Time-course transcriptome analysis reveals the mechanisms of Burkholderia sp. adaptation to high phenol concentrations

Ma, Yankun; Li, Lijun; Awasthi, Mukesh Kumar; Tian, Hua; Lu, Mingli; Megharaj, Mallavarapu; Pan, Yuanjiang; He, Wenxiang

doi:10.1007/s00253-020-10672-2

Cited by 19 publications

(22 citation statements)

References 65 publications

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“…Burkholderia sp. BNS showed during phenol catabolism an increase in superoxide dismutase, DNA repair enzymes RecN and RadA, and chaperones Hsp15 and Hsp12 [ 47 ]. Fluoranthene catabolism induces expression of catalase and superoxide dismutase in Mycobacterium sp.…”

Section: Discussionmentioning

confidence: 99%

The OxyR and SoxR transcriptional regulators are involved in a broad oxidative stress response in Paraburkholderia xenovorans LB400

et al. 2022

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Background Aerobic metabolism generates reactive oxygen species that may cause critical harm to the cell. The aim of this study is the characterization of the stress responses in the model aromatic-degrading bacterium Paraburkholderia xenovorans LB400 to the oxidizing agents paraquat and H2O2. Methods Antioxidant genes were identified by bioinformatic methods in the genome of P. xenovorans LB400, and the phylogeny of its OxyR and SoxR transcriptional regulators were studied. Functionality of the transcriptional regulators from strain LB400 was assessed by complementation with LB400 SoxR of null mutant P. aeruginosa ΔsoxR, and the construction of P. xenovorans pIZoxyR that overexpresses OxyR. The effects of oxidizing agents on P. xenovorans were studied measuring bacterial susceptibility, survival and ROS formation after exposure to paraquat and H2O2. The effects of these oxidants on gene expression (qRT-PCR) and the proteome (LC–MS/MS) were quantified. Results P. xenovorans LB400 possesses a wide repertoire of genes for the antioxidant defense including the oxyR, ahpC, ahpF, kat, trxB, dpsA and gorA genes, whose orthologous genes are regulated by the transcriptional regulator OxyR in E. coli. The LB400 genome also harbors the soxR, fumC, acnA, sodB, fpr and fldX genes, whose orthologous genes are regulated by the transcriptional regulator SoxR in E. coli. The functionality of the LB400 soxR gene was confirmed by complementation of null mutant P. aeruginosa ΔsoxR. Growth, susceptibility, and ROS formation assays revealed that LB400 cells were more susceptible to paraquat than H2O2. Transcriptional analyses indicated the upregulation of the oxyR, ahpC1, katE and ohrB genes in LB400 cells after exposure to H2O2, whereas the oxyR, fumC, ahpC1, sodB1 and ohrB genes were induced in presence of paraquat. Proteome analysis revealed that paraquat induced the oxidative stress response proteins AhpCF and DpsA, the universal stress protein UspA and the RNA chaperone CspA. Both oxidizing agents induced the Ohr protein, which is involved in organic peroxide resistance. Notably, the overexpression of the LB400 oxyR gene in P. xenovorans significantly decreased the ROS formation and the susceptibility to paraquat, suggesting a broad OxyR-regulated antioxidant response. Conclusions This study showed that P. xenovorans LB400 possess a broad range oxidative stress response, which explain the high resistance of this strain to the oxidizing compounds paraquat and H2O2.

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Section: Discussionmentioning

confidence: 99%

The OxyR and SoxR transcriptional regulators are involved in a broad oxidative stress response in Paraburkholderia xenovorans LB400

et al. 2022

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“…Sun et al (2019) found Sphingobacteriales associated with aromatics degradation genes in phenol-degrading activated sludge bioreactors. Other Burkholderia species have also been found to degrade aromatics like phenol (Ma et al, 2020b), and Dokdonella has been associated with the degradation of paracetamol (Palma et al, 2018) and polycyclic aromatic hydrocarbons (Bacosa and Inoue, 2015).…”

Section: Organisms Associated With 3-ca Degradationmentioning

confidence: 99%

“…Metagenomic and metatranscriptomic analyses allow the examination of differential gene enrichment and transcription respectively, in complex microbial communities like activated sludge. Some researchers have used transcriptomics approaches to elucidate degradation pathways via gene transcription in aromatics degradation in pure culture experiments (Tam et al, 2006;Yan and Wu, 2017;Cauduro et al, 2020;Ma et al, 2020b).…”

Section: Introductionmentioning

confidence: 99%

“…Metagenomic and metatranscriptomic analyses allow the examination of gene abundance and expression, respectively, in complex microbial communities like activated sludge. Transcriptomics has been used to elucidate degradation pathways in the context of aromatics degradation in pure culture experiments (Tam et al, 2006; Yan and Wu, 2017; Cauduro et al, 2020; Ma et al, 2020b). Long-term metatranscriptomics sampling has also shown differential abundance and expression of genes related to aromatic-compound degradation in activated sludge bioreactors (Sato et al, 2019; Sun et al, 2019; Yu et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Metagenomics and Metatranscriptomics Suggest Pathways of 3-Chloroaniline Degradation in Wastewater Reactors

