Wang Xu, Fu Changai, Chen Meng, Wu Yanan, Chen Yu, Chen Yan, Li Li
Shandong Provincial Key Laboratory of Water Pollution Control and Resource Reuse, School of Environmental Science and Engineering, Shandong University, 72 Binhai Road, Jimo, Qingdao, 266237, China.
Marine Genomics and Biotechnology Program, Institute of Marine Science and Technology, Shandong University, 72 Binhai Road, Jimo, Qingdao, 266237, China.
World J Microbiol Biotechnol. 2025 Jan 27;41(2):51. doi: 10.1007/s11274-025-04270-5.
Catabolic plasmids are critical factors in the degradation of recalcitrant xenobiotics, such as dioxins. Understanding the persistence and evolution of native catabolic plasmids is pivotal for controlling their function in microbial remediation. Here, we track the fitness and evolution of Rhodococcus sp. strain p52 harboring dioxin-catabolic plasmids under nonselective conditions without contaminant. Growth curve analysis and competition experiments demonstrated that pDF01 imposed fitness costs, whereas pDF02 conferred fitness benefits. During stability tests, pDF01 tended to be lost from the population, while pDF02 maintained at least one copy in the cell until proliferation of the 400th generation. Genome-wide gene expression profiling combined with codon usage bias analysis revealed that the high expression of pDF01 genes involved in dibenzofuran catabolism and regulation caused metabolic burdens. In contrast, potential cooperation between the pDF02-encoded short-chain dehydrogenase/reductase family oxidoreductase and the redox cofactor mycofactocin, which synthetic genes are located on the chromosome, may explain the benefit of pDF02. The fitness cost imposed by pDF01 was alleviated during adaptive evolution and was associated with the transcriptional downregulation of the dibenzofuran degradation genes on pDF01, and the global regulation of genome-wide gene expression involving basic metabolism, transport, and signal transduction. This study broadens our understandings on the persistence and evolution of dioxin-catabolic mega-plasmids, thus paving the way for the bioremediation of recalcitrant xenobiotic pollution in the environment.
分解代谢质粒是降解难降解的外源性物质（如二噁英）的关键因素。了解天然分解代谢质粒的持久性和进化对于控制其在微生物修复中的功能至关重要。在这里，我们追踪了携带二噁英分解代谢质粒的红球菌属菌株p52在无污染物的非选择性条件下的适应性和进化情况。生长曲线分析和竞争实验表明，pDF01带来了适应性成本，而pDF02赋予了适应性优势。在稳定性测试中，pDF01倾向于从群体中丢失，而pDF02在细胞中至少保持一个拷贝，直到第400代增殖。全基因组基因表达谱分析结合密码子使用偏好分析表明，参与二苯并呋喃分解代谢和调控相关的pDF01基因的高表达导致了代谢负担。相比之下，pDF02编码的短链脱氢酶/还原酶家族氧化还原酶与氧化还原辅因子真菌硫辛素之间的潜在合作（其合成基因位于染色体上），可能解释了pDF02的优势。pDF01带来的适应性成本在适应性进化过程中得到缓解，这与pDF01上二苯并呋喃降解基因的转录下调以及涉及基本代谢、转运和信号转导的全基因组基因表达的全局调控有关。这项研究拓宽了我们对二噁英分解代谢大质粒的持久性和进化的理解，从而为环境中难降解外源性物质污染的生物修复铺平了道路。
