Biotechnological Potential of Rhodococcus Biodegradative Pathways Dockyu Kim1*, Ki Young Choi2, Miyoun Yoo3, Gerben J
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J. Microbiol. Biotechnol. (2018), 28(7), 1037–1051 https://doi.org/10.4014/jmb.1712.12017 Research Article Review jmb Biotechnological Potential of Rhodococcus Biodegradative Pathways Dockyu Kim1*, Ki Young Choi2, Miyoun Yoo3, Gerben J. Zylstra4, and Eungbin Kim5 1Division of Polar Life Sciences, Korea Polar Research Institute, Incheon 21990, Republic of Korea 2University College, Yonsei University, Incheon 21983, Republic of Korea 3Korea Research Institute of Chemical Technology, Daejeon 34114, Republic of Korea 4Department of Biochemistry and Microbiology, School of Environmental and Biological Sciences, Rutgers University, NJ 08901-8520, USA 5Department of Systems Biology, Yonsei University, Seoul 03722, Republic of Korea Received: December 8, 2017 Revised: March 26, 2018 The genus Rhodococcus is a phylogenetically and catabolically diverse group that has been Accepted: May 1, 2018 isolated from diverse environments, including polar and alpine regions, for its versatile ability First published online to degrade a wide variety of natural and synthetic organic compounds. Their metabolic May 8, 2018 capacity and diversity result from their diverse catabolic genes, which are believed to be *Corresponding author obtained through frequent recombination events mediated by large catabolic plasmids. Many Phone: +82-32-760-5525; rhodococci have been used commercially for the biodegradation of environmental pollutants Fax: +82-32-760-5509; E-mail: [email protected] and for the biocatalytic production of high-value chemicals from low-value materials. Recent studies of their physiology, metabolism, and genome have broadened our knowledge regarding pISSN 1017-7825, eISSN 1738-8872 the diverse biotechnological applications that exploit their catabolic enzymes and pathways. Copyright© 2018 by The Korean Society for Microbiology Keywords: Biodegradation, degradative pathway, catabolic enzyme, bacteria, Rhodococcus and Biotechnology Introduction According to this book, rhodococci are generally found to be harmless, and some are very attractive biotechnological The genus Rhodococcus is a phylogenetically and candidates, although there are rare pathogenic species such physiologically diverse bacterial group within nocardioform as R. equi and R. fascians that cause foal pneumonia and actinomycetes, which contain mycolic acid in their cell leafy gall disease in plants, respectively. The reasons for walls. Rhodococcus (family Nocardiaceae) belongs to the their value as promising biotechnological candidates for phylum Actinobacteria that includes two other well-known applications are as follows. The members of Rhodococcus families, Mycobacteriaceae and Corynebacteriaceae. show a remarkable ability to degrade and transform a wide Rhodococcus members are described as nonmotile and aerobic variety of natural organic and xenobiotic compounds via gram-positive bacteria that generally show pleomorphic diverse catabolic pathways. In addition to the capacity to morphology, depending on the species or growth metabolize a broad spectrum of chemical compounds, cell conditions, such as different growth substrates. They have tolerance to toxic substrates and solvents, a frequent lack of been isolated from a wide variety of sources, including soil, catabolite repression, the production of biosurfactants, and rocks, groundwater, marine sediments, animal feces, internal environmental persistence make them excellent candidates organs of insects, and healthy and diseased animals and for bioremediation and bioconversion. They also have the plants [1]. Recently, cold-adapted rhodococcal strains have potential to synthesize useful products such as valuable been isolated from naturally cold environments, such as chemical synthons, amides, and polymers [1, 5]. alpine areas, the Arctic, and the Antarctic [2-4]. The metabolic versatility of Rhodococcus has been After approximately a decade since the first comprehensive extensively studied in microbial biotechnology fields account of the genus Rhodococcus in 1998 (see the special worldwide. Presently, there are over 1,800 and over 3,200 issue of Antonie Van Leeuwenhoek, volume 74), an excellent patents retrieved by even a quick search on Google’s patent book was published that described the biology of Rhodococcus. search engine using “rhodococcus biodegradation” and July 2018 ⎪ Vol. 28⎪ No. 7 1038 Kim et al. “rhodococcus biocatalysis,” respectively, as keywords. Several range of metabolic capabilities and degrade a wide variety review papers have also described the biotechnological of natural organic and xenobiotic compounds, including potential of rhodococci cells and their biodegradative aliphatic, aromatic (halogenated