187-195.

100. Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, et al. (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32: 927-955.

101. Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, et al. (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32: 927-955.

102. Pignatello JJ, B Xing (1995) Mechanisms of slow sorption of organic chemicals to natural particles. Environmental Science & Technology 30: 1-11.

103. Potter CL, JA Glaser, LW Chang, JR Meier, MA Dosani, et al. (1999) Degradation of polynuclear aromatic hydrocarbons under bench-scale compost conditions. Environmental Science & Technology 33: 1717-1725.

104. Radwan S (2008) Microbiology of oil-contaminated desert soils and coastal areas in the arabian gulf region in Microbiology of Extreme Soils, P. Dion and C.S. Nautiyal (eds) Springer Berlin Heidelberg. 275-298.

105. Radwan SS, D Al-Mailem, I El-Nemr, S Salamah (2000) Enhanced remediation of hydrocarbon contaminated desert soil fertilized with organic carbons. International Biodeterioration & Biodegradation 46: 129-132.

106. Radwan SS, Sorkhoh NA, Fardoun F, al-Hasan RH (1995) Soil management enhancing hydrocarbon biodegradation in the polluted Kuwaiti desert. Appl Microbiol Biotechnol 44: 265-270.

107. Reichenberg F, Mayer P (2006) Two complementary sides of bioavailability: accessibility and chemical activity of organic contaminants in sediments and soils. Environ Toxicol Chem 25: 1239-1245.

108. Reid BJ, Jones KC, Semple KT (2000) Bioavailability of persistent organic pollutants in soils and sediments--a perspective on mechanisms, consequences and assessment. Environ Pollut 108: 103-112.

109. Reilley KA, MK Banks, AP Schwab (1996) Dissipation of polycyclic aromatic hydrocarbons in the rhizosphere. Journal of Environmental Quality 25: 212-219.

110. Robertson GP, S Grabndy (2006) Soil system management in temperate regions, in Biological Approaches to Sustainable Soil Systems, CRC Press: Boca Raton, Florida.

111. Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409: 1092-1101.

112. Ruberto L, Vazquez SC, Mac Cormack WP (2003) Effectiveness of the natural bacterial flora, biostimulation and bioaugmentation on the bioremediation of a hydrocarbon contaminated antarctic soil. International Biodeterioration & Biodegradation 52: 115-125.

113. Semple KT, Doick KJ, Jones KC, Burauel P, Craven A, et al. (2004) Defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environ Sci Technol 38: 228A-231A.

114. Semple KT, Doick KJ, Wick LY, Harms H (2007) Microbial interactions with organic contaminants in soil: definitions, processes and measurement. Environ Pollut 150: 166-176.

115. Semple KT, Morriss AWJ, Paton GI (2003) Bioavailability of hydrophobic organic contaminants in soils: Fundamental concepts and techniques for analysis. European Journal of Soil Science 54: 809-818.

116. Shelton DR, Parkin TB (1991) Effect of moisture on sorption and biodegradation of carbofuran in soil. Journal of Agricultural & Food Chemistry 39: 2063-2068.

117. Shuttleworth KL, Cerniglia CE (1995) Environmental aspects of PAH biodegradation. Appl Biochem Biotechnol 54: 291-302.

118. Six J, Feller C, Denef K, Ogle SM, C MSJ, et al. (2002) Soil organic matter, biota and aggregation in temperate and tropical soils – effects of no-tillage. Agronomie 22: 755-775.

119. Smith DJT, Edelhauser EC, Harrison RM (1995) Polynuclear aromatic hydrocarbon concentrations in road dust and soil samples collected in the United Kingdom and Pakistan. Environmental Technology 16: 45-53.

120. Soclo HH, Garrigues P, Ewald M (2000) Origin of polycyclic aromatic hydrocarbons (PAHs) in coastal marine sediments: case studies in Cotonou (Benin) and Aquitaine (France) areas. Marine Pollution Bulletin 40: 387-396.

