Microorganisms Involved in Anaerobic Benzene Degradation
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Ann Microbiol (2015) 65:1201–1213 DOI 10.1007/s13213-014-0926-8 REVIEW ARTICLE Microorganisms involved in anaerobic benzene degradation Arturo Aburto-Medina & Andrew S. Ball Received: 17 March 2014 /Accepted: 29 May 2014 /Published online: 26 June 2014 # Springer-Verlag Berlin Heidelberg and the University of Milan 2014 Abstract Benzene is a highly toxic compound. Moreover, Keywords Benzene . Benzene-contaminated groundwater . benzene-contaminated groundwater is a widespread problem Benzene-degrading microorganisms . Syntrophic interactions caused mainly by the lack of oxygen in the subsurface. Long- term exposure may cause leukaemia. However, pure cultures of microorganisms with the ability to degrade benzene anaer- Introduction obically have recently been isolated from novel enrichment cultures. The novel pure cultures include the hyperthermo- Benzene is derived from fossil fuels, cigarette smoke and philic archaeon Ferroglobus placidus and the Geobacter forest fires, among other sources. It is an important raw strains Ben and metallireducens which degrade benzene an- chemical used as an intermediate to produce a wide range of aerobically coupled to the reduction of Fe(III). Syntrophic products, such as plastics, resins, nylon, lubricants and pesti- interactions have been suggested in enrichments where mem- cides. Benzene is also highly toxic; it may cause acute mye- bers of the Peptococcaceae within the class Clostridia are the loid leukaemia, secondary aplastic anaemia and damage to the dominant organisms and suggested as being responsible for reproductive system. It can enter the body by skin contact, the first attack on the benzene ring. Laboratory enrichment inhalation or consumption of contaminated water. Benzene- studies have also resulted in the development of consortia contaminated groundwater is a widespread problem caused which degrade benzene, with different terminal electron ac- partially by its high solubility in water (1.8 g l−1 at 25°C) ceptors supporting the syntrophy. Other benzene-degrading relative to other organic compounds and partly to spills at microorganisms have been identified under methanogenic production sites and leaks in underground storage tanks. The- conditions, involving the reduction of humic acids by, for se leaks have been documented by studies of the environment example, the deltaproteobacterium Hasda-A and members of agencies in the USA and UK (Rudolph 1996;Atlas2005). the Betaproteobacteria, Gammaproteobacteria and Benzene is readily degraded under aerobic conditions Deltaproteobacteria, respectively. This review focuses on (Alvarez and Vogel 1991; Werlen et al. 1996; Fairlee et al. the microorganisms involved in anaerobic benzene degrada- 1997; Greene et al. 2000) by ubiquitous microorganisms, such tion under conditions involving several electron acceptors in as Pseudomonas sp. and Rhodococcus sp. (Fahy et al. 2006). recent years. Information related to the anaerobic degradation However contaminated groundwater is usually under anaero- of benzene is critical to understanding and predicting the fate bic conditions due to the rapid depletion of available oxygen of this contaminant in groundwater. in subterranean environments, which in turn decreases the redox potential, favouring the growth of denitrifying, sulphate-reducing, iron-reducing and methanogenic popula- * A. Aburto-Medina ( ) tions that may also degrade the contaminant. Therefore, in- Department of Environmental Sciences, Universidad Autónoma Metropolitana, Lerma 52006, Mexico formed knowledge of anaerobic microorganisms capable of e-mail: [email protected] benzene degradation is critical to understanding and predicting the fate of this contaminant. A. S. Ball Initial studies suggested the lack of benzene degradation School of Applied Sciences, Centre for Environment, Sustainability and Remediation, Royal Melbourne Institute of Technology, under anaerobic conditions (Barker et al. 1987;Kuhnetal. Bundoora, VIC 3083, Australia 1988; Acton and Barker 1992; Barbaro et al. 1992; Patterson 1202 Ann Microbiol (2015) 65:1201–1213 et al. 1993). However, laboratory-based and field studies in 2001). However, no anaerobic degradation genes were found the last 20 years have confirmed the degradation of this in the Dechloromonas aromatica RCB genome (Salinero et al. pollutant coupled to the reduction of nitrate (Burland and 2009), and subsequent data suggests the involvement of oxy- Edwards 1999;Coatesetal.2001; Chakraborty and Coates gen under nitrate-reducing conditions (Ettwig et al. 2010; 2005; Ulrich et al. 2005; Kasai et al. 2006;Jakoncicetal. Zhang et al. 2013). Nevertheless, recent studies have reported 2007), sulphate (Lovley et al. 1995; Phelps et al. 