Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA.
Infectious Diseases Institute, The Ohio State University, Columbus, Ohio, USA.
Microbiol Spectr. 2024 Apr 2;12(4):e0413823. doi: 10.1128/spectrum.04138-23. Epub 2024 Mar 1.
Chemistry in eukaryotic intercellular spaces is shaped by both hosts and symbiotic microorganisms such as bacteria. Pathogenic microorganisms like barley-associated (Xt) swiftly overtake the inner leaf tissue becoming the dominant microbial community member during disease development. The dynamic metabolic changes due to Xt pathogenesis in the mesophyll spaces remain unknown. Genomic group I of Xt consists of two barley-infecting lineages: pathovar translucens (Xtt) and pathovar undulosa (Xtu). Xtu and Xtt, although genomically distinct, cause similar water-soaked lesions. To define the metabolic signals associated with inner leaf colonization, we used untargeted metabolomics to characterize Xtu and Xtt metabolism signatures associated with mesophyll growth. We found that mesophyll apoplast fluid from infected tissue yielded a distinct metabolic profile and shift from catabolic to anabolic processes over time compared to water-infiltrated control. The pathways with the most differentially expressed metabolites by time were glycolysis, tricarboxylic acid cycle, sucrose metabolism, pentose interconversion, amino acids, galactose, and purine metabolism. Hierarchical clustering and principal component analysis showed that metabolic changes were more affected by the time point rather than the individual colonization of the inner leaves by Xtt compared to Xtu. Overall, in this study, we identified metabolic pathways that explain carbon and nitrogen usage during host-bacterial interactions over time for mesophyll tissue colonization. This foundational research provides initial insights into shared metabolic strategies of inner leaf colonization niche occupation by related but phylogenetically distinct phyllosphere bacteria.
The phyllosphere is a habitat for microorganisms including pathogenic bacteria. Metabolic shifts in the inner leaf spaces for most plant-microbe interactions are unknown, especially for species in understudied plants like barley (). pv. translucens (Xtt) and pv. undulosa (Xtu) are phylogenomically distinct, but both colonize barley leaves for pathogenesis. In this study, we used untargeted metabolomics to shed light on Xtu and Xtt metabolic signatures. Our findings revealed a dynamic metabolic landscape that changes over time, rather than exhibiting a pattern associated with individual pathovars. These results provide initial insights into the metabolic mechanisms of inner leaf pathogenesis.
真核细胞间空间的化学物质由宿主和共生微生物如细菌共同塑造。像大麦相关的（Xt）这样的致病性微生物迅速占领叶片内部组织，在疾病发展过程中成为主要的微生物群落成员。由于 Xt 致病而在叶肉空间中发生的动态代谢变化尚不清楚。Xt 的基因组第 I 组由两个大麦感染谱系组成：透明病变体（Xtt）和波纹病变体（Xtu）。尽管 Xtu 和 Xtt 在基因组上有区别，但它们引起的水浸状病斑相似。为了确定与叶片内部定殖相关的代谢信号，我们使用非靶向代谢组学来描述与叶肉生长相关的 Xtu 和 Xtt 代谢特征。我们发现，与水浸润对照相比，来自感染组织的叶肉质外液在时间上表现出独特的代谢特征，并随着时间的推移从分解代谢向合成代谢转变。随着时间的推移，差异表达代谢物最多的途径是糖酵解、三羧酸循环、蔗糖代谢、戊糖互变、氨基酸、半乳糖和嘌呤代谢。层次聚类和主成分分析表明，代谢变化受时间点的影响比 Xtt 与 Xtu 对内叶的单独定殖更大。总的来说，在这项研究中，我们确定了随着时间的推移，在叶肉组织定殖过程中解释宿主-细菌相互作用过程中碳和氮利用的代谢途径。这项基础研究为相关但系统发育上不同的叶际细菌对叶片内部定殖生态位的共同代谢策略提供了初步见解。
叶际是包括致病性细菌在内的微生物的栖息地。大多数植物-微生物相互作用的叶片内部空间的代谢变化尚不清楚，特别是对于像大麦这样的研究较少的植物中的物种（）。pv. translucens（Xtt）和 pv. undulosa（Xtu）在系统发育上是不同的，但都在大麦叶片上进行致病定殖。在这项研究中，我们使用非靶向代谢组学来揭示 Xtu 和 Xtt 的代谢特征。我们的发现揭示了一个随时间变化的动态代谢景观，而不是表现出与单个病变体相关的模式。这些结果为 叶片内部发病机制的代谢机制提供了初步的见解。