121. Spain JC, Van Veld PA (1983) Adaptation of natural microbial communities to degradation of xenobiotic compounds: effects of concentration, exposure time, inoculum, and chemical structure. Appl Environ Microbiol 45: 428-435.

122. Stokes JD, Paton GI, Semple KT (2005) Behaviour and assessment of bioavailability of organic contaminants in soil: relevance for risk assessment and remediation. Soil Use and Management 21: 475-486.

123. Stroud JL, Paton GI, Semple KT (2007) Microbe-aliphatic hydrocarbon interactions in soil: implications for biodegradation and bioremediation. J Appl Microbiol 102: 1239-1253.

124. Takada H, Ishiwatari R (1990) Biodegradation experiments of linear alkylbenzenes (LABs) - isomeric composition of C-12 LABs as an indicator of the degree of LAB degradation in the aquatic environment. Environmental Science & Technology 24: 86-91.

125. Tin T, Fleming KA, Hughes DG, Ainley P, Convey CA, et al. (2009) Impacts of local human activities on the Antarctic environment. Antarctic Science 21: 3-33.

126. Trapido M (1999) Polycyclic aromatic hydrocarbons in estonian soil: contamination and profiles. Environmental Pollution 105: 67-74.

127. Trumbore SE (1993) Comparison of carbon dynamics in tropical and temperate soils using radiocarbon measurements. Global Biogeochemical Cycles 7: 275-290.

128. Uyttebroek M, Ortega-Calvo JJ, Breugelmans P, Springael D (2006) Comparison of mineralization of solid-sorbed phenanthrene by polycyclic aromatic hydrocarbon (PAH)-degrading Mycobacterium spp. and Sphingomonas spp. Appl Microbiol Biotechnol 72: 829-836.

129. Vadali M (2001) Bioremediation. An overview. Pure & Applied Chemistry 73: 1163-1172.

130. van der Meer JR, de Vos WM, Harayama S, Zehnder AJ (1992) Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol Rev 56: 677-694.

131. Vogt NB, F Brakstad, K Thrane, S Nordenson, J Krane, et al. (1987) Polycyclic aromatic hydrocarbons in soil and air: statistical analysis and classification by the simca method. Environmental Science & Technology 21: 35-44.

132. Walworth JL, Reynolds CM (1995) Bioremediation of a petroleum‐contaminated cryic soil: effects of phosphorus, nitrogen, and temperature. Journal of Soil Contamination 4: 299-310.

133. Wania F, Mackay D (1996) Peer reviewed: tracking the distribution of persistent organic pollutants. Environ Sci Technol 30: 390A-6A.

134. Webster J, Webster K, Nelson P, Waterhouse E (2003) The behaviour of residual contaminants at a former station site, Antarctica. Environ Pollut 123: 163-179.

135. Wharton DA (2002) Life at the limits: Organisms in Extreme Environments. Cambridge university press Cambridge 14: 427-431.

136. Whyte LG, Bourbonnière L, Bellerose C, Greer CW (1999) Bioremediation assessment of hydrocarbon-contaminated soils from the high Arctic. Bioremediation Journal 3: 69-80.

137. Wilcke W(2000) Synopsis polycyclic aromatic hydrocarbons (PAHs) in soil — a review. Journal of Plant Nutrition & Soil Science 163: 229-248.

138. Wilcke W (2007) Global patterns of polycyclic aromatic hydrocarbons (PAHs) in soil. Geoderma 141: 157-166.

139. Wilcke W, Amelung W, Krauss M, Martius C, Bandeira A, et al. (2003) Polycyclic aromatic hydrocarbon (PAH) patterns in climatically different ecological zones of Brazil. Organic Geochemistry 34: 1405-1417.