and nitro-substituted), enzymes for pollutant removal in environmental biotechnology heterocyclic, and polycyclic aromatic compounds [1], and for biocatalysis in pharmaceutical and chemical alicyclic hydrocarbons [8], nitriles [5], cholesterol [9], and industries [6, 7]. The biodegradation and biocatalysis lignins [10]. The wide range of substrates metabolized by activities are linked by biotransformation reactions and rhodococci suggests that members of this genus are enzymes that catalyze the reactions. In this review, we comparable to pseudomonads in their biotechnological will briefly summarize the current knowledge on the applications. The biodegradative pathways in rhodococci biodegradative pathways of Rhodococcus, including a brief generally consist of many peripheral (upper) pathways and collation of selected genomic data. We will then describe a few central (lower) pathways. For example, in the case of examples and strategies for utilizing the real and potential aromatic hydrocarbons, a wide range of monooxygenases value of biodegradative rhodococci. and dioxygenases in the peripheral pathways initiate the oxidative attack of the aromatic ring, producing central Rhodococci as Superb Degraders intermediates such as catechol, protocatechuate, and gentisate, which are further degraded by the ortho-, meta-, As summarized in Table 1, rhodococci display a diverse or modified 3-oxoadipate routes to intermediates of the Table 1. Members of the genus Rhodococcus that possess biocatalytic enzymes and/or biodegradative pathways for representative organic compounds. Reference Isolation Degradation Application Strain name Key pathway or enzyme for source substrate field isolation R. rhodochrous Soil sample Benzonitrile Production of Nitrile hydratase [72] J1 acrylamide (H_NHase α and β subunits) R. opacus 1CP Contaminated soil 4-Chlorophenol, Remediation of Modified ortho-cleavage [73] in Moscow, Russia 2,4-dichlorophenol (chloro)aromatics pathway for chlorocatechols R. rhodochrous Soil sample Propionitrile Production of Nitrile hydratase [74] PA-34 acrylamide (H_NHase α and β subunits) R. erythropolis Dry wood termites, Biphenyl Remediation of Biphenyl-degrading genes [75] TA421 Japan organic pollutants (bph) R. erythropolis Trichloroethene- and Isopropylbenzene Remediation of Isopropylbenzene- [12] BD2 toluene-contaminated soil trichloroethene degrading genes (ipb) Rhodococcus sp. Air-dried soil from an Acetonitrile, Remediation of Nitrile hydratase and [76] AJ270 industrial site, UK heteroaromatic acrylonitrile amidase nitriles R. jostii RHA1 Hexachlorocyclohexane- Polychlorinated Remediation of Biphenyl- and ethylbenzene- [77] contaminated soil, biphenyl, organic pollutants; degrading genes (bph and etb); Japan alkylbenzenes vanillin production dye-decolorizing peroxidase (dypB) Rhodococcus sp. Plant-amended soil Biphenyl, Remediation of Biphenyl-degrading genes [78] T104 terpenes polychlorinated (bph) biphenyls Rhodococcus sp. Oil-contaminated soil, Toluene Production of Toluene dioxygenase [79] B-264-1 USA cis-(1S,2R)-indandiol (todC1C2BA) Rhodococcus sp. Terra Nova Bay, n-Alkanes, Low-temperature n-Alkane-degrading and [80] strain Antarctica biphenyl remediation biosurfactant-producing genes R. opacus Topsoil in Hilversum, Toluene Production of Limonene-6-hydroxylase [53] PWD4 The Netherlands trans-carveol J. Microbiol. Biotechnol. Biotechnological Potential of Genus Rhodococcus 1039 Table 1. Continued. Reference Isolation Degradation Application Strain name Key pathway or enzyme for source substrate field isolation Rhodococcus Crude oil-contaminated Alkylbenzenes, Production of o-Xylene dioxygenase [81] sp. DK17 soil, Korea phthalates, cis-dihydrodiols and (akbA1A2A3) and cis-dihydrodiol bicyclics catechols dehydrogenase (akbB) Rhodococcus Petroleum hydrocarbon- Hexadecane, Low-temperature Phenol-degrading genes [82] sp. NO14-1 contaminated alpine soil, phenol remediation of Austria phenol R. opacus B4 Soil in Hiroshima, Japan Benzene, Remediation of Benzene dioxygenase (bnzA1A2)[83] aromatic/aliphatic benzene R. erythropolis Deep sea of the Pacific Alkanes Remediation of Alkane-degrading genes (alk)[84] PR4 Ocean alkanes R. erythropolis Soil surrounding hop β-Myrcene Production of Unknown enzymatic mechanism [54] MLT1 plants geraniol R. ruber TH Nitrile-contaminated soil Acrylonitrile Production of Nitrilase [85] ammonium acrylate R. ruber Petroleum-contaminated Acetonitrile Production of acrylic Nitrilase [42] AKSH-84 sludge, India acid Rhodococcus Petroleum hydrocarbon- n-Hexadecane, Low-temperature n-Alkane-degrading and [86] spp. strains contaminated North diesel remediation biosurfactant-producing genes Atlantic Canada R. erythropolis Soil Cholesterol, Production of Cholesterol oxidase Unknown ATCC 25544 aromatic cholestenone compounds citric acid cycle. pathway multiplicities, different