Abstract
The anaerobic oxidation of petroleum hydrocarbons can be coupled to the reduction of metals. At contaminated subsurface sites, this phenomenon will accelerate the removal of pollutants and will have an important influence on biogeochemical cycles. Due to its abundance, iron is the most prominent metallic terminal electron acceptor involved in hydrocarbon degradation followed by manganese. Dissimilatory metal-reducing microbes (DMRM) capable of oxidizing either monocyclic aromatic or polycyclic hydrocarbons are phylogenetically diverse with representatives from bacteria as well as from archaea. It has been shown that the monocyclic aromatic hydrocarbons benzene, toluene, ethylbenzene, and xylene and the polyaromatic hydrocarbons naphthalene, 1-methylnaphthalene, and 2-methylnaphtalene can be degraded by metal-reducing enrichment cultures or pure cultures. In recent years, significant breakthroughs have been made in the field of functional genomics for the characterization of the metabolic pathways, enzymes, and genes participating to hydrocarbons degradation by metal-reducing microbes. Here, we present an updated portrait of the monocyclic aromatic and polycyclic hydrocarbons metabolism of DMRM.
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1 Introduction
Contamination of sediments, soil, aquifer, and groundwater with petroleum hydrocarbons is a widespread concern posing a threat to human health and ecosystems. Due to the fast depletion of oxygen, polluted sites often become anaerobic and under these circumstances, the degradation of hydrocarbons requires the metabolic activity of microbes using other terminal electron acceptors (TEA) (Aburto-Medina and Ball 2015). This includes metals abundant in soil and sediments such as iron and manganese. Dissimilatory metal-reducing microbes (DMRM) couple the oxidation of organic molecules such as hydrocarbons with the reduction of metals as their sole TEA for energy conservation (Foght 2008). Because metals in soil and sediments are usually in a solid state, DMRM have developed unique extracellular electron transfer mechanisms. This includes direct electron transfer via outer membrane c-type cytochromes, conductive nanowires and pili as well as the synthesis of soluble electron shuttles (Lovley 2012; White et al. 2016).
The anaerobic oxidation of monocyclic aromatic hydrocarbons including benzene, toluene, ethylbenzene, and xylene has been demonstrated with DMRM-containing consortia as well as with DMRM pure cultures either with Fe(III) or Mn(IV) as the TEA (Lovley et al. 2011; Meckenstock and Mouttaki 2011; Meckenstock et al. 2016; Lovley and Lonergan 1990; Heider et al. 1998; Chakraborty and Coates 2004; Botton and Parsons 2006; Rooney-Varga et al. 1999; Jahn et al. 2005; Langenhoff et al. 1997a, b; Villatoro-Monzón et al. 2003). Furthermore, several studies have reported the microbial degradation of polycyclic hydrocarbons such as naphthalene and its derivatives with Fe(III) as TEA (Anderson and Lovley 1999; Kleemann and Meckenstock 2011). Until now, the microbial degradation of aliphatic hydrocarbons including alkane, alkene, and cycloalkane coupled with metal reduction by DMRM has never been reported.
Metabolic pathways responsible for the anaerobic oxidation of aromatic hydrocarbons by DMRM are complex and comprise multiple reactions with unique chemistry. Currently, many of those reactions are still poorly understood. This chapter will focus on the ongoing research effort aiming at elucidating the anaerobic hydrocarbon oxidation metabolism of DMRM and at characterizing the genes and enzymes involved.