1996; Weiner the novel pure cultures archaeon Ferroglobus placidus and Lovley 1998a; Sublette et al. 2006; Musat and Widdel (Holmes et al. 2011)andaGeobacter metallireducens strain 2008; Berlendis et al. 2010), iron (Lovley and Woodward named Ben (Zhang et al. 2012), both of which are capable of 1996;Kazumietal.1997; Rooney-Varga et al. 1999;Jahn anaerobic benzene degradation. The hyperthermophilic et al. 2005; Kunapuli et al. 2007), manganese (Villatoro- archaeon F. placidus is able to degrade benzene anaerobically Monzón et al. 2003, 2008), humic acids (Cervantes et al. under iron-reducing conditions, producing benzoate as the 2011) and methanogenesis (Vogel and Grbicgalic 1986; main metabolite, suggesting the carboxylation of benzene to Grbicgalic and Vogel 1987;Kazumietal.1997; Weiner and form benzoate (Holmes et al. 2011). The Geobacter strain Lovley 1998b; Caldwell and Suflita 2000;Ulrichand Ben, isolated from sediments within the ferric ion [Fe(III)]- Edwards 2003; Chang et al. 2005; Da Silva and Alvarez reducing zone in a petroleum-contaminated aquifer in 2007; Sakai et al. 2009). Bemidji, USA, was found to degrade benzene with ferric iron Moreover, recent studies on the novel pure cultures of and anthraquinone-2,6-disulfonate (AQDS) as the only elec- Geobacter species and the archaeon Ferroglobus placidus tron acceptors. In addition, G. metallireducens is also able to have confirmed the degradation of benzene coupled to iron- degrade benzene coupled to the reduction of Fe(III); trace reducing conditions and have also provided information on amounts of phenol were detected during the degradation of the metabolites produced during growth on benzene (Holmes benzene, suggesting phenol as an intermediate. This finding is et al. 2011; Zhang et al. 2012). In addition, syntrophic asso- also supported by the inhibition of benzene degradation by the ciations are also suggested in enrichments capable of benzene deletion of genes involved in the metabolism of phenol and by degradation where members of the Peptococcaceae are the their upregulation during benzene oxidation (Zhang et al. key players (Taubert et al. 2012; van der Zaan et al. 2012). 2012; Zhang et al. 2013). Other microorganisms involved in the degradation of benzene under methanogenic conditions or coupled to the reduction of humic acids include the deltaproteobacterium Hasda-A and Microorganisms identified in recent anaerobic benzene two phylotypes of Gammaproteobacteria, respectively degradation studies (Cervantes et al. 2011;Masumotoetal.2012). In this review, we focus on the microorganisms which have been identified in Genera of the family Peptococcaceae (phylum anaerobic benzene degradation studies in recent years and the Firmicutes,classClostridia) have been identified as the possible terminal electron acceptors. It should be noted that main benzene degraders with most of the terminal elec- excellent reviews on the anaerobic degradation of hydrocar- tron acceptors [sulphate, nitrate, Fe(III), chlorate], and bons (Boll et al. 2002; Foght 2008; Fuchs et al. 2011; syntrophic interactions are strongly suggested. The most Meckenstock and Mouttaki 2011;Flanaganetal.2013; recent study by the Vogt group involved a sulphate- Heider and Schühle 2013;Bolletal.2014), anaerobic micro- reducing enrichment analysed by the protein-SIP tech- bial communities in hydrocarbon-contaminated aquifers nique, with their observations indicating syntrophy be- (Kleinsteuber et al. 2012), the use of stable isotope probing tween a benzene-fermenting clostridial group, a (SIP) to identify anaerobic benzene and toluene degraders sulphate-reducing deltaproteobacterial group that uses (Cupples 2011) and the degradation of benzene under anaer- the metabolites generated during benzene fermentation obic conditions (Lovley 2000; Coates et al. 2002; Weelink and a putative scavenger group from Bacteroidetes/ et al. 2010;Vogtetal.2011) have been published during the Chlorobi (Taubert et al. 2012). This result is consistent past 12 years. with that of a previous study on the same consortium where acetate and hydrogen were strongly suggested as intermediate metabolites in the anaerobic benzene degra- Pure cultures capable of anaerobic benzene degradation dation process (Rakoczy et al. 2011). Members of the Cryptanaerobacter/Pelotomaculum group are suggested Until a few years ago there were only a few pure cultures able to be the benzene-fermenting group, as has been indicated to degrade benzene anaerobically, and all of these were in other studies from the same group (Kleinsteuber et al. coupled to nitrate reduction: an Azoarcus strain DN11 and 2008;Herrmannetal.2010). Moreover, the syntrophic AN9 (Kasai et al. 2006), a Bacillus cereus strain (Dou et al. interactions and the presence of the Peptococcaceae mem- 2010)andDechloromonas strains JJ and