Gut microbiome and serum metabolome alterations associated with lactose intolerance (LI): a case‒control study and paired-sample study based on the American Gut Project (AGP).

IF 5 2区 生物学 Q1 MICROBIOLOGY mSystems Pub Date : 2024-10-22 Epub Date: 2024-09-25 DOI:10.1128/msystems.00839-24
Hong Xue, Yitian Wang, Chunfeng Mei, Lili Han, Mengxiong Lu, Xuan Li, Ting Chen, Fengyun Wang, Xudong Tang
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Abstract

Lactose intolerance (LI) is a prevalent condition characterized by gastrointestinal symptoms that arise following lactose consumption. Recent evidence suggests that the gut microbiome may influence lactose levels in the gut. However, there is limited understanding regarding the alterations in microbiota and metabolism between individuals with LI and non-LI. This study conducted a paired-sample investigation utilizing data from the American Gut Project (AGP) and performed metagenomic and untargeted metabolomic analyses in a Chinese cohort to explore the interaction between the gut microbiome and serum metabolites. In addition, fecal microbiota transplantation (FMT) experiments were conducted to further examine the impact of the LI-associated gut microbiome on inflammatory outcomes. We identified 14 microbial genera that significantly differed between LI and controls from AGP data. Using a machine learning approach, group separation was predicted based on seven species and nine metabolites in the Chinese cohort. Notably, increased levels of Escherichia coli in the LI group were negatively correlated with several metabolites, including PC (22:6/0:0), indole, and Lyso PC, while reduced levels of Faecalibacterium prausnitzii and Eubacterium rectale were positively correlated with indole and furazolidone. FMT-LI rats displayed visceral hypersensitivity and an altered gut microbiota composition compared to FMT-HC rats. Metagenomic and metabolomic analyses revealed an enrichment of MAPK signaling in LI, which was confirmed by FMT-LI rats showing higher expression of ERK and RAS, along with increased concentrations of proinflammatory cytokines. This study provides valuable insights into the disrupted microbial and metabolic traits associated with LI, emphasizing potential microbiome-based approaches for its prevention and treatment.

Importance: Lactose intolerance (LI) is a prevalent condition characterized by gastrointestinal symptoms after lactose consumption due to a deficiency of lactase. There is limited understanding regarding the microbiota and metabolic alterations between individuals with LI and non-LI. This study represents the first exploration to investigate metagenomic and metabolomic signatures among subjects with lactose intolerance as far as our knowledge. We identified 14 microbial genera in the Western cohort and 7 microbial species, along with 9 circulating metabolites in the Chinese cohort, which significantly differed in LI patients. Metagenomic and metabolomic analyses revealed an enrichment of MAPK signaling in LI patients. This finding was confirmed by FMT-LI rats, exhibiting increased expression of ERK and RAS, along with higher concentrations of pro-inflammatory cytokines. Our study provides insights into the disrupted functional and metabolic traits of the gut microbiome in LI, highlighting potential microbiome-based approaches for preventing and treating LI.

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与乳糖不耐症(LI)相关的肠道微生物组和血清代谢组改变:基于美国肠道项目(AGP)的病例对照研究和配对样本研究。
乳糖不耐症(LI)是一种普遍存在的疾病,其特征是在摄入乳糖后出现胃肠道症状。最近的证据表明,肠道微生物群可能会影响肠道中的乳糖水平。然而,人们对乳糖依赖症患者和非乳糖依赖症患者之间微生物群和新陈代谢的改变了解有限。本研究利用美国肠道项目(AGP)的数据进行了配对样本调查,并在中国队列中进行了元基因组和非靶向代谢组分析,以探索肠道微生物组和血清代谢物之间的相互作用。此外,我们还进行了粪便微生物群移植(FMT)实验,以进一步研究李氏综合征相关肠道微生物群对炎症结果的影响。我们从 AGP 数据中发现了 14 个在 LI 和对照组之间存在显著差异的微生物属。利用机器学习方法,根据中国队列中的 7 个物种和 9 个代谢物预测了组别分离。值得注意的是,LI 组大肠埃希氏菌含量的增加与包括 PC(22:6/0:0)、吲哚和溶血 PC 在内的几种代谢物呈负相关,而普氏粪杆菌和直肠大肠杆菌含量的减少与吲哚和呋喃唑酮呈正相关。与 FMT-HC 大鼠相比,FMT-LI 大鼠表现出内脏过敏性和肠道微生物群组成的改变。元基因组学和代谢组学分析表明,LI 中的 MAPK 信号转导丰富,FMT-LI 大鼠的 ERK 和 RAS 表达较高,促炎细胞因子浓度增加,证实了这一点。这项研究为了解与乳糖不耐受症相关的微生物和代谢紊乱特征提供了有价值的见解,强调了预防和治疗乳糖不耐受症的潜在微生物方法:乳糖不耐受(LI)是一种普遍存在的疾病,其特征是由于缺乏乳糖酶而在摄入乳糖后出现胃肠道症状。人们对乳糖不耐受症患者与非乳糖不耐受症患者之间的微生物群和新陈代谢变化的了解有限。据我们所知,本研究是对乳糖不耐受患者的元基因组和代谢组特征进行的首次探索。我们在西方队列中发现了 14 个微生物属,在中国队列中发现了 7 个微生物物种和 9 种循环代谢物,这些微生物属和代谢物在乳糖不耐受患者中存在显著差异。元基因组学和代谢组学分析表明,MAPK 信号在 LI 患者中富集。FMT-LI大鼠证实了这一发现,其ERK和RAS的表达增加,促炎细胞因子的浓度也更高。我们的研究深入揭示了李氏综合症患者肠道微生物组功能和代谢特征的紊乱,突出了基于微生物组的预防和治疗李氏综合症的潜在方法。
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来源期刊
mSystems
mSystems Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
10.50
自引率
3.10%
发文量
308
审稿时长
13 weeks
期刊介绍: mSystems™ will publish preeminent work that stems from applying technologies for high-throughput analyses to achieve insights into the metabolic and regulatory systems at the scale of both the single cell and microbial communities. The scope of mSystems™ encompasses all important biological and biochemical findings drawn from analyses of large data sets, as well as new computational approaches for deriving these insights. mSystems™ will welcome submissions from researchers who focus on the microbiome, genomics, metagenomics, transcriptomics, metabolomics, proteomics, glycomics, bioinformatics, and computational microbiology. mSystems™ will provide streamlined decisions, while carrying on ASM''s tradition of rigorous peer review.
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