2 Dissimilatory Metal-Reducing Microbes Involved in Anaerobic Hydrocarbons Degradation
Key Fe(III)-reducing microorganisms involved in the complete oxidation of monocyclic aromatic hydrocarbons at anoxic contaminated environments are often members of the Geobacteraceae family (Rooney-Varga et al. 1999) (Table 1). From this group, only pure cultures Geobacter metallireducens and Geobacter strain Ben have been shown to degrade both benzene and toluene (Lovley and Lonergan 1990; Lovley et al. 1993; Zhang et al. 2012). Two other Geobacter species, Geobacter grbiciae and Geobacter toluenoxydans, only degrade toluene (Coates et al. 2001; Kunapuli et al. 2010). Other Fe(III)-reducing bacteria capable of oxidizing toluene in pure culture include Georgfuchsia toluolica and Desulfitobacterium aromaticivorans, which are members of the Betaproteobacteria and Clostridia, respectively (Kunapuli et al. 2010; Weelink et al. 2009). D. aromaticivorans can also oxidize o-xylene with Fe(III) as TEA. When manganese is the TEA, G. toluolica and an enrichment culture dominated by an Azoarcus species can degrade both toluene and ethylbenzene (Dorer et al. 2016). Besides mesophilic bacteria, the hyperthermophilic archaeon Ferroglobus placidus can also degrade benzene and transfer electrons to Fe(III) (Holmes et al. 2011).
Polycyclic aromatic hydrocarbons degradation by metal-reducing microbes was demonstrated initially via the anaerobic oxidation of naphthalene with Fe(III) as the TEA (Anderson and Lovley 1999). Community composition involved in polycyclic aromatic hydrocarbons degradation with metal as TEA has not been investigated as much as for BTEX degradation. The only study to our knowledge on bacterial population in Fe(III)-reducing enrichment degrading naphthalene identified a Gram-positive spore-forming bacterium of the Peptococcaceae family as the dominating species (Kleemann and Meckenstock 2011). This enrichment could also degrade 1-methylnaphthalene and 2-methylnaphthalene.
3 Degradation of Monocyclic Aromatic Compounds
Genes, enzymes, and metabolic pathways involved in monocyclic aromatic hydrocarbons degradation by metal-reducing bacteria have mainly been studied in G. metallireducens, which is genetically tractable and had its genome sequenced in 2005 (Tremblay et al. 2012; Oberender et al. 2012; Butler et al. 2007; Lovley and Lonergan 1990; Lovley et al. 1993; Zhang et al. 2012). Genome survey of G. metallireducens have led to the identification of genes participating in the anaerobic oxidation of monocyclic aromatic hydrocarbons and of other monocyclic aromatic compounds including phenol, para-cresol, benzyl alcohol, benzaldehyde, and 4-hydroxybenzoate (Butler et al. 2007; Heinnickel et al. 2010). Additionally, G. metallireducens has been used as a model bacterium to study extracellular electron transfer to insoluble TEA such as Fe(III) oxide or the electrode of a bioelectrochemical system for electricity production (Lovley 2012; Bond et al. 2002; Smith et al. 2013).
3.1 Degradation of Benzene to Benzoyl-CoA
Because of its structural stability and high solubility in water, benzene is the most persistent monocyclic aromatic hydrocarbon in the environment (Vogt et al. 2011). Benzene is harmful for humans and other animals as it can cause cancer and aplastic anemia and impairs the reproductive system (Aburto-Medina and Ball 2015). Anaerobic bacteria such as G. metallireducens convert monocyclic aromatic compounds including benzene into the central intermediate benzoyl-CoA before subsequent dearomatization (Heinnickel et al. 2010; Zhang et al. 2012) (Fig. 1). The metabolic pathway from benzene to benzoyl-CoA in G. metallireducens has not been completely characterized yet. Several activation mechanisms with specific thermodynamic constraints have been proposed as the first step of anaerobic benzene oxidation including hydroxylation to phenol, carboxylation to benzoate or methylation to toluene (Vogel and Grbìc-Galìc 1986; Grbić-Galić and Vogel 1987; Caldwell and Suflita 2000; Chakraborty and Coates 2005; Abu Laban et al. 2009, 2010; Phelps et al. 2001; Kunapuli et al. 2008; Ulrich et al. 2005). In 2013, Zhang et al. presented evidences indicating that benzene is degraded via hydroxylation to phenol by G. metallireducens. In this study, phenol was labeled with 18O when H218O was added to benzene-oxidizing cell suspension and complete benzene oxidation to CO2 was inhibited when genes essential for the phenol metabolism were deleted (Zhang et al. 2013). A recent functional genetic study led to the identification of two adjacent genes (Gmet_0231 and Gmet_0232) coding for a zinc-containing oxidoreductase and a hypothetical protein required for benzene oxidation but not for phenol oxidation that may be involved in the first step of benzene degradation (Zhang et al. 2014). Still, the identity of the enzyme responsible for benzene hydroxylation and its mechanism of action are still unclear.
