Wei Jia, Pengji Zhou, Zhang Jiajia, Peng Tangjian, Luo Jiayou, Yang Fei
Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha, Hunan 410078, China.
Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, School of Public Health, University of South China, Hengyang, Hunan 421001, China.
Water Res. 2023 Feb 1;229:119397. doi: 10.1016/j.watres.2022.119397. Epub 2022 Nov 20.
Microcystins (MCs) are harmful to the ecology and public health. Some bacteria can degrade MCs into Adda, but few can destroy Adda. Adda is the key bioactive moiety of MCs and mainly contributes to hepatotoxicity. We had previously isolated an indigenous novel bacterial strain named Sphingopyxis sp. YF1 that can efficiently degrade MCs and its key bioactive moiety Adda, but the mechanisms remained unknown. Here, the biodegradation mechanisms and pathways of Adda were systematically investigated using multi-omics analysis, mass spectrometry and heterologous expression. The transcriptomic and metabolomic profiles of strain YF1 during Adda degradation were revealed for the first time. Multi-omics analyses suggested that the fatty acid degradation pathway was enriched. Specifically, the expression of genes encoding aminotransferase, beta oxidation (β-oxidation) enzymes and phenylacetic acid (PAA) degradation enzymes were significantly up-regulated during Adda degradation. These enzymes were further proven to play important roles in the biodegradation of Adda. Simultaneously, some novel potential degradation products of Adda were identified successfully, including 7‑methoxy-4,6-dimethyl-8-phenyloca-2,4-dienoic acid (CHO), 2-methyl-3‑methoxy-4-phenylbutyric acid (CHO) and phenylacetic acid (PAA, CHO). In summary, the Adda was converted into PAA through aminotransferase and β-oxidation enzymes, then the PAA was further degraded by PAA degradation enzymes, and finally to CO via the tricarboxylic acid cycle. This study comprehensively elucidated the novel MC-LR biodegradation mechanisms, especially the new enzymatic pathway of Adda degradation. These findings provide a new perspective on the applications of microbes in the MCs polluted environment.
微囊藻毒素(MCs)对生态和公众健康有害。一些细菌能将MCs降解为Adda,但很少有细菌能破坏Adda。Adda是MCs的关键生物活性部分,主要导致肝毒性。我们之前分离出一种本土新菌株,名为鞘氨醇单胞菌属YF1,它能有效降解MCs及其关键生物活性部分Adda,但其机制仍不清楚。在此,利用多组学分析、质谱和异源表达系统地研究了Adda的生物降解机制和途径。首次揭示了菌株YF1在Adda降解过程中的转录组和代谢组图谱。多组学分析表明脂肪酸降解途径得到富集。具体而言,编码转氨酶、β氧化酶和苯乙酸(PAA)降解酶的基因表达在Adda降解过程中显著上调。这些酶被进一步证明在Adda的生物降解中发挥重要作用。同时,成功鉴定出一些Adda的新型潜在降解产物,包括7-甲氧基-4,6-二甲基-8-苯基辛酸-2,4-二烯酸(CHO)、2-甲基-3-甲氧基-4-苯基丁酸(CHO)和苯乙酸(PAA,CHO)。总之,Adda通过转氨酶和β氧化酶转化为PAA,然后PAA被PAA降解酶进一步降解,最终通过三羧酸循环转化为CO。本研究全面阐明了新型MC-LR生物降解机制,尤其是Adda降解的新酶促途径。这些发现为微生物在MCs污染环境中的应用提供了新的视角。