Department of Microbiology, Key Laboratory of Microbiology for Agricultural Environment, Ministry of Agriculture, College of Life Sciences, Nanjing Agricultural University, Nanjing, China.
Key Laboratory of Agri-food Safety of Anhui Province, College of Resources and Environment, Anhui Agricultural University, Hefei, China.
Appl Environ Microbiol. 2021 May 11;87(11). doi: 10.1128/AEM.00170-21.
1-Naphthol, a widely used raw material for organic synthesis, is also a well-known organic pollutant. Due to its high toxicity, 1-naphthol is rarely used by microorganisms as the sole carbon source for growth. In this study, catabolism of 1-naphthol by sp. strain B2 was found to be greatly enhanced by additional supplementation with primary carbon sources (e.g., glucose, maltose, and sucrose), and 1-naphthol was even used as the carbon source for growth when strain B2 cells had been preinduced by both 1-naphthol and glucose. A distinct two-component flavin-dependent monooxygenase, NdcA1A2, was found to be responsible for the initial hydroxylation of 1-naphthol to 1,2-dihydroxynaphthalene, a more toxic compound. Transcriptional levels of genes were significantly upregulated when strain B2 cells were cultured with both 1-naphthol and glucose compared to cells cultured with only 1-naphthol or glucose. Two transcriptional regulators, the activator NdcS and the inhibitor NdcR, were found to play key roles in the synergistic regulation of the transcription of the 1-naphthol initial catabolism genes Cometabolism is a widely observed phenomenon, especially in the field of microbial catabolism of highly toxic xenobiotics. However, the mechanisms of cometabolism are ambiguous, and the roles of the obligately coexisting growth substrates remain largely unknown. In this study, we revealed that the roles of the coexisting primary carbon sources (e.g., glucose) in the enhanced catabolism of the toxic compound 1-naphthol in sp. strain B2 were not solely because they were used as growth substrates to support cell growth but, more importantly, because they acted as coinducers to interact with two transcriptional regulators, the activator NdcS and the inhibitor NdcR, to synergistically regulate the transcription of the 1-naphthol initial catabolism genes Our findings provide new insights into the cometabolic mechanism of highly toxic compounds in microorganisms.
1-萘酚是一种广泛用于有机合成的原料，也是一种众所周知的有机污染物。由于其高毒性，1-萘酚很少被微生物用作生长的唯一碳源。在这项研究中，发现 sp. 菌株 B2 对 1-萘酚的分解代谢可以通过额外补充初级碳源（如葡萄糖、麦芽糖和蔗糖）得到极大增强，并且当菌株 B2 细胞同时被 1-萘酚和葡萄糖预诱导时，1-萘酚甚至可以用作生长的碳源。发现一种独特的黄素依赖的双组分单加氧酶，NdcA1A2，负责 1-萘酚初始羟化生成更有毒的化合物 1,2-二羟基萘。与仅用 1-萘酚或葡萄糖培养的细胞相比，当菌株 B2 细胞同时用 1-萘酚和葡萄糖培养时， 基因的转录水平显著上调。发现两个转录调节因子，激活剂 NdcS 和抑制剂 NdcR，在协同调节 1-萘酚初始分解代谢基因的转录中发挥关键作用。共代谢是一种广泛观察到的现象，特别是在微生物对高毒性外来化合物的代谢中。然而，共代谢的机制尚不清楚，共存的必需生长底物的作用在很大程度上仍然未知。在这项研究中，我们揭示了共存的初级碳源（如葡萄糖）在增强 sp. 菌株 B2 中对有毒化合物 1-萘酚的分解代谢中的作用不仅是因为它们被用作生长底物来支持细胞生长，更重要的是，因为它们作为共诱导物与两个转录调节因子，激活剂 NdcS 和抑制剂 NdcR，相互作用以协同调节 1-萘酚初始分解代谢基因的转录。我们的发现为微生物中高毒性化合物的共代谢机制提供了新的见解。