The suggested product of benzene hydroxylation, phenol, is degraded in G. metallireducens via a metabolic pathway analogous to the one found in the denitrifying bacterium Thauera aromatica (Butler et al. 2007; Breinig et al. 2000) (Fig. 1a). Phenol is first converted to phenylphosphate by an ATP-dependent phenylphosphate synthase composed of three different subunits (PpsABC) (Schmeling et al. 2004). Phenylphosphate is then carboxylated by a phenylphosphate carboxylase (PpcBD) to 4-hydroxybenzoate. In T. aromatica, the phenylphosphate carboxylase has four subunits. The δ-subunit is thought to catalyze the exergonic dephosphorylation of phenylphosphate resulting in a phenolate anion that will be carboxylated with CO2 by the subunits α, β, and γ (Schühle and Fuchs 2004). Phenylphosphate carboxylase activity has been detected in G. metallireducens but the enzyme structure and mechanism of action may be different from T. aromatica since only two subunits are encoded on the genome (Schleinitz et al. 2009; Lovley et al. 2011). Subsequently, 4-hydroxybenzoate is converted to 4-hydroxybenzoyl-CoA by a 4-hydroxybenzoate-CoA ligase. Activity of this enzyme has been detected in G. metallireducens but its exact identity is still unknown (Peters et al. 2007; Wischgoll et al. 2005). Finally, 4-hydroxybenzoyl-CoA is reduced to benzoyl-CoA by a 4-hydroxybenzoyl-CoA reductase composed of three subunits (α2β2γ2) (PcmRST) (Butler et al. 2007; Breese and Fuchs 1998).
Other studies suggested that carboxylation is also an important benzene activation reaction in hydrocarbons contaminated environments. Proteome analysis of a benzene-degrading mixed community dominated by Peptococcaceae-related Gram-positive bacteria led to the identification of a putative anaerobic benzene carboxylase (Abu Laban et al. 2010). This enzyme is probably formed by at least two subunits (AbcDA) homologous to proteins comprised in two families of carboxylases: phenylphosphate carboxylase and 3-octaprenyl-4-hydroxybenzoate carboxy-lyase. Furthermore, benzoate is an important intermediate of benzene degradation in the Fe(III)-reducing archaeon F. placidus (Holmes et al. 2011) (Fig. 1b). Accumulation of trace amounts of benzoate as well as higher transcript abundance of genes thought to be involved in the conversion of benzene to benzoate during benzene metabolism are evidences supporting a carboxylation-dependent pathway in F. placidus. One upregulated gene in particular is thought to code for a putative benzene carboxylase homologous to proteins of the 3-octaprenyl-4-hydroxybenzoate carboxy-lyase (UbiD-like) family. After benzene carboxylation, benzoate will be converted to benzoyl-CoA at the expense of ATP via a benzoate-CoA ligase (Bcl1/BamY) formed by a single protein (Holmes et al. 2011; Butler et al. 2007; Schühle et al. 2003).
3.2 Degradation of Toluene, Ethylbenzene, and Xylene
Degradation of toluene by DMRM such as G. metallireducens involves the addition of fumarate to toluene via glycyl radical mediated C-C bond formation by a benzylsuccinate synthase yielding benzylsuccinate (Butler et al. 2007; Rabus et al. 2005; Rabus 2005) (Fig. 2). The benzylsuccinate synthase comprises three subunits with a (αβγ)2 structure (BssABC) (Leuthner et al. 1998). The catalytic α-subunit harbors a glycyl radical enzyme fold surrounding the glycyl radical cofactor and the active site (Funk et al. 2014). The glycyl radical cofactor will be formed from a conserved glycine residue by an activating enzyme (BssD) of the S-adenosyl-L-methionine radical enzymes superfamily (Leuthner et al. 1998). The function of subunits β and γ that both possess a FeS cluster is still unclear (Li et al. 2009; Hilberg et al. 2012). Recently, it has been suggested that they may be involved in modulating the conformational dynamics of the benzylsuccinate synthase enzyme (Funk et al. 2014).
