On the Enigma of Glutathione-Dependent Styrene Degradation in Gordonia rubripertincta CWB2

Abstract

Among bacteria, only a single styrene-specific degradation pathway has been reported so far. It comprises the activity of styrene monooxygenase, styrene oxide isomerase, and phenylacetaldehyde dehydrogenase, yielding phenylacetic acid as the central metabolite. The alternative route comprises ring-hydroxylating enzymes and yields vinyl catechol as central metabolite, which undergoes -cleavage. This was reported to be unspecific and also allows the degradation of benzene derivatives. However, some bacteria had been described to degrade styrene but do not employ one of those routes or only parts of them. Here, we describe a novel "hybrid" degradation pathway for styrene located on a plasmid of foreign origin. As putatively also unspecific, it allows metabolizing chemically analogous compounds (e.g., halogenated and/or alkylated styrene derivatives). CWB2 was isolated with styrene as the sole source of carbon and energy. It employs an assembled route of the styrene side-chain degradation and isoprene degradation pathways that also funnels into phenylacetic acid as the central metabolite. Metabolites, enzyme activity, genome, transcriptome, and proteome data reinforce this observation and allow us to understand this biotechnologically relevant pathway, which can be used for the production of ibuprofen. The degradation of xenobiotics by bacteria is not only important for bioremediation but also because the involved enzymes are potential catalysts in biotechnological applications. This study reveals a novel degradation pathway for the hazardous organic compound styrene in CWB2. This study provides an impressive illustration of horizontal gene transfer, which enables novel metabolic capabilities. This study presents glutathione-dependent styrene metabolization in an (actino-)bacterium. Further, the genomic background of the ability of strain CWB2 to produce ibuprofen is demonstrated.

Isoprene Oxidation by the Gram-Negative Model bacterium Variovorax sp. WS11

“…AD45, since IsoI detoxifies the epoxyisoprene produced from isoprene by IsoMO by producing a glutathione conjugate, 1-hydroxy-2-glutathionyl-2-methyl-3-butene (HGMB) [22][23][24]. The styrene oxidation pathway of the Gram-positive strain Gordonia rubripertincta CWB2 also involves glutathione [73]. In common with other Gram-negative bacteria, Variovorax spp.…”

Biodegradation of High Concentrations of Aliphatic Hydrocarbons in Soil from a Petroleum Refinery: Implications for Applicability of New Actinobacterial Strains

“…The actinobacteria Gordonia rubripertincta CWB2 and Rhodococcus erythropolis S43 used in Experiment B were isolated in Freiberg, Germany and partly characterized [10,19,[24][25][26]. Strain S43 was obtained from a former mining area heavily contaminated with heavy metals and arsenic, while strain CWB2 was isolated from plant potting soil using styrene as sole carbon source.…”

“…Seeking new resistant and metabolically active biodegrading strains capable of degrading of high concentrations of pollutants is important for successful application of bioremediation techniques. Techniques for improvement of biodegrading strains [10] (adaptation for higher toxicities, genetic engineering etc.) have been developed, however the major source of new strains remains their isolation from contaminated soils [9,[11][12][13].…”

“…Recently new actinobacterial strains applicable for bioremediation have been described or characterized, e.g., Gordonia sp. capable of biodegradation of phthalic esters [16], Gordonia polyisoprenivorans capable of cleavage of poly(cis-1,4-isoprene) [17], Gordonia rubripertincta CWB2 capable of biodegradation of styrene [10], or Gordonia phthalatica sp. capable of biodegradation of various phthalic esters [18].…”

“…to variants of periodic bioaugmentation and biostimulation. In a second experiment (Experiment B), we treated the soil with two recently isolated strains of actinobacteria, Gordonia rubripertincta CWB2 [10] and Rhodococcus erythropolis S43 [19]. As these strains are known producers of siderophores, we tested the hypothesis that iron bioavailability could influence the overall biodegradation performance of the strains used.…”