Deazaflavin metabolite produced by endosymbiotic bacteria controls fungal host reproduction

Ingrid Richter, Mahmudul Hasan, Johannes W Kramer, Philipp Wein, Jana Krabbe, K Philip Woitas, Timothy P Stinear, Sacha J Pidot, Florian Kloss, Christian Hertweck, Gerald Lackner
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Abstract

The endosymbiosis between the pathogenic fungus Rhizopus microsporus and the toxin-producing bacterium Mycetohabitans rhizoxinica represents a unique example of host control by an endosymbiont. Fungal sporulation strictly depends on the presence of endosymbionts as well as bacterially produced secondary metabolites. However, an influence of primary metabolites on host control remained unexplored. Recently, we discovered that M. rhizoxinica produces FO and 3PG-F420, a derivative of the specialized redox cofactor F420. Whether FO/3PG-F420 plays a role in the symbiosis has yet to be investigated. Here, we report that FO, the precursor of 3PG-F420, is essential to the establishment of a stable symbiosis. Bioinformatic analysis revealed that the genetic inventory to produce cofactor 3PG-F420 is conserved in the genomes of eight endofungal Mycetohabitans strains. By developing a CRISPR/Cas-assisted base editing strategy for M. rhizoxinica, we generated mutant strains deficient in 3PG-F420 (M. rhizoxinica ΔcofC) and in both FO and 3PG-F420 (M. rhizoxinica ΔfbiC). Co-culture experiments demonstrated that the sporulating phenotype of apo-symbiotic R. microsporus is maintained upon reinfection with wild-type M. rhizoxinica or M. rhizoxinica ΔcofC. In contrast, R. microsporus is unable to sporulate when co-cultivated with M. rhizoxinica ΔfbiC, even though the fungus was observed by super-resolution fluorescence microscopy to be successfully colonized. Genetic and chemical complementation of the FO deficiency of M. rhizoxinica ΔfbiC led to restoration of fungal sporulation, signifying that FO is indispensable for establishing a functional symbiosis. Even though FO is known for its light-harvesting properties, our data illustrate an important role of FO in inter-kingdom communication.
内共生细菌产生的脱氮黄素代谢物控制真菌宿主的繁殖
致病真菌根瘤菌(Rhizopus microsporus)与产毒细菌根瘤菌(Mycetohabitans rhizoxinica)之间的内共生关系是内共生体控制宿主的一个独特例子。真菌孢子的产生严格依赖于内生菌的存在以及细菌产生的次级代谢产物。然而,初级代谢物对宿主控制的影响仍未得到研究。最近,我们发现根瘤酵母菌能产生 FO 和 3PG-F420(一种特殊氧化还原辅助因子 F420 的衍生物)。FO/3PG-F420是否在共生中发挥作用还有待研究。在这里,我们报告了 3PG-F420 的前体 FO 对建立稳定的共生关系至关重要。生物信息学分析表明,产生辅助因子3PG-F420的基因库存在8个内真菌Mycetohabitans菌株的基因组中是保守的。通过开发一种 CRISPR/Cas 辅助的根肿菌碱基编辑策略,我们生成了缺乏 3PG-F420 的突变菌株(根肿菌 ΔcofC)和同时缺乏 FO 和 3PG-F420 的突变菌株(根肿菌 ΔfbiC)。共培养实验表明,在再感染野生型根瘤酵母菌或根瘤酵母菌 ΔcofC后,无共生型小孢子根瘤酵母菌的孢子表型得以保持。与此相反,小孢子根瘤菌与根瘤霉素 M. ΔfbiC共培养时不能产生孢子,尽管通过超分辨率荧光显微镜观察到真菌已成功定殖。对根瘤酵母菌 ΔfbiC 的 FO 缺乏进行遗传和化学互补后,真菌孢子繁殖得以恢复,这表明 FO 是建立功能性共生所不可或缺的。尽管 FO 因其采光特性而闻名,但我们的数据说明了 FO 在王国间交流中的重要作用。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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