Subsequently, a succinyl-CoA:benzylsuccinate CoA transferase will transfer coenzyme A from succinyl-CoA to benzylsuccinate generating benzylsuccinyl-CoA and succinate (Heider et al. 1998). This enzyme comprises two subunits (BbsEF) arranged in a α2β2 structure (Leutwein and Heider 2001). Benzylsuccinyl-CoA will then be oxidized to (E)-phenylitaconyl-CoA by a benzylsuccinyl-CoA dehydrogenase (BbsG) (Leutwein and Heider 2002). Deletion of the gene bbsG coding for this homotetrameric enzyme in G. metallireducens eliminates its capacity to degrade toluene further confirming the importance of this enzyme (Chaurasia et al. 2015). E-phenylitaconyl-CoA will then be converted by a (E)-phenylitaconyl-CoA hydratase (BbsH) into 2-carboxymethyl-3-hydroxy-phenylpropionyl-CoA which will be oxidized into benzoyl-succinyl-CoA by a 3-hydroxyacyl-CoA dehydrogenase (BbsCD). Finally, the succinyl-CoA moiety is replaced by CoA in a reaction catalyzed by a benzoylsuccinyl-CoA thiolase (BbsB) to generate the central metabolite benzoyl-CoA (Butler et al. 2007; Leuthner and Heider 2000).
Metabolic pathways involved in ethylbenzene and o-xylene oxidation by iron-reducing bacteria including G. toluolica and D. aromaticivorans are poorly characterized. A mixed culture dominated by an Azoarcus species has been shown to couple the degradation of ethylbenzene with manganese reduction (Dorer et al. 2016). In this study, it is not clear if the Azoarcus species is directly coupling ethylbenzene oxidation with manganese reduction or if a syntrophic interaction with another microbial species is required. In the closely related denitrifying bacterium Azoarcus sp. EbN1, degradation of ethylbenzene is initiated by the hydroxylation of the C1-methylene carbon of the sidechain yielding (S)-1-phenylethanol, which is catalyzed by an ethylbenzene dehydrogenase (EbdABC) (Fuchs et al. 2011; Ball et al. 1996; Kniemeyer and Heider 2001a) (Fig. 3). The ethylbenzene dehydrogenase is a heterotrimeric molybdoenzyme located in the periplasmic space of microbial cells (Heider et al. 2016; Kloer et al. 2006). (S)-1-phenylethanol is then oxidized to acetophenone by a (S)-1-phenylethanol dehydrogenase (Ped) (Kniemeyer and Heider 2001b). Later, acetophenone is carboxylated into benzoylacetate in an ATP-dependent manner by a complex acetophenone carboxylase comprising five different subunits (ApcABCDE) (Jobst et al. 2010). Subsequently, benzoylacetate is activated to benzoylacetate-CoA by a putative benzoylacetate-CoA ligase (Bal). In the last step, benzoylacetate-CoA is cleaved into benzoyl-CoA and acetyl-CoA by an unknown thiolase (Rabus 2005; Muhr et al. 2015). In the case of o-xylene, a lot less is known about its degradation pathway, but the initial reaction is possibly the addition of a fumarate molecule to the alkyl side-chain by a glycyl radical enzyme (Heider 2007).
