Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons under anaerobic conditions: Overview of studies, proposed pathways and future perspectives☆
Graphical abstract
Introduction
Polycyclic aromatic hydrocarbons (PAHs) are organic compounds consisting of carbon and hydrogen, forming aromatic cycles with 2 or more rings. These molecules are all solid and stable, and therefore, they have high melting and boiling points and low solubility in aqueous solutions (Masih et al., 2012). As the number of rings increases, the aqueous solubility of PAHs decreases, leading to their persistence in the environment; thus, these compounds represent an important class of environmental pollutants (Abdel-Shafy and Mansour, 2016).
PAHs comprise low-molecular-weight PAHs (LMW-PAHs) with two rings, such as naphthalene (NAPH), and three-ring fluorene (FLR), anthracene (ANT), and phenanthrene (PHEN); and high-molecular-weight PAHs (HMW-PAHs) with four or more rings. The HMW-PAHs include pyrene (PYR), chrysene, and fluoranthene (FLT) [four rings] as well as benzo[a]pyrene (BZP) and benzo[a]anthracene [five rings] (Fig. 1) (Abdel-Shafy and Mansour, 2016).
The negative effects of these compounds on various organisms have been well documented. PAHs display moderate to high levels of acute toxicity in aquatic life and birds, including toxic effects on the development of the reproductive system, immunity and a risk of tumour development (Abdel-Shafy and Mansour, 2016; Kim et al., 2013). In humans in particular, and in mammals in general, PAHs have been shown to be carcinogenic and teratogenic (Abdel-Shafy and Mansour, 2016; Ohura et al., 2004), and compelling evidence indicates that humans who are exposed to PAHs develop lung cancer (Abdel-Shafy and Mansour, 2016; Kim et al., 2013). In addition, a growing body of evidence also indicates a possible role for PAHs as endocrine disruptors (Zhang et al., 2016).
The environment is contaminated with PAHs primarily derived from pyrogenic and petrogenic sources. In general, PAH production from pyrogenic processes originates from the exposure of organic molecules to high temperatures under low levels of or in the absence of oxygen. These situations include the transformation of coal into coke and coal tar, the thermal cracking of petroleum products into lighter hydrocarbons, the incomplete combustion of fuels in motor vehicles and the combustion of wood in forest fires and fireplaces (Abdel-Shafy and Mansour, 2016). Additionally, PAHs originating from petrogenic sources are produced by petroleum product spills and leakage during transport, storage and refinery processes. In addition, PAHs (primarily those derived from petroleum products) have various industrial uses, such as in the lubrication of photographic products and thermosetting plastics (Abdel-Shafy and Mansour, 2016). The waste generated by these industrial activities further increases PAH contamination in the environment.
In natural settings, these pollutants are removed by biodegradation, a process based on the ability of microorganisms to use these pollutants as their carbon and energy sources. PAH biodegradation have been extensively examined under aerobic conditions, as shown by the substantial number of papers on this topic. This form of biodegradation has been evaluated in various environments (soil, sea, and sediments); PAH-degrading microorganisms have been characterised, and the PAH biochemical pathways have been elucidated (Haritash and Kaushik, 2009; Nzila, 2013; Seo et al., 2009). Comparatively, little is known about the anaerobic biodegradation of these compounds.
As discussed earlier, PAHs are not soluble in aqueous solutions; therefore, they tend to accumulate in the environment. For example, they accumulate in the lower soil layer, where the O2 concentration is reduced or even zero (Li et al., 2009). Because O2 is required for both ring opening and terminal electron acceptor (TEA) activity, aromatic compounds may not undergo biodegradation in anoxic environments. However, naturally occurring anaerobic microorganisms with unique biochemical characteristics that are present within these environments would likely degrade these compounds. This concept was supported in the 1980s, when the first evidence of mono- and dicyclic aromatic hydrocarbon biodegradation was provided (Evans and Fuchs, 1988; Mihelcic and Luthy, 1988). Since then, more studies have been dedicated to examining the biodegradation of aromatic compounds and understanding the mechanisms underlying this process. However, a careful examination of the studies published to date shows a primary focus on the monocyclic aromatic hydrocarbon (MAH) benzene and its derivatives as well as the LMW-PAH NAPH and its derivatives. Readers are referred to several excellent reviews that summarise this work (Ghattas et al., 2017; Heider and Fuchs, 1997; Meckenstock and Mouttaki, 2011; Meckenstock et al., 2004).
