Chlorate Reduction
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microorganisms Review Biotechnological Applications of Microbial (Per)chlorate Reduction Ouwei Wang 1,2 and John D. Coates 1,2,3,* 1 Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USA; [email protected] 2 Energy Biosciences Institute, University of California, Berkeley, CA 94704, USA 3 Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA * Correspondence: [email protected] Received: 5 October 2017; Accepted: 22 November 2017; Published: 24 November 2017 Abstract: While the microbial degradation of a chloroxyanion-based herbicide was first observed nearly ninety years ago, only recently have researchers elucidated the underlying mechanisms of perchlorate and chlorate [collectively, (per)chlorate] respiration. Although the obvious application of these metabolisms lies in the bioremediation and attenuation of (per)chlorate in contaminated environments, a diversity of alternative and innovative biotechnological applications has been proposed based on the unique metabolic abilities of dissimilatory (per)chlorate-reducing bacteria (DPRB). This is fueled in part by the unique ability of these organisms to generate molecular oxygen as a transient intermediate of the central pathway of (per)chlorate respiration. This ability, along with other novel aspects of the metabolism, have resulted in a wide and disparate range of potential biotechnological applications being proposed, including enzymatic perchlorate detection; gas gangrene therapy; enhanced xenobiotic bioremediation; oil reservoir bio-souring control; chemostat hygiene control; aeration enhancement in industrial bioreactors; and, biogenic oxygen production for planetary exploration. While previous reviews focus on the fundamental science of microbial (per)chlorate reduction (for example see Youngblut et al., 2016), here, we provide an overview of the emerging biotechnological applications of (per)chlorate respiration and the underlying organisms and enzymes to environmental and biotechnological industries. Keywords: perchlorate; chlorate; microbial perchlorate reduction; perchlorate bioremediation; bio-souring control; bioreactor hygiene controls; aeration enhancement 1. Introduction − − The oxyanions of chlorine, perchlorate (ClO4 ), and chlorate (ClO3 ), are highly soluble, strong oxidants that are deposited in the environment through both anthropogenic and natural processes [1–8]. Perchlorate is a common commodity chemical with a diverse range of industrial uses, ranging from pyrotechnics to lubricating oils [4], but it is predominantly used as an energetics booster or oxidant in solid rocket fuels by the munitions industry [4,9–11]. Although being a powerful oxidant, under most environmental conditions perchlorate is highly stable on account of the high energy of activation that is associated with its reduction [1,9]. Perchlorate is toxic to humans as it inhibits the uptake of iodine by the thyroid gland [12], disrupting the production of thyroid hormones, potentially leading to hypothyroidism [13,14]. For humans, oral ingestion is the primary source of perchlorate exposure as contamination is widespread in soil, fertilizers, and groundwater, allowing it to readily move into our food chain [15]. In contrast, chlorate is far more chemically reactive than perchlorate [16]. It is currently used to produce chlorine dioxide in bleaching and disinfection processes [17] and as a precursor for the Microorganisms 2017, 5, 76; doi:10.3390/microorganisms5040076 www.mdpi.com/journal/microorganisms Microorganisms 2017, 5, 76 2 of 16 manufactureMicroorganisms of 2017 perchlorate., 5, 76 Historically, it was widely used as the active component of herbicides2 of 16 during the early twentieth century [18,19]. Chlorate is also toxic to humans causing oxidative damage manufacture of perchlorate. Historically, it was widely used as the active component of herbicides to red blood cells, resulting in methemoglobin formation [20,21]. In both plant and microbial cells, during the early twentieth century [18,19]. Chlorate is also toxic to humans causing oxidative damage chlorate can be a substrate for respiratory or assimilatory nitrate reductases, which reduce it to chlorite to− red blood cells, resulting in methemoglobin formation [20,21]. In both plant and microbial cells, (ClO2chlorate)[22], can a compound be a substrate with for demonstrated respiratory or broad-spectrum assimilatory nitrate biocidal reductases, activity which against reduce Gram-negative it to and Gram-positivechlorite (ClO2−) [22], bacteria a compound [23–28 with], bacteriophages demonstrated broad- [29], fungispectrum [23 ],biocidal and algae activity [25 against]. Because Gram- of this, chloritenegative is often and