Department of Biology, Northeastern University, Boston, MA, 02115, USA.
Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, SP, 13400-970, Brazil.
NPJ Biofilms Microbiomes. 2023 Jul 19;9(1):50. doi: 10.1038/s41522-023-00418-z.
Pulcherrimin is an iron-binding reddish pigment produced by various bacterial and yeast species. In the soil bacterium Bacillus subtilis, this pigment is synthesized intracellularly as the colorless pulcherriminic acid by using two molecules of tRNA-charged leucine as the substrate; pulcherriminic acid molecules are then secreted and bind to ferric iron extracellularly to form the red-colored pigment pulcherrimin. The biological importance of pulcherrimin is not well understood. A previous study showed that secretion of pulcherrimin caused iron depletion in the surroundings and growth arrest on cells located at the edge of a B. subtilis colony biofilm. In this study, we identified that pulcherrimin is primarily produced under biofilm conditions and provides protection to cells in the biofilm against oxidative stress. We presented molecular evidence on how pulcherrimin lowers the level of reactive oxygen species (ROS) and alleviates oxidative stress and DNA damage caused by ROS accumulation in a mature biofilm. We also performed global transcriptome profiling to identify differentially expressed genes in the pulcherrimin-deficient mutant compared with the wild type, and further characterized the regulation of genes by pulcherrimin that are related to iron homeostasis, DNA damage response (DDR), and oxidative stress response. Based on our findings, we propose pulcherrimin as an important antioxidant that modulates B. subtilis biofilm development.
美丽菌素是一种由多种细菌和酵母产生的含铁红色素。在土壤细菌枯草芽孢杆菌中,这种色素作为无色的美丽菌素酸在细胞内合成,使用两个分子的负载亮氨酸的 tRNA 作为底物;然后将美丽菌素酸分子分泌到细胞外,并与三价铁结合形成红色的色素美丽菌素。美丽菌素的生物学意义尚不清楚。先前的研究表明,美丽菌素的分泌导致周围铁元素的消耗,并使位于枯草芽孢杆菌菌膜菌落边缘的细胞生长停滞。在这项研究中,我们确定美丽菌素主要在菌膜条件下产生,并为菌膜中的细胞提供针对氧化应激的保护。我们提供了分子证据,证明美丽菌素如何降低活性氧 (ROS) 的水平,并减轻成熟菌膜中 ROS 积累引起的氧化应激和 DNA 损伤。我们还进行了全转录组谱分析,以确定与铁稳态、DNA 损伤反应 (DDR) 和氧化应激反应相关的美丽菌素缺陷突变体与野生型之间差异表达的基因,并进一步表征了美丽菌素对这些基因的调控。基于我们的发现,我们提出美丽菌素作为一种重要的抗氧化剂,调节枯草芽孢杆菌菌膜的发育。