3.3 Benzoyl-CoA Reduction
As described above, benzene, toluene, ethylbenzene, and o-xylene are converted to the central metabolite benzoyl-CoA in DMRM. The next step in the degradation of monocyclic aromatic hydrocarbons is the two electrons reduction of benzoyl-CoA to cyclohex-1,5-diene-1-carboxyl-CoA, a reaction comparable to the chemical Birch reduction catalyzed by the benzoyl-CoA reductases (Boll et al. 2014) (Fig. 4). Two different classes of benzoyl-CoA reductases are active in DMRM. In the strictly anaerobic archeon F. placidus, an ATP-consuming class I benzoyl-CoA reductase is responsible for the dearomatization of benzoyl-CoA during benzene metabolism (Holmes et al. 2011) (Fig. 4a). This is unusual since class I benzoyl-CoA reductases are normally found in facultative anaerobes, while strict anaerobes possess class II benzoyl-CoA reductases (Boll et al. 2014). The four genes (bzdNOPQ) coding for the class I benzoyl-CoA reductase found in the genome of F. placidus had higher transcript abundance in benzene-grown cells compared to acetate-grown cells. Recently, in vitro assays with purified BzdNOPQ showed that these proteins catalyze the ATP-dependent reduction of benzoyl-CoA with two electrons to cyclohex-1,5-diene-1-carboxyl-CoA (Schmid et al. 2015, 2016). The four subunits of the class I benzoyl-CoA reductases are organized in two different modules (Boll et al. 2014). The first module composed of subunits α (BzdQ) and δ (BzdP) harbors two ATP-binding sites and a single bridging [4Fe-4S] cluster. Its function is to transfer electrons from reduced ferredoxins in an ATP-dependent manner to the second modules catalyzing the benzoyl-CoA ring reduction (Boll 2005). The second module formed by subunits β (BzdO) and γ (BzdN) includes the benzoyl-CoA binding site as well as two [4Fe-4S] clusters involved in electron transport to the substrate.
In the model bacterium G. metallireducens that is a strict anaerobe, an ATP-independent class II benzoyl-CoA reductase is responsible for the dearomatization of benzoyl-CoA (Löffler et al. 2011; Boll et al. 2014) (Fig. 4a). Class II benzoyl-CoA reductases require significantly less energy than class I benzoyl-CoA reductases and this is probably the reason why class II enzymes are widespread in strict anaerobes. Class II benzoyl-CoA reductase of G. metallireducens is encoded by a cluster of eight genes, bamBCDEFGHI (Wischgoll et al. 2005). A recent study showed that the enzyme is crystallized as a Bam(BC)2 heterotetramer (Weinert et al. 2015). The substrate benzoyl-CoA binds to the subunit BamB (Kung et al. 2009). Reduction of the substrate occurs via electrons transferred from the tungsten-bispyranopterin monophosphate cofactor of the BamB subunit. A single [4Fe-4S] cluster in BamB and three [4Fe-4S] clusters in BamC have been proposed to shuttle electrons from BamDEF to the tungsten-bispyranopterin monophosphate cofactor (Weinert et al. 2015). The exact function of the products of bamDEFGHI genes is still unknown, but the amino acids sequences and the presence of binding sites for flavin adenine dinucleotide cofactors suggest that they could participate in an energy conservation mechanism analogous to flavin-based electron bifurcation coupling endergonic and exergonic redox reactions (Boll et al. 2014; Buckel and Thauer 2013). It has been hypothesized that electrons from the oxidation of four reduced ferredoxins are bifurcated by the BamCDEF module for the endergonic reduction of benzoyl-CoA by BamB and the exergonic reduction of NAD+, which has been predicted to bind to the BamGHI module (Boll et al. 2014; Fuchs et al. 2011).