However, the anaerobic biodegradation of HMW-PAHs (PYR and BZP) and, to some extent, the LMW-PAHs PHEN and ANT, have received little attention compared with that of MAH and NAPH. The reason is that the high complexity of these PAHs makes them less amenable to anaerobic biodegradation. Nevertheless, few reports have investigated their biodegradation, and the current review attempts to summarise this work. The anaerobic degradation of MAH and NAPH are excluded from this review, except in terms of a broader overview. This review identifies important knowledge gaps that limit our understanding of the anaerobic biodegradation of PAHs, and it also proposes future research strategies to overcome these limitations. Overall, this review suggests new avenues for research on the anaerobic biodegradation of complex PAHs.
Section snippets
Reduction conditions, TEAs and ATP formation
Respiration is a process in which the cell converts the energy stored in organic compounds to ATP (adenosine triphosphate). This process is initiated by the breakdown of organic compounds into smaller compounds and eventually to CO2, releasing electrons that will drive the conversion of ADP (adenosine diphosphate) to ATP (Fig. 2). For this process to continue, these electrons must be captured in fine by TEAs. Oxygen is the TEA under aerobic conditions, whereas in an anaerobic (or anoxic)
Anaerobic biodegradation of HMW-PAHs
The anaerobic biodegradation of PHEN, ANT, PYR and BZP has been investigated using single PAHs and mixtures of various PAH compounds. Thus, the author summarised studies in which single substrates were used to obtain a better understanding of this process.
Chemical pathways of the anaerobic biodegradation of HMW-PAHs
The MAH and PAH biodegradation processes have been well studied under aerobic conditions. Biodegradation is always initiated by the addition of molecular O2 to one of the rings, a process that is mediated by mono- and di-oxygenases, leading to the hydroxylation of PAHs. This addition weakens the C-C bond, rendering it amenable to cleavage. The same ring cleavage process continues until all the rings are cleaved, leading to the generation of acetate, which enters the Krebs cycle to promote
Limitations in anaerobic biodegradation and possible strategies to overcome these limitations
This PAH anaerobic degradation process has 3 advantages: the first is the removal of pollutants; the second is the reduction (and therefore the removal) of sulfate and nitrates from various environments (water or soil); and the third is the possibility of producing biomethane, an alternative energy source. These advantages contrast with aerobic biodegradation, a process that only leads to the removal of pollutants. Thus, strategies aiming to improve the efficiency of anaerobic PAH
Future perspectives and concluding remarks
Approximately 20 years ago, the high stability of the HMW-PAHs was postulated to hinder their biodegradation in the absence of O2. However, microorganisms have devised various mechanisms to activate HMW-PAH rings, thus making them more amenable to ring opening and subsequent biodegradation. The anaerobic biodegradation of HMW-PAHs has been achieved under sulfate-, nitrate-, and metal-ion-reducing conditions as well as methanogenic conditions. However, the available knowledge based on our
Acknowledgements
The author acknowledges the support provided by King Abdulaziz City for Science and Technology through the Science and Technology Unit at King Fahd University of Petroleum and Minerals for funding this work through project No. 13-ENV1628-04 as part of the National Science, Technology and Innovation Plan of Saudi Arabia. The author thanks Dr. Musa Mohammed Musa of the Department of Chemistry, KFUPM for providing useful comments on this manuscript. Finally, the author is grateful to KFUPM for
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This paper has been recommended for acceptance by Dr. Hageman Kimberly Jill.