Wang Peng, Cao Hai-Yan, Chen Xiu-Lan, Li Chun-Yang, Li Ping-Yi, Zhang Xi-Ying, Qin Qi-Long, Todd Jonathan D, Zhang Yu-Zhong
Marine Biotechnology Research Center, State Key Laboratory of Microbial Technology, School of Life Science, Shandong University, Jinan 250100, China.
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK.
Mol Microbiol. 2017 Sep;105(5):674-688. doi: 10.1111/mmi.13727. Epub 2017 Jul 7.
Dimethylsulfoniopropionate (DMSP) cleavage, yielding dimethyl sulfide (DMS) and acrylate, provides vital carbon sources to marine bacteria, is a key component of the global sulfur cycle and effects atmospheric chemistry and potentially climate. Acrylate and its metabolite acryloyl-CoA are toxic if allowed to accumulate within cells. Thus, organisms cleaving DMSP require effective systems for both the utilization and detoxification of acrylate. Here, we examine the mechanism of acrylate utilization and detoxification in Roseobacters. We propose propionate-CoA ligase (PrpE) and acryloyl-CoA reductase (AcuI) as the key enzymes involved and through structural and mutagenesis analyses, provide explanations of their catalytic mechanisms. In most cases, DMSP lyases and DMSP demethylases (DmdAs) have low substrate affinities, but AcuIs have very high substrate affinities, suggesting that an effective detoxification system for acylate catabolism exists in DMSP-catabolizing Roseobacters. This study provides insight on acrylate metabolism and detoxification and a possible explanation for the high K values that have been noted for some DMSP lyases. Since acrylate/acryloyl-CoA is probably produced by other metabolism, and AcuI and PrpE are conserved in many organisms across all domains of life, the detoxification system is likely relevant to many metabolic processes and environments beyond DMSP catabolism.
二甲基巯基丙酸内盐（DMSP）裂解产生二甲基硫醚（DMS）和丙烯酸酯，为海洋细菌提供重要碳源，是全球硫循环的关键组成部分，影响大气化学并可能影响气候。如果丙烯酸酯及其代谢物丙烯酰辅酶A在细胞内积累则具有毒性。因此，裂解DMSP的生物需要有效的系统来利用和解毒丙烯酸酯。在这里，我们研究了玫瑰杆菌中丙烯酸酯利用和解毒的机制。我们提出丙酸辅酶A连接酶（PrpE）和丙烯酰辅酶A还原酶（AcuI）是关键酶，并通过结构和诱变分析，对它们的催化机制进行了解释。在大多数情况下，DMSP裂解酶和DMSP去甲基酶（DmdAs）的底物亲和力较低，但AcuIs具有非常高的底物亲和力，这表明在分解代谢DMSP的玫瑰杆菌中存在一种有效的酰基分解代谢解毒系统。这项研究提供了对丙烯酸酯代谢和解毒的见解，并对一些DMSP裂解酶所观察到的高K值给出了可能的解释。由于丙烯酸酯/丙烯酰辅酶A可能由其他代谢产生，并且AcuI和PrpE在生命所有领域的许多生物体中都保守存在，因此该解毒系统可能与除DMSP分解代谢之外的许多代谢过程和环境相关。