3.4 Degradation of Cyclohex-1,5-Diene-1-Carboxyl-CoA to Central Carbon Metabolites
After benzoyl-CoA reduction, metal-reducing bacteria such as G. metallireducens as well as the archaeon F. placidus convert cyclohex-1,5-diene-1-carboxyl-CoA to 3-hydroxypimeloyl-CoA via a pathway widespread in microbes oxidizing monocyclic aromatic compounds that was initially characterized in T. aromatica (Butler et al. 2007) (Fig. 4b). This pathway comprises three reactions and starts with the addition of water to cyclohex-1,5-diene-1-carboxyl-CoA by a hydratase (BamR) yielding 6-hydroxycyclohex-1-ene-1-carboxyl-CoA (Peters et al. 2007; Laempe et al. 1998; Schmid et al. 2015). This product is then converted to 6-oxocyclohexa-1-ene-1-carboxyl-CoA by a NAD+-dependent dehydrogenase (BamQ). The third reaction is catalyzed by a 6-oxocyclohex-1-ene-1-carboxyl-CoA hydratase (BamA) and consists in a hydration followed by ring cleavage to form 3-hydroxypimeloyl-CoA (Kuntze et al. 2008; Schmid et al. 2015; Laempe et al. 1998). This molecule will be further oxidized via three steps: (1) a dicarboxylic acid oxidation pathway, (2) followed by a decarboxylation and oxidation reaction catalyzed by a decarboxylating glutaryl-CoA dehydrogenase, and (3) a short-chain fatty acid oxidation pathway. In total, the oxidation of 3-hydroxypimeloyl-CoA requires six reactions and yields three acetyl-CoA molecules (Harwood and Gibson 1997; Carmona et al. 2009; Wischgoll et al. 2009).
4 Polycyclic Aromatic Hydrocarbons Degradation Pathway in Iron-Reducing Gram-Positive Bacteria
Two initial activation mechanisms have been proposed for the degradation of naphthalene by anaerobic microbes including DMRM (Fig. 5). The first mechanism proceeds via the carboxylation of naphthalene into 2-naphthoic acid. Experimental evidence supporting this pathway includes the accumulation of the metabolite 2-naphthoic acid during naphthalene degradation (Kleemann and Meckenstock 2011; Meckenstock et al. 2000; Zhang et al. 2000). Furthermore, growth with naphthalene in 13C–bicarbonate-buffered medium resulted in the formation of 13C–labelled 2-naphthoic acid (Zhang and Young 1997; Mouttaki et al. 2012). Alternatively, naphthalene degradation could be activated via a methylation reaction yielding 2-methyl-naphthalene (Safinowski and Meckenstock 2006). However, biochemical evidence supporting a naphthalene methylation pathway is lacking until now.
In recent years, the carboxylation pathway has mainly been investigated in naphthalene-degrading sulfate-reducing bacteria. The activation reaction in this pathway is mediated by an ATP-independent naphthalene carboxylase (Mouttaki et al. 2012) (Fig. 5a). Proteomic investigation and genome survey carried out in the sulfate-reducing enrichment culture N47 led to the identification of the α- and β-subunits of a putative carboxylase possibly catalyzing the conversion of naphthalene into 2-naphthoic acid (Bergmann et al. 2011). The genes coding for these two subunits are found in a cluster organized similarly in N47 as well as in the naphthalene-degrading sulfate-reducing Deltaproteobacterium NaphS2 (DiDonato et al. 2010).
Subsequently, 2-naphthoic acid is converted into 2-naphthoyl-CoA by an ATP-dependent 2-naphthoyl-CoA ligase (Eberlein et al. 2013b). 2-naphthoyl-CoA is then converted into 5,6-dihydro-2-naphthoyl-CoA via a two-electron reduction mediated by a 2-naphthoyl-CoA reductase, a member of the “old yellow enzyme family” of flavoproteins (Estelmann et al. 2015). The 5,6,-dihydro-2-naphthoyl-CoA formed is subsequently reduced with two electrons into 5,6,7,8-tetrahydro-2-naphthoyl-CoA by a 5,6-dihydro-2-naphthoyl-CoA reductase (Eberlein et al. 2013a; Estelmann et al. 2015). The 2-naphthoyl-CoA reductase and the 5,6-dihydro-2-naphthoyl-CoA reductase could not be completely separated via purification steps, and there is a significant possibility that both enzymes form a complex in vivo. In the next step, 5,6,7,8-tetrahydro-2-naphthoyl-CoA is possibly reduced to hexahydro-naphthoyl-CoA by an ATP-dependent class I benzoyl-CoA reductase with two electrons (Eberlein et al. 2013b; Estelmann et al. 2015). Until now, the natural electron donors of both the 2-naphtoyl-CoA reductase and the 5,6-dihydro-2-naphthoyl-CoA reductase are unknown, but genes located nearby as well as cofactors associated with the enzymes indicate that a flavin-based electron bifurcation energy conservation mechanism may be involved (Estelmann et al. 2015). After dearomatization, it has been suggested that the complete degradation of naphthalene to CO2 is continued further via cyclohexane ring comprising CoA esters instead of monocyclic aromatic compounds (Annweiler et al. 2002).
