Physiological Role of the Previously Unexplained Benzenetriol Dioxygenase Homolog in the Burkholderia sp. Strain SJ98 4-Nitrophenol Catabolism Pathway
Liu, Juan1,2; Xu, Ying1,2; Deng, Shi-Kai1,2; Liu, Lei1,2; Min, Jun3; Shi, Ting1,2; Spain, Jim C.4; Zhou, Ning-Yi1,2
发表期刊APPLIED AND ENVIRONMENTAL MICROBIOLOGY
ISSN0099-2240
2021-07-01
卷号87期号:14页码:14
关键词4-nitrophenol 4-nitrocatechol 1,2,4-benzenetriol 1, 2-dioxygenase Burkholderia sp. strain SJ98
DOI10.1128/AEM.00007-21
通讯作者Xu, Ying(ying.xu@sju.edu.cn)
英文摘要4-Nitrophenol, a priority pollutant, is degraded by Gram-positive and Gramnegative bacteria via 1,2,4-benzenetriol (BT) and hydroquinone (HQ), respectively. All enzymes involved in the two pathways have been functionally identified. So far, all Gramnegative 4-nitrophenol utilizers are from the genera Pseudomonas and Burkholderia. But it remains a mystery why pnpG, an apparently superfluous BT 1,2-dioxygenase-encoding gene, always coexists in the catabolic cluster (pnpABCDEF) encoding 4-nitrophenol degradation via HQ. Here, the physiological role of pnpG in Burkholderia sp. strain SJ98 was investigated. Deletion and complementation experiments established that pnpG is essential for strain SJ98 growing on 4-nitrocatechol rather than 4-nitrophenol. During 4-nitrophenol degradation by strain SJ98 and its two variants (pnpG deletion and complementation strains), 1,4-benzoquinone and HQ were detected, but neither 4-nitrocatechol nor BT was observed. When the above-mentioned three strains (the wild type and complementation strains with 2,2'-dipyridyl) were incubated with 4-nitrocatechol, BT was the only intermediate detected. The results established the physiological role of pnpG that encodes BT degradation in vivo. Biotransformation analyses showed that the pnpA-deleted strain was unable to degrade both 4-nitrophenol and 4-nitrocatechol. Thus, the previously characterized 4-nitrophenol monooxygenase PnpA(SJ98) is also essential for the conversion of 4-nitrocatechol to BT. Among 775 available complete genomes for Pseudomonas and Burkhoideria, as many as 89 genomes were found to contain the putative pnpBCDEFG genes. The paucity of pnpA (3 in 775 genomes) implies that the extension of BT and HQ pathways enabling the degradation of 4-nitrophenol and 4-nitrocatechol is rarer, more recent, and likely due to the release of xenobiotic nitroaromatic compounds. IMPORTANCE An apparently superfluous gene (pnpG) encoding BT 1,2-dioxygenase is always found in the catabolic clusters involved in 4-nitrophenol degradation via HQ by Gram-negative bacteria. Our experiments reveal that pnpG is not essential for 4-nitrophenol degradation in Burkholderia sp. strain SJ98 but instead enables its degradation of 4-nitrocatechol via BT. The presence of pnpG genes broadens the range of growth substrates to include 4-nitrocatechol or BT, intermediates from the microbial degradation of many aromatic compounds in natural ecosystems. In addition, the existence of pnpCDEFG in 11.6% of the above-mentioned two genera suggests that the ability to degrade BT and HQ simultaneously is ancient. The extension of BT and HQ pathways including 4-nitrophenol degradation seems to be an adaptive evolution for responding to synthetic nitroaromatic compounds entering the environment since the industrial revolution.
资助机构National Key Research and Development Program of China ; National Natural Science Foundation of China ; SJTU JiRLMDS Joint Research Fund
收录类别SCI
语种英语
关键词[WOS]DEGRADATION GENE-CLUSTER ; P-NITROPHENOL ; METHYL PARATHION ; BIODEGRADATION ; BACTERIUM ; 4-NITROCATECHOL ; HYDROXYQUINOL ; OXIDATION ; PLASMIDS ; ISOLATE
研究领域[WOS]Biotechnology & Applied Microbiology ; Microbiology
WOS记录号WOS:000693249500001
引用统计
被引频次:1[WOS]   [WOS记录]     [WOS相关记录]
文献类型期刊论文
条目标识符http://ir.yic.ac.cn/handle/133337/29750
专题海岸带生物学与生物资源利用重点实验室_海岸带生物学与生物资源保护实验室
通讯作者Xu, Ying
作者单位1.Shanghai Jiao Tong Univ, Joint Int Res Lab Metab & Dev Sci, State Key Lab Microbial Metab, Shanghai, Peoples R China
2.Shanghai Jiao Tong Univ, Sch Life Sci & Biotechnol, Shanghai, Peoples R China
3.Chinese Acad Sci, Yantai Inst Coastal Zone Res, Key Lab Coastal Biol & Bioresource Utilizat, Yantai, Shandong, Peoples R China
4.Univ West Florida, Ctr Environm Diagnost & Bioremediat, Pensacola, FL USA
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Liu, Juan,Xu, Ying,Deng, Shi-Kai,et al. Physiological Role of the Previously Unexplained Benzenetriol Dioxygenase Homolog in the Burkholderia sp. Strain SJ98 4-Nitrophenol Catabolism Pathway[J]. APPLIED AND ENVIRONMENTAL MICROBIOLOGY,2021,87(14):14.
APA Liu, Juan.,Xu, Ying.,Deng, Shi-Kai.,Liu, Lei.,Min, Jun.,...&Zhou, Ning-Yi.(2021).Physiological Role of the Previously Unexplained Benzenetriol Dioxygenase Homolog in the Burkholderia sp. Strain SJ98 4-Nitrophenol Catabolism Pathway.APPLIED AND ENVIRONMENTAL MICROBIOLOGY,87(14),14.
MLA Liu, Juan,et al."Physiological Role of the Previously Unexplained Benzenetriol Dioxygenase Homolog in the Burkholderia sp. Strain SJ98 4-Nitrophenol Catabolism Pathway".APPLIED AND ENVIRONMENTAL MICROBIOLOGY 87.14(2021):14.
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