El delito

Biodegradation driven by many bacteria and fungi is one of the most direct pathways for the dissipation of PAHs in nature. This microbial activity is dependent on the stability of the benzene rings in the PAH molecules and on other factors related to the hydrophobicity of PAHs (Niqui-Arroyo et al., 2011). The half lives of LMW-PAHs in nature, such as phenanthrene, range from 16-126 days, while HMW-PAHs, such as benzo(a)pyrene, possess substantially longer half lives of up to 1400 days (Husain, 2008). The estimation of half-life takes into account the reduction in PAH concentrations caused mainly by biodegradation.

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The metabolic pathways for utilizing LMW-PAHs by microorganisms were studied since the 1980s, and later (in the 1990s) for HMW-PAHs. Some metabolic pathways of such LMW-PAHs like naphthalene and phenanthrene have been proposed, which are shown in Figs. 4 and 5, respectively. In case of HMW-PAHs, their metabolic pathways found in diverse bacterial taxa were well summarized by Kanaly and Harayama (2000; 2010).

Figure 4 Bacterial metabolic pathways of naphthalene to salicylate. The pathways were modified according to a summary of Eaton and Chapman (1992), where the chemical structures were drawn with MarvinSketch (http://www.chemaxon.com/marvin/sketch/index.php, Available on 5 Feb., 2014).

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Figure 5 Bacterial metabolic pathways of phenanthrene. The figure was modified according to the proposed pathways elucidated by Moody et al. (2001), where the chemical structures were drawn with MarvinSketch (http://www.chemaxon.com/marvin/sketch/index.php, Available on 5 Feb., 2014).

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The aerobic metabolism of PAHs has been well studied, and it occurs through three main catabolic activities (Cerniglia, 1992; Haritash and Kaushik, 2009; Husain, 2008; Kanaly and Harayama, 2000; Peng et al., 2008; Semple et al., 1999; Steffen et al., 2000):

1) Oxidation of aromatic ring by dioxygenase (Fig. 6), exclusively for bacteria and usually through their metabolism to use PAHs as a carbon and energy source, which may lead to a co-metabolic process;

Figure 6 Biodegradation at the first step for breaking down the aromatic ring of PAHs by dioxygenase.

The figure was summed up from the literatures cited. The chemical structures were drawn with MarvinSketch (http://www.chemaxon.com/marvin/sketch/index.php, Available on 5 Feb., 2014).

2) Oxidation by means of lignin and manganese peroxidases excreted from white-rot fungi (Fig. 7), considered as a co-metabolic process of PAHs in nature;

Figure 7 Biodegradation at the first step for breaking down the aromatic ring of PAHs by lignin and manganese peroxidases. The figure was summed up from the literatures cited. The chemical structures were drawn with MarvinSketch (http://www.chemaxon.com/marvin/sketch/index.php, Available on 5 Feb., 2014).

3) Oxidation with cytochrome P450 monooxygenase found in both prokaryotes and eukaryotes (Fig. 8), it is typically relevant to the detoxification and metabolite transform, but does not usually entail the mineralization of PAHs.

PAH

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Figure 8 Biodegradation at the first step for breaking down the aromatic ring of PAHs by cytochrome P450 monooxygenase. The figure was summed up from the literatures cited. The chemical structures were drawn with MarvinSketch (http://www.chemaxon.com/marvin/sketch/index.php, Available on 5 Feb., 2014).

The current knowledge on the biodegradation of PAHs reveals that most PAHs listed in Table 1 can be degraded through aerobic metabolism, except for some HMW-PAHs such as benzo[a]pyrene that require co-metabolic process (Kanaly and Harayama, 2000; 2010). The co-metabolism of PAHs does not provide any benefit to the microbial cells, as because it does not cause extensive modification of PAHs neither incorporation them into biomass nor direct conversion them into CO2. Recent findings have demonstrated also that microorganisms can use other electron acceptors, such as nitrates and sulphates, for oxidation of PAHs (Quantin et al., 2005; Rothermich et al., 2002). Futhermore, it was evidenced that biodegradation of PAHs in anaerobic environments could occur only in the presence of a second carbon source like acetate or glucose (Ambrosoli et al., 2005).

The biodegradation of PAHs sorbed to black carbon or NAPLs is typically a slow process that contributes to their long-term persistence in environments (Lopez et al., 2008; Ortega-Calvo and Gschwend, 2010; Ortega-Ortega-Calvo et al., 1995). Dissolved organic carbon (DOC) also plays a key role in the biodegradation of PAHs. It was found that the addition of DOC in the form of humic fractions to PAH-polluted soils caused an enhancement of biodegradation, probably as a result of the enhanced desorption of PAHs from soils to the aqueous fraction (Bengtsson and Zerhouni, 2003; Bogan and Sullivan, 2003; Haderlein et al., 2001). The other DOC-mediated enhancements of PAH biodegradation include the enlargement of PAH solubility (Liang et al., 2007), a direct access to DOC-sorbed PAHs due to the physical association of bacteria and DOC (Ortega-Calvo and Saiz-Jimenez, 1998), and an increased diffusive flux toward bacterial cells caused by DOC (Haftka et al., 2008).

PAH

Cytochrome P450- / Methane-monooxygenases Bacteria, Algae, Fungi

Arene oxide

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Due to their charged nature and high specific surface, natural clay minerals also play an important role in the biodegradation of PAHs. Microbial cells often show a high affinity for clay surfaces, as evidenced by their spontaneous association in suspensions and percolation columns (Lahlou et al., 2000; Ortega-Calvo et al., 1999; Velasco-Casal et al., 2008). This association can explain, for example, the population density of PAH-degrading mycobacteria in the PAH-enriched clay fraction of a long-term polluted soil (Uyttebroek et al., 2006).

Surface of clay can also scavenge organic chemoeffectors from the pore water by sorption, thereby eliminating their effect in promoting the transport of chemotactic bacteria through porous materials (Velasco-Casal et al., 2008), and associate with organic matter, resulting in slow desorption of PAHs with limited bioavailability to microbial degradation (Lahlou and Ortega-Calvo, 1999). Clay-rich soil may also present a limited oxygen and nutrient supply to PAH-degrading populations, due to slow diffusion and low hydraulic conductivity (Niqui-Arroyo et al., 2006).

The biodegradation in bioremediation of PAHs is often found to have a conceptual link with pollutant bioavailability and microbial accessibility toward these pollutants. This interconnection is proposed with a graphical model described in Fig. 9.