Seshan

Santillan

Constancias

et al. 2021

Preprint

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Biological wastewater treatment systems are often affected by major shifts in influent quality, including the input of various toxic chemicals. Yet the mechanisms underlying adaptation of activated sludge process performance when challenged with a sustained toxin input have not been studied in a controlled and replicated experiment. Three replicate bench-scale bioreactors were subjected to a chemical disturbance in the form of 3-chloroaniline (3-CA) input over 132 days, following an acclimation period of 58 days, while three control reactors received no 3-CA input. The nitrification process was initially affected by 3-CA input; yet all three treatment reactors evolved to biologically degrade 3-CA within three weeks of the experiment, resulting in partial nitrification recovery. 16S rRNA amplicon sequencing revealed that ammonia oxidizers were initially impacted by 3-CA, and a new ammonia oxidizing community emerged with the onset of 3-CA degradation. Combining process and microbial community data from amplicon sequencing with potential functions gleaned from assembled metagenomics and metatranscriptomics data, 3-CA degradation was shown to likely occur via a phenol monooxygenase followed by ortho-cleavage of the aromatic ring. The relative abundance of genera Gemmatimonas, Saprospiraceae OLB8 and Taibaiella correlated significantly with 3-CA degradation. This study demonstrated the impact of a sustained stress on the activated sludge community and wastewater treatment process and its subsequent recovery. Using a combination of techniques in a controlled and replicated experiment, we showed that microbial communities can evolve degradative capacity following a sustained xenobiotic input, specific functions like nitrification can fully or partially recover and targeted culture-independent approaches can be used to elucidate the mechanisms of adaptation.

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“…Phenol is a crucial raw organic material that is widely used in industrial production, pharmaceutical manufacturing, and petroleum refining ( Liu et al, 2020 ). However, the extensive use and discharge of phenol have major impacts on the ecological environment, as phenol is generally toxic to living organisms ( Ma Y. et al, 2020 ). Many physicochemical treatment techniques have been adopted to deal with phenol-contaminated water, including reverse osmosis, electrochemical oxidation, nanofiltration, ultraviolet radiation, ion exchange, adsorption, and immobilized enzymes.…”

Section: Introductionmentioning

confidence: 99%

Genomic Analysis and Stability Evaluation of the Phenol-Degrading Bacterium Acinetobacter sp. DW-1 During Water Treatment

Chen

Zhang

et al. 2021

Front. Microbiol.

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Phenol is a toxic organic molecule that is widely detected in the natural environment, even in drinking water sources. Biological methods were considered to be a good tool for phenol removal, especially microbial immobilized technology. However, research on the “seed” bacteria along with microbial community analysis in oligotrophic environment such as drinking water system has not been addressed. In this study, Acinetobacter sp. DW-1 with high phenol degradation ability had been isolated from a drinking water biofilter was used as seeded bacteria to treat phenol micro-polluted drinking water source. Meanwhile, the whole genome of strain DW-1 was sequenced using nanopore technology. The genomic analysis suggests that Acinetobacter sp. DW-1 could utilize phenol via the β-ketoadipate pathway, including the catechol and protocatechuate branches. Subsequently, a bio-enhanced polyhedral hollow polypropylene sphere (BEPHPS) filter was constructed to investigate the stability of the seeded bacteria during the water treatment process. The denatured gradient gel electrophoresis (DGGE) profile and the quantification of phenol hydroxylase gene results indicate that when the BEPHPS filter was operated for 56 days, Acinetobacter sp. was still a persistent and competitive bacterium in the treatment group. In addition, 16S rRNA gene amplicon sequencing results indicate that Acinetobacter sp., as well as Pseudomonas sp., Nitrospira sp., Rubrivivax sp. were the predominant bacteria in the treatment group, which were different from that in the CK group. This study provides a better understanding of the mechanisms of phenol degradation by Acinetobacter sp. DW-1 at the gene level, and provides new insights into the stability of seeded bacteria and its effects on microbial ecology during drinking water treatment.

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Time-course transcriptome analysis reveals the mechanisms of Burkholderia sp. adaptation to high phenol concentrations

Cited by 19 publications

References 65 publications

The OxyR and SoxR transcriptional regulators are involved in a broad oxidative stress response in Paraburkholderia xenovorans LB400

The OxyR and SoxR transcriptional regulators are involved in a broad oxidative stress response in Paraburkholderia xenovorans LB400

Metagenomics and Metatranscriptomics Suggest Pathways of 3-Chloroaniline Degradation in Wastewater Reactors

Genomic Analysis and Stability Evaluation of the Phenol-Degrading Bacterium Acinetobacter sp. DW-1 During Water Treatment

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