State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China; State Key Laboratory of Genetic Engineering, Center for Evolutionary Biology, Human Phenome Institute, Zhangjiang Fudan International Innovation Center, School of Life Science, Fudan University, Shanghai 200438, China.
State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China.
Mol Phylogenet Evol. 2024 Dec;201:108208. doi: 10.1016/j.ympev.2024.108208. Epub 2024 Sep 27.
Sulfate is the second most common nonmetallic ion in modern oceans, as its concentration dramatically increased alongside tectonic activity and atmospheric oxidation in the Proterozoic. Microbial sulfate/sulfite metabolism, involving organic carbon or hydrogen oxidation, is linked to sulfur and carbon biogeochemical cycles. However, the coevolution of microbial sulfate/sulfite metabolism and Earth's history remains unclear. Here, we conducted a comprehensive phylogenetic analysis to explore the evolutionary history of the dissimilatory sulfite reduction (Dsr) pathway. The phylogenies of the Dsr-related genes presented similar branching patterns but also some incongruencies, indicating the complex origin and evolution of Dsr. Among these genes, dsrAB is the hallmark of sulfur-metabolizing prokaryotes. Our detailed analyses suggested that the evolution of dsrAB was shaped by vertical inheritance and multiple horizontal gene transfer events and that selection pressure varied across distinct lineages. Dated phylogenetic trees indicated that key evolutionary events of dissimilatory sulfur-metabolizing prokaryotes were related to the Great Oxygenation Event (2.4-2.0 Ga) and several geological events in the "Boring Billion" (1.8-0.8 Ga), including the fragmentation of the Columbia supercontinent (approximately 1.6 Ga), the rapid increase in marine sulfate (1.3-1.2 Ga), and the Neoproterozoic glaciation event (approximately 1.0 Ga). We also proposed that the voluminous iron formations (approximately 1.88 Ga) might have induced the metabolic innovation of iron reduction. In summary, our study provides new insights into Dsr evolution and a systematic view of the coevolution of dissimilatory sulfur-metabolizing prokaryotes and the Earth's environment.
硫酸盐是现代海洋中第二常见的非金属离子，其浓度随着元古代构造活动和大气氧化作用的增强而显著增加。涉及有机碳或氢氧化的微生物硫酸盐/亚硫酸盐代谢与硫和碳的生物地球化学循环有关。然而，微生物硫酸盐/亚硫酸盐代谢与地球历史的共同进化仍然不清楚。在这里，我们进行了全面的系统发育分析，以探索异化亚硫酸盐还原（Dsr）途径的进化历史。Dsr 相关基因的系统发育呈现出相似的分支模式，但也存在一些不一致，表明 Dsr 的起源和进化复杂。在这些基因中，dsrAB 是硫代谢原核生物的标志。我们的详细分析表明，dsrAB 的进化受到垂直遗传和多次水平基因转移事件的影响，并且不同谱系的选择压力不同。有时间的系统发育树表明，异化硫代谢原核生物的关键进化事件与大氧化事件（2.4-2.0 亿年前）和“无聊十亿年”（1.8-0.8 亿年前）中的几个地质事件有关，包括哥伦比亚超大陆的分裂（约 1.6 亿年前）、海洋硫酸盐的快速增加（1.3-1.2 亿年前）和新元古代冰期事件（约 1.0 亿年前）。我们还提出，大量的铁建造（约 1.88 亿年前）可能导致了铁还原代谢的创新。总之，我们的研究为 Dsr 进化提供了新的见解，并为异化硫代谢原核生物与地球环境的共同进化提供了系统的观点。