Until now, the anaerobic degradation pathway of 1-methylnaphthalene remains unresolved (Kleemann and Meckenstock 2011). Like with naphthalene, the degradation pathway of 2-methyl-naphthalene has not been investigated in metal-reducing microbes but only in sulfate-reducing bacteria (Annweiler et al. 2000; Annweiler et al. 2002; Safinowski and Meckenstock 2004; Musat et al. 2009). Similar to anaerobic toluene oxidation, 2-methylnaphthalene is first converted to naphthyl-2-methyl-succinate by the addition of a fumarate molecule to the methyl group (Selesi et al. 2010) (Fig. 5b). This reaction is mediated by the glycyl radical enzyme naphthyl-2-methyl-succinate synthase (NmsABC). Subsequently, naphthyl-2-methyl-succinate is activated to yield naphthyl-2-methylene-succinyl-CoA by the naphthyl-2-methyl-succinate CoA transferase (BnsEF). The following four reactions catalyzed respectively by a naphthyl-2-methyl-succinyl-CoA dehydrogenase (BnsG), a naphthyl-2-methylene-succinyl-CoA hydratase (BnsH), a naphthyl-2-hydroxymethyl-succinyl-CoA dehydrogenase (BnsCD), and a naphthyl-2-oxomethyl-succinyl-CoA thiolase (BnsAB) result in the β-oxidation of the side chain leading to the formation of 2-naphtoyl-CoA, which will then be dearomatized.
5 Research Needs
Exploring anaerobic hydrocarbon oxidation by DMRM could lead to several promising applications. For instance, many of the reactions involved in hydrocarbon oxidation have unusual chemistry that could be exploited for biotechnological purposes. Microbes capable of transferring electrons to solid metal oxides such as Geobacter spp. can also use a solid electrode as the TEA (Franks and Nevin 2010). This characteristic has conducted to the development of a bioremediation strategy where electrodes are buried in contaminated sediments to stimulate hydrocarbons degradation (Zhang et al. 2010; Morris and Jin 2012; Wang et al. 2012). Because electrodes are low-maintenance and can be installed permanently at polluted sites, electrobioremediation is a promising approach since it has the potential of being less expensive than competing technologies. Another possible application associated with DMRM, which usually generate magnetite from the Fe(III) oxide reduction, is the possibility of developing tools for the localization of petroleum deposit based on magnetic anomaly signals (Lovley et al. 2004).
Developing novel technologies related to hydrocarbons degradation with DMRM will require a better understanding of their metabolism. Although important progress has been made in the last 5 years, hydrocarbons degradation pathways in DMRM are still only partially characterized. Outstanding questions remaining include: (1) the identity of the enzymes responsible for benzene hydroxylation in G. metallireducens (Zhang et al. 2013) and benzene carboxylation in F. placidus (Holmes et al. 2011); (2) the nature of the electron transport route and energy conservation mechanism involved in benzoyl-CoA reductase, 2-naphthoyl-CoA reductase, and 5,6-dihydro-2-naphthoyl-CoA reductase activity (Boll et al. 2014; Estelmann et al. 2015); and (3) the nature in metal-reducing microbes of the polycyclic hydrocarbons degradation pathways described only in other phylogenetic classes of microbes until now. These examples are representing only a small fraction of the unexplored elements that will require extensive research work before achieving a complete portrait of the hydrocarbon degradation metabolism in metal-reducing microbes.
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Tremblay, PL., Zhang, T. (2020). Functional Genomics of Metal-Reducing Microbes Degrading Hydrocarbons. In: Boll, M. (eds) Anaerobic Utilization of Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50391-2_13
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