140. Wilcke W, Amelung W, Martius C, Garcia MVB, Zech W (2000) Biological

Citation: Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘Pristine’ Soils from Different Climatic Regions. J Bioremed Biodegrad S1:006. doi:10.4172/2155-6199.S1-006

Page 11 of 11

ISSN: 2155-6199 JBRBD, an open access journalBioremediation: Environmental MicrobiologyJ Bioremed Biodegrad

sources of polycyclic aromatic hydrocarbons (PAHs) in the Amazonian rain forest. Journal of Plant Nutrition and Soil Science 163: 27-30.

141. Wilcke W, Krauss M, Amelung W (2002) Carbon isotope signature of polycyclic aromatic hydrocarbons (PAHs): evidence for different sources in tropical and temperate environments? Environ Sci Technol 36: 3530-3535.

142. Wilcke W, Müller S, Kanchanakool, Niamskul C, Zech W (1999) Polycyclic aromatic hydrocarbons in hydromorphic soils of the tropical metropolis Bangkok. Geoderma 91: 297-309.

143. Wilcke W, Zech W (1997) Polycyclic aromatic hydrocarbons (PAHs) in forest floors of the northern Czech mountains. Zeitschrift für Pflanzenernährung und Bodenkunde 160: 573-579.

144. Wilcke W, Zech W, Kobza J (1996) PAH-pools in soils along a PAH-deposition gradient. Environ Pollut 92: 307-313.

145. Wild SR, Berrow ML, Jones KC (1991) The persistence of polynuclear aromatic hydrocarbons (PAHs) in sewage sludge amended agricultural soils. Environ Pollut 72: 141-157.

146. Wild SR, Jones KC (1993) Biological and abiotic losses of polynuclear aromatic hydrocarbons (PAHs) from soils freshly amended with sewage sludge. Environmental Toxicology & Chemistry 12: 5-12.

147. Wild SR, Jones KC (1995) Polynuclear aromatic hydrocarbons in the United Kingdom environment: a preliminary source inventory and budget. Environ Pollut 88: 91-9108.

148. Wild SR, KS Waterhouse, SP McGrath, KC Jones (1990) Organic contaminants in an agricultural soil with a known history of sewage sludge amendments: polynuclear aromatic hydrocarbons. Environmental Science & Technology 24: 1706-1711.

149. Wilson SC, Jones KC (1993) Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): a review. Environ Pollut 81: 229-249.

150. Xing B, Pignatello JJ (1997) Dual-mode sorption of low-polarity compounds in glassy poly(vinyl chloride) and soil organic matter. Environmental Science & Technology 31: 792-799.

151. Yang SYN, Connell DW, Hawker DW, Kayal SI (1991) Polycyclic aromatic hydrocarbons in air, soil and vegetation in the vicinity of an urban roadway. The Science of The Total Environment 102: 229-240.

152. Youngblood WW, Blumer M (1975) Polycyclic aromatic hydrocarbons in the environment: homologous series in soils and recent marine sediments. Geochimica et Cosmochimica Act 39: 1303-1314.

153. Zander (1983) Physical and chemical properties of polycyclic aromatic hydrocarbons. Handbook of Polycyclic Aromatic Hydrocarbons, Marcel Dekker: New York, 1-26.

154. Zeinali M, Vossoughi M, Ardestani SK, Babanezhad E, Masoumian M (2007) Hydrocarbon degradation by thermophilic Nocardia otitidiscaviarum strain TSH1: physiological aspects. J Basic Microbiol 47: 534-539.

155. Zhang XX, Cheng SP, Zhu CJ, Sun SL (2006) Microbial PAH-degradation in soil: degradation pathways and contributing factors. Pedosphere 16: 555-565.

156. Zhang XL, Tao S, Liu WX, Yang Y, Zuo Q, et al. (2005) Source diagnostics of polycyclic aromatic hydrocarbons based on species ratios: a multimedia approach. Environ Sci Technol 39: 9109-9114.

Thisarticlewasoriginallypublishedinaspecialissue,Bioremediation: En-vironmental Microbiology handledbyEditor(s).Dr.HebeMónicaDionisi,PatagonianNationalResearchCenter,Argentina.