College of Engineering, Peking University, 100871, Beijing, China.
Institute of Ocean Research, Peking University, 100871, Beijing, China.
ISME J. 2021 Feb;15(2):605-617. doi: 10.1038/s41396-020-00800-1. Epub 2020 Oct 9.
Microbes spontaneously release membrane vesicles (MVs), which play roles in nutrient acquisition and microbial interactions. Iron is indispensable for microbes, but is a difficult nutrient to acquire. However, whether MVs are also responsible for efficient iron uptake and therefore involved in microbial interaction remains to be elucidated. Here, we used a Gram-positive strain, Dietzia sp. DQ12-45-1b, to analyze the function of its MVs in heme-iron recycling and sharing between species. We determined the structure and constituent of MVs and showed that DQ12-45-1b releases MVs originating from the mycomembrane. When comparing proteomes of MVs between iron-limiting and iron-rich conditions, we found that under iron-limiting conditions, heme-binding proteins are enriched. Next, we proved that MVs participate in extracellular heme capture and transport, especially in heme recycling from environmental hemoproteins. Finally, we found that the heme carried in MVs is utilized by multiple species, and we further verified that membrane fusion efficiency and species evolutionary distance determine heme delivery. Together, our findings strongly suggest that MVs act as a newly identified pathway for heme recycling, and represent a public good shared between phylogenetically closely related species.
微生物会自发释放膜泡（MVs），这些膜泡在养分获取和微生物相互作用中发挥作用。铁对于微生物是不可或缺的，但却是一种难以获取的养分。然而，MVs 是否也负责高效的铁摄取，从而参与微生物相互作用，这仍有待阐明。在这里，我们使用革兰氏阳性菌株 Dietzia sp. DQ12-45-1b 来分析其 MVs 在血红素铁回收和物种间共享中的功能。我们确定了 MVs 的结构和组成，并表明 DQ12-45-1b 释放源自菌膜的 MVs。当比较铁限制和铁丰富条件下 MVs 的蛋白质组时，我们发现铁限制条件下，血红素结合蛋白富集。接下来，我们证明 MVs 参与细胞外血红素的捕获和运输，特别是从环境血红素蛋白中进行血红素的回收。最后，我们发现 MVs 携带的血红素被多种物种利用，并且我们进一步验证了膜融合效率和物种进化距离决定血红素的传递。总之，我们的研究结果强烈表明，MVs 是血红素回收的新途径，代表了亲缘关系密切的物种之间共享的公共利益。