used Gram-positive to treat freshwater bacteria [23–28], copepod bacteriophages parasites [ 30[29],], andfungi as [23], an activeand algae ingredient [25]. Because in topical woundof this, treatments. chlorite is often used to treat freshwater copepod parasites [30], and as an active ingredient in topicalIn the wound 1920’s, treatments. bacteria were discovered that used chlorate, (and presumably perchlorate, althoughIn this the is1920’s, not abacteria prerequisite were discovered [18]) as athat terminal used chlorate, electron (and acceptor presumably for anaerobic perchlorate, energy productionalthough [31 this]. Recentis not studiesa prerequisite have identified[18]) as a theterminal molecular electron mechanisms acceptor for underlying anaerobic thisenergy unique production [31]. Recent studies have identified the molecular mechanisms underlying this unique biochemistry (Figure1)[ 9,18,19]. Dissimilatory (per)chlorate reducing bacteria (DPRB) use a highly biochemistry (Figure 1) [9,18,19]. Dissimilatory (per)chlorate reducing bacteria (DPRB) use a highly conserved perchlorate reductase, PcrABC, to reduce perchlorate to chlorate and subsequently chlorite. conserved perchlorate reductase, PcrABC, to reduce perchlorate to chlorate and subsequently The chloritechlorite. Theis rapidly chlorite removedis rapidly byremoved another by another highly highly conserved conserved enzyme, enzyme, chlorite chlorite dismutase dismutase (Cld), − to produce(Cld), tomolecular produce molecular oxygen oxygen (O2) and(O2) and innocuous innocuous chloride chloride (Cl(Cl−) )[[9,18,19,32].9,18,19,32 The]. oxygen The oxygen that is that is producedproduced is is thenthen respiredrespired by the same same organi organism,sm, generally generally through through the theuse useof a ofhigh-affinity a high-affinity cytochromecytochromecbb3 cbb3-oxidase-oxidase [18 [18,19].,19]. Specialized Specialized dissimilatory chlorate-reducing chlorate-reducing bacteria bacteria (DCRB) (DCRB) respire respire onlyonly chlorate chlorate and and not not perchlorate perchlorate using using anan analogousanalogous pathway pathway involving involving chlorite chlorite and andCld, Cld,but thebut the chloratechlorate is initiallyis initially reduced reduced via via a a specializedspecialized chlorate reductase reductase (ClrABC), (ClrABC), a structurally a structurally and and evolutionarilyevolutionarily distinct distinct enzyme enzyme from from the the PcrABCPcrABC that that can can reduce reduce chlorate chlorate but butnot notperchlorate perchlorate [33–37]. [33 –37]. Owing to the unique ability to degrade (per)chlorate and generate molecular oxygen under anaerobic Owing to the unique ability to degrade (per)chlorate and generate molecular oxygen under anaerobic conditions, DPRB, perchlorate reductase, chlorate reductase, and chlorite dismutase provide conditions,innovative DPRB, solutions perchlorate to outstanding reductase, problems chlorate in reductase, current industrial and chlorite processes. dismutase In this provide review, innovative we solutionsprovide to an outstanding overview of problems the potential in current applications industrial of microbial processes. (per)chlorate In this review,reduction, we and provide the an overviewunderlying of the genes potential and enzymes. applications The taxonomy, of microbial evolution, (per)chlorate biochemistry, reduction, and physiology and the underlying of microbial genes and enzymes.(per)chlorate The reduction taxonomy, are beyond evolution, the scope biochemistry, of this review and physiologyand have been of microbialdescribed in (per)chlorate detail reductionelsewhere are beyond[18,19]. the scope of this review and have been described in detail elsewhere [18,19]. FigureFigure 1. A 1. schematicA schematic of of the the current model model for for the the bioc biochemicalhemical pathway pathway of perchlorate of perchlorate reduction. reduction. As As partpart ofof thisthis pathway,pathway, hypochloritehypochlorite (ClO (ClO−) −is) isinadvertently inadvertently produced produced at the at thechlorite chlorite dismutase. dismutase. PerchloratePerchlorate reducing reducing bacteria bacteria have have evolved evolved a detoxification a detoxification process process based based on on a methionine a methionine rich rich peptide peptide that chemically reacts with ClO− to produce methionine sulfoxide, which is subsequently re- that chemically reacts with ClO− to produce methionine sulfoxide, which is subsequently re-reduced by reduced by the methionine sulfoxide reductase (YedY) using reducing equivalents from the quinone the methionine sulfoxide reductase (YedY) using reducing equivalents from the quinone oxidoreductase oxidoreductase (YedZ). QH—quinone pool; Pcr—Perchlorate reductase;