State Key Laboratory of Agrobiotechnology, MOA Key Laboratory of Soil Microbiology, Rhizobium Research Center, College of Biological Sciences, China Agricultural University, Beijing, China.
State Key Laboratory of Agrobiotechnology, MOA Key Laboratory of Soil Microbiology, Rhizobium Research Center, College of Biological Sciences, China Agricultural University, Beijing, China
mBio. 2020 Feb 18;11(1):e03193-19. doi: 10.1128/mBio.03193-19.
Pathogenic bacteria need high-affinity zinc uptake systems to counteract the nutritional immunity exerted by infected hosts. However, our understanding of zinc homeostasis in mutualistic systems such as the rhizobium-legume symbiosis is limited. Here, we show that the conserved high-affinity zinc transporter ZnuABC and accessory transporter proteins (Zip1, Zip2, and c06450) made cumulative contributions to nodulation of the broad-host-range strain CCBAU45436. Zur acted as a zinc-dependent repressor for the operon, , and by binding to the associated Zur box, but did not regulate and ZnuABC was the major zinc transporter. Combined mutants lacking and one of the three accessory genes had more severe defects in nodulation and growth under zinc starvation conditions than the mutant, though rhizoplane colonization by these mutants was not impaired. In contrast to the elite strain CCBAU45436, more drastic symbiotic defects were observed for the mutants of other strains, which lack at least one of the three accessory genes in their genomes and are characterized by their limited host range and geographical distribution. The -derived mutants showed a higher expression level of genes involved in Nod factor biosynthesis and a reduced expression of genes encoding a type three secretion system and its effector NopP, which can interfere with the host immune system. Application of exogenous zinc restored the nodulation ability of these -derived mutants. Therefore, the conserved ZnuABC and accessory components in the zinc starvation machinery play an important role in modulating symbiotic compatibility. The rhizobium-legume symbiosis contributes around 65% of biological nitrogen fixation in agriculture systems and is critical for sustainable agriculture by reducing the amount of chemical nitrogen fertilizer being used. Rhizobial inocula have been commercialized for more than 100 years, but the efficiency of inoculation can vary among legume cultivars, field sites, and years. These long-lasting challenging problems impede the establishment of a sustainable agriculture, particularly in developing countries. Here, we report that rhizobial zinc starvation machinery containing a conserved high-affinity zinc transporter and accessory components makes cumulative contributions to modulating rhizobial symbiotic compatibility. This work highlights a critical role of largely unexplored nutritional immunity in the rhizobium-legume symbiosis, which makes zinc starvation machinery an attractive target for improving rhizobial symbiotic compatibility.
致病细菌需要高亲和力的锌摄取系统来抵抗受感染宿主施加的营养免疫。然而，我们对共生系统（如根瘤菌-豆科植物共生体）中的锌动态平衡的理解是有限的。在这里，我们表明保守的高亲和力锌转运体 ZnuABC 和辅助转运蛋白（Zip1、Zip2 和 c06450）对广泛宿主范围菌株 CCBAU45436 的结瘤做出了累积贡献。Zur 通过与相关 Zur 盒结合，作为锌依赖性的 操纵子、和的阻遏物，但不调节和。ZnuABC 是主要的锌转运体。与缺失和三个辅助基因之一的组合突变体相比，缺失和三个辅助基因之一的组合突变体在缺锌条件下的结瘤和生长缺陷更为严重，尽管这些突变体的根际定殖不受损害。与优良菌株 CCBAU45436 相比，其他菌株的突变体观察到更严重的共生缺陷，这些菌株的基因组中至少缺失三个辅助基因之一，其特征是宿主范围有限且地理分布有限。衍生自的突变体表现出参与 Nod 因子生物合成的基因的更高表达水平，以及编码 III 型分泌系统及其效应物 NopP 的基因的表达降低，NopP 可以干扰宿主免疫系统。外源锌的应用恢复了这些衍生自的突变体的结瘤能力。因此，在锌饥饿机制中保守的 ZnuABC 和辅助成分在调节共生相容性方面发挥着重要作用。根瘤菌-豆科植物共生体在农业系统中贡献了约 65%的生物固氮，并且通过减少使用化学氮肥的数量，对可持续农业至关重要。根瘤菌接种剂已经商业化了 100 多年，但接种效率在豆科作物品种、田间和年份之间可能有所不同。这些长期存在的挑战性问题阻碍了可持续农业的建立，特别是在发展中国家。在这里，我们报告称，包含保守的高亲和力锌转运体和辅助成分的根瘤菌锌饥饿机制对调节根瘤菌共生相容性做出了累积贡献。这项工作强调了营养免疫在根瘤菌-豆科植物共生体中起着至关重要的作用，这使得锌饥饿机制成为提高根瘤菌共生相容性的有吸引力的目标。
