Friedrich Loeffler Institute of Medical Microbiology, University Medicine Greifswald, Greifswald, Germany.
SYNMIKRO Research Center and Department of Chemistry, Philipps-University Marburg, Marburg, Germany.
PLoS Pathog. 2021 May 28;17(5):e1009604. doi: 10.1371/journal.ppat.1009604. eCollection 2021 May.
Burkholderia pseudomallei, the etiological agent of melioidosis in humans and animals, often occupies environmental niches and infection sites characterized by limited concentrations of oxygen. Versatile genomic features enable this pathogen to maintain its physiology and virulence under hypoxia, but the crucial regulatory networks employed to switch from oxygen dependent respiration to alternative terminal electron acceptors (TEA) like nitrate, remains poorly understood. Here, we combined a Tn5 transposon mutagenesis screen and an anaerobic growth screen to identify a two-component signal transduction system with homology to RegAB. We show that RegAB is not only essential for anaerobic growth, but also for full virulence in cell lines and a mouse infection model. Further investigations of the RegAB regulon, using a global transcriptomic approach, identified 20 additional regulators under transcriptional control of RegAB, indicating a superordinate role of RegAB in the B. pseudomallei anaerobiosis regulatory network. Of the 20 identified regulators, NarX/L and a FNR homolog were selected for further analyses and a role in adaptation to anaerobic conditions was demonstrated. Growth experiments identified nitrate and intermediates of the denitrification process as the likely signal activateing RegAB, NarX/L, and probably of the downstream regulators Dnr or NsrR homologs. While deletions of individual genes involved in the denitrification process demonstrated their important role in anaerobic fitness, they showed no effect on virulence. This further highlights the central role of RegAB as the master regulator of anaerobic metabolism in B. pseudomallei and that the complete RegAB-mediated response is required to achieve full virulence. In summary, our analysis of the RegAB-dependent modulon and its interconnected regulons revealed a key role for RegAB of B. pseudomallei in the coordination of the response to hypoxic conditions and virulence, in the environment and the host.
类鼻疽伯克霍尔德菌是人类和动物类鼻疽病的病原体,常存在于氧气浓度有限的环境小生境和感染部位。多样的基因组特征使该病原体能够在低氧条件下维持其生理机能和毒力,但对于从依赖氧的呼吸切换到替代末端电子受体(TEA),如硝酸盐的关键调控网络仍知之甚少。在这里,我们结合 Tn5 转座子诱变筛选和厌氧生长筛选,鉴定了一个与 RegAB 同源的双组分信号转导系统。我们发现 RegAB 不仅对厌氧生长是必需的,而且对细胞系和小鼠感染模型中的完全毒力也是必需的。使用全局转录组学方法进一步研究 RegAB 调控子,发现了 20 个额外的受 RegAB 转录调控的调控因子,这表明 RegAB 在 B. pseudomallei 厌氧调节网络中具有主导作用。在所鉴定的 20 个调控因子中,NarX/L 和一个 FNR 同源物被选择进行进一步分析,并证明了它们在适应厌氧条件中的作用。生长实验确定硝酸盐和反硝化过程的中间产物是激活 RegAB、NarX/L,可能还有下游调控因子 Dnr 或 NsrR 同源物的信号。虽然参与反硝化过程的单个基因的缺失表明它们在厌氧适应性方面的重要作用,但它们对毒力没有影响。这进一步强调了 RegAB 作为 B. pseudomallei 厌氧代谢的主要调控因子的核心作用,并且需要完整的 RegAB 介导的反应来实现完全的毒力。总之,我们对 RegAB 依赖性调节子及其相互关联的调节子的分析揭示了 RegAB 在协调 B. pseudomallei 对低氧条件和毒力的反应方面的关键作用,无论是在环境中还是在宿主中。