Adaption and Degradation Strategies of Methylotrophic 1,4-Dioxane Degrading Strain Xanthobacter sp. YN2 Revealed by Transcriptome-Scale Analysis

Abstract

Biodegradation of 1,4-dioxane (dioxane) contamination has gained much attention for decades. In our previous work, we isolated a highly efficient dioxane degrader, Xanthobacter sp. YN2, but the underlying mechanisms of its extraordinary degradation performance remained unresolved. In this study, we performed a comparative transcriptome analysis of YN2 grown on dioxane and citrate to elucidate its genetic degradation mechanism and investigated the transcriptomes of different dioxane degradation stages (T0, T24, T48). We also analyzed the transcriptional response of YN2 over time during which the carbon source switched from citrate to dioxane. The results indicate that strain YN2 was a methylotroph, which provides YN2 a major advantage as a pollutant degrader. A large number of genes involved in dioxane metabolism were constitutively expressed prior to dioxane exposure. Multiple genes related to the catabolism of each intermediate were upregulated by treatment in response to dioxane. Glyoxylate metabolism was essential during dioxane degradation by YN2, and the key intermediate glyoxylate was metabolized through three routes: glyoxylate carboligase pathway, malate synthase pathway, and anaplerotic ethylmalonyl–CoA pathway. Genes related to quorum sensing and transporters were significantly upregulated during the early stages of degradation (T0, T24) prior to dioxane depletion, while the expression of genes encoding two-component systems was significantly increased at late degradation stages (T48) when total organic carbon in the culture was exhausted. This study is the first to report the participation of genes encoding glyoxalase, as well as methylotrophic genes xoxF and mox, in dioxane metabolism. The present study reveals multiple genetic and transcriptional strategies used by YN2 to rapidly increase biomass during growth on dioxane, achieve high degradation efficiency and tolerance, and adapt to dioxane exposure quickly, which provides useful information regarding the molecular basis for efficient dioxane biodegradation.

Harnessing Paenarthrobacter ureafaciens YL1 and Pseudomonas koreensis YL2 Interactions to Improve Degradation of Sulfamethoxazole

“…Biological treatment uses microbial interaction to remove SMX, which is currently the most promising processing method [ 10 ]. To overcome the persistent toxicity and the high environmental mobility of SMX, various removal technologies have been reported, including biological treatment [ 11 , 12 , 13 , 14 ], adsorption [ 15 , 16 ], advanced oxidation [ 17 , 18 , 19 , 20 ], and electrochemical oxidation [ 21 , 22 ].…”

Advances in Remediation Solutions: New Developments and Opportunities in 1,4‐Dioxane Biological Treatment

“…2016; Wang et al. 2021c). Because constitutive enzymes are present regardless of substrate concentrations, when the substrate is encountered, degradation can proceed without a lag period.…”

“…Microbial production of these enzymes often must be induced by the presence of one or more target sub-strates at sufficient concentrations. However, constitutive monooxygenase enzymes that degrade 1,4-dioxane have also been documented (Sei et al 2013a;Chen et al 2016;Wang et al 2021c). Because constitutive enzymes are present regardless of substrate concentrations, when the substrate is encountered, degradation can proceed without a lag period.…”

Biodegradation of Pollutants in the Environment: Omics Approaches

“…The use of genomics, tanscriptomics, proteomics, and metabolomics allows us to decipher the metabolic pathway and adaptations of bacteria in the presence of pollutants which allow them to tolerate and degrade the compounds. In the study of Wang et al [1], the analysis of the transcriptome of Xanthobacter sp. YN2, along with the degradation of 1,4-dioxane (compared with citrate), identified glycoxylate as a key intermediate, which was further metabolized by three routes.…”