{"title":"Multiomics approach reveals the comprehensive interactions between nutrition and children's gut microbiota, and microbial and host metabolomes.","authors":"Mingyu Zhu, Qi Wang, Yan Yang, Xiaobing Liu, Jiawen Zhang, Guanghao Li, Wenqing Liu, Xuesong Xiang, Juanjuan Chen","doi":"10.1186/s12937-025-01116-6","DOIUrl":null,"url":null,"abstract":"<p><p>The gut microbiome can modulate nutrient metabolism to produce many metabolites interacting with the host. However, the intricate interactions among dietary intake, the gut microbiome and metabolites, and host metabolites need to be further explored although some studies have been devoted to it. Here, in a cross-sectional studies, 88 children aged 2-12 years were enrolled from northwestern China. The dietary intake data were collected via a designed food frequency questionnaire to calculate plant-based diet indices (PDIs). Stool and plasma samples were collected for metagenomic and broad-targeted metabolomic analysis. Spearman's rank correlation was used to describe the associations between nutrients/PDIs and the gut microbiota and metabolites. PDI was significantly positively associated with Bilophila wadsworthia, Bacteroides thetaiotaomicron, and Alistipes indistinctus, etc., but was obviously negatively correlated with Roseburia intestinalis, Faecalibacterium prausnitzii, etc. However, these species showed no significant associations with either healthy PDI (hPDI) or unhealthy PDI (uPDI). Interestingly, hPDI was significantly positively related to species, including Ruminococcus bicirculans, and was significantly negatively associated with uPDI, and vice versa. The above correlation trends were also observed between PDIs and predicted gut microbial functional pathways, microbial metabolites and the host metabolome. Notably, the significantly related pathways were focused mainly on substances and energy metabolism. PDI was significantly positively associated with the fecal contents of P-aminobenzoate, chenodeoxycholic acid, 4,6-dihydroxyquinoline, quinoline-4,8-diol, etc., but was significantly negatively associated with those of TMAO, FFA, creatine phosphate, etc. In plasma, PDI was significantly positively associated with sarcosine, ornithine, L-histidine, etc., but was distinctly negatively correlated with FFAs, carnitine C2:0, etc. Strikingly, the healthy plant-based diet index (hPDI) is correlated with increased levels of metabolites related to tryptophan metabolism, whereas the unhealthy PDI (uPDI) is linked to increased levels of metabolites associated with tyrosine and sphingolipid metabolism, which are pathways commonly associated with Western diets. Our studies provide reliable data support and a comprehensive understanding of the effects of dietary intake on the gut microbiome and microbial and host metabolites and lay a foundation for further studies of the diet-gut microbiota-microbial metabolites and host metabolism.</p>","PeriodicalId":19203,"journal":{"name":"Nutrition Journal","volume":"24 1","pages":"50"},"PeriodicalIF":4.4000,"publicationDate":"2025-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Nutrition Journal","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1186/s12937-025-01116-6","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NUTRITION & DIETETICS","Score":null,"Total":0}
引用次数: 0
Abstract
The gut microbiome can modulate nutrient metabolism to produce many metabolites interacting with the host. However, the intricate interactions among dietary intake, the gut microbiome and metabolites, and host metabolites need to be further explored although some studies have been devoted to it. Here, in a cross-sectional studies, 88 children aged 2-12 years were enrolled from northwestern China. The dietary intake data were collected via a designed food frequency questionnaire to calculate plant-based diet indices (PDIs). Stool and plasma samples were collected for metagenomic and broad-targeted metabolomic analysis. Spearman's rank correlation was used to describe the associations between nutrients/PDIs and the gut microbiota and metabolites. PDI was significantly positively associated with Bilophila wadsworthia, Bacteroides thetaiotaomicron, and Alistipes indistinctus, etc., but was obviously negatively correlated with Roseburia intestinalis, Faecalibacterium prausnitzii, etc. However, these species showed no significant associations with either healthy PDI (hPDI) or unhealthy PDI (uPDI). Interestingly, hPDI was significantly positively related to species, including Ruminococcus bicirculans, and was significantly negatively associated with uPDI, and vice versa. The above correlation trends were also observed between PDIs and predicted gut microbial functional pathways, microbial metabolites and the host metabolome. Notably, the significantly related pathways were focused mainly on substances and energy metabolism. PDI was significantly positively associated with the fecal contents of P-aminobenzoate, chenodeoxycholic acid, 4,6-dihydroxyquinoline, quinoline-4,8-diol, etc., but was significantly negatively associated with those of TMAO, FFA, creatine phosphate, etc. In plasma, PDI was significantly positively associated with sarcosine, ornithine, L-histidine, etc., but was distinctly negatively correlated with FFAs, carnitine C2:0, etc. Strikingly, the healthy plant-based diet index (hPDI) is correlated with increased levels of metabolites related to tryptophan metabolism, whereas the unhealthy PDI (uPDI) is linked to increased levels of metabolites associated with tyrosine and sphingolipid metabolism, which are pathways commonly associated with Western diets. Our studies provide reliable data support and a comprehensive understanding of the effects of dietary intake on the gut microbiome and microbial and host metabolites and lay a foundation for further studies of the diet-gut microbiota-microbial metabolites and host metabolism.
期刊介绍:
Nutrition Journal publishes surveillance, epidemiologic, and intervention research that sheds light on i) influences (e.g., familial, environmental) on eating patterns; ii) associations between eating patterns and health, and iii) strategies to improve eating patterns among populations. The journal also welcomes manuscripts reporting on the psychometric properties (e.g., validity, reliability) and feasibility of methods (e.g., for assessing dietary intake) for human nutrition research. In addition, study protocols for controlled trials and cohort studies, with an emphasis on methods for assessing dietary exposures and outcomes as well as intervention components, will be considered.
Manuscripts that consider eating patterns holistically, as opposed to solely reductionist approaches that focus on specific dietary components in isolation, are encouraged. Also encouraged are papers that take a holistic or systems perspective in attempting to understand possible compensatory and differential effects of nutrition interventions. The journal does not consider animal studies.
In addition to the influence of eating patterns for human health, we also invite research providing insights into the environmental sustainability of dietary practices. Again, a holistic perspective is encouraged, for example, through the consideration of how eating patterns might maximize both human and planetary health.