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Metabolomics and Transcriptomics Integration of Early Response of Populus tomentosa to Reduced Nitrogen Availability.

ABSTRACT: Nitrogen (N) is one of the most crucial elements for plant growth and development. However, little is known about the metabolic regulation of trees under conditions of N deficiency. In this investigation, gas chromatography-mass spectrometry (GC-MS) was used to determine global changes in metabolites and regulatory pathways in Populus tomentosa. Thirty metabolites were found to be changed significantly under conditions of low-N stress. N deficiency resulted in increased levels of carbohydrates and decreases in amino acids and some alcohols, as well as some secondary metabolites. Furthermore, an RNA-sequencing (RNA-Seq) analysis was performed to characterize the transcriptomic profiles, and 1,662 differentially expressed genes were identified in P. tomentosa. Intriguingly, four pathways related to carbohydrate metabolism were enriched. Genes involved in the gibberellic acid and indole-3-acetic acid pathways were found to be responsive to low-N stress, and the contents of hormones were then validated by high-performance liquid chromatography/electrospray ionization tandem mass spectrometry (HPLC-ESI-MS/MS). Coordinated metabolomics and transcriptomics analysis revealed a pattern of co-expression of five pairs of metabolites and unigenes. Overall, our investigation showed that metabolism directly related to N deficiency was depressed, while some components of energy metabolism were increased. These observations provided insights into the metabolic and molecular mechanisms underlying the interactions of N and carbon in poplar.

SUBMITTER: Chen M

PROVIDER: S-EPMC8692568 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Nutrient acquisition from the host environment is crucial for the survival of intracellular pathogens, but conceptual and technical challenges limit our knowledge of pathogen diets. To overcome some of these technical roadblocks, we exploited an experimentally accessible model for early infection of human macrophages by Mycobacterium tuberculosis, the etiological agent of tuberculosis, to study host-pathogen interactions with a multi-omics approach. We collected metabolomics and complete transcriptome RNA sequencing (dual RNA-seq) data of the infected macrophages, integrated them in a genome-wide reaction pair network, and identified metabolic subnetworks in host cells and M. tuberculosis that are modularly regulated during infection. Up- and downregulation of these metabolic subnetworks suggested that the pathogen utilizes a wide range of host-derived compounds, concomitant with the measured metabolic and transcriptional changes in both bacteria and host. To quantify metabolic interactions between the host and intracellular pathogen, we used a combined genome-scale model of macrophage and M. tuberculosis metabolism constrained by the dual RNA-seq data. Metabolic flux balance analysis predicted coutilization of a total of 33 different carbon sources and enabled us to distinguish between the pathogen's substrates directly used as biomass precursors and the ones further metabolized to gain energy or to synthesize building blocks. This multiple-substrate fueling confers high robustness to interventions with the pathogen's metabolism. The presented approach combining multi-omics data as a starting point to simulate system-wide host-pathogen metabolic interactions is a useful tool to better understand the intracellular lifestyle of pathogens and their metabolic robustness and resistance to metabolic interventions. IMPORTANCE The nutrients consumed by intracellular pathogens are mostly unknown. This is mainly due to the challenge of disentangling host and pathogen metabolism sharing the majority of metabolic pathways and hence metabolites. Here, we investigated the metabolic changes of Mycobacterium tuberculosis, the causative agent of tuberculosis, and its human host cell during early infection. To this aim, we combined gene expression data of both organisms and metabolite changes during the course of infection through integration into a genome-wide metabolic network. This led to the identification of infection-specific metabolic alterations, which we further exploited to model host-pathogen interactions quantitatively by flux balance analysis. These in silico data suggested that tubercle bacilli consume up to 33 different nutrients during early macrophage infection, which the bacteria utilize to generate energy and biomass to establish intracellular growth. Such multisubstrate fueling strategy renders the pathogen's metabolism robust toward perturbations, such as innate immune responses or antibiotic treatments.

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Metabolomics and Transcriptomics Integration of Early Response of Populus tomentosa to Reduced Nitrogen Availability.

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