墨西哥裔美国人的肠道噬菌体组:代谢功能障碍相关性脂肪肝和糖尿病的高危人群。

IF 5 2区 生物学 Q1 MICROBIOLOGY mSystems Pub Date : 2024-09-17 Epub Date: 2024-08-21 DOI:10.1128/msystems.00434-24
Suet-Ying Kwan, Caroline M Sabotta, Lorenzo R Cruz, Matthew C Wong, Nadim J Ajami, Joseph B McCormick, Susan P Fisher-Hoch, Laura Beretta
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引用次数: 0

摘要

墨西哥裔美国人受代谢功能障碍相关性脂肪性肝病(MASLD)的影响不成比例,这种疾病通常与糖尿病并发。尽管有大量证据表明肠道微生物组在 MASLD 中的致病作用,但确定肠道噬菌体参与其中的研究却很少。在这项横断面研究中,我们通过对 340 名受试者进行粪便猎枪元基因组测序,确定了南得克萨斯州墨西哥裔美国人肠道噬菌体组的特征,并同时通过瞬时弹性成像技术筛查肝脏脂肪变性。噬菌体组的个体间差异与性别、出生国、糖尿病和肝脏脂肪变性有关。随后确定了糖尿病和肝脏脂肪变性的噬菌体特征。Inoviridae 的富集与糖尿病和肝脏脂肪变性有关。糖尿病还与主要是温带大肠杆菌噬菌体的富集有关,其中一些噬菌体具有毒力因子。肝脏脂肪变性与乳球菌噬菌体 r1t 和 BK5-T 的减少以及全球流行的 Crassvirales 噬菌体的富集有关,其中包括属群 IX(大肠伯沙病毒、粪伯沙病毒)和 VI(口腔卡诺病毒)的成员。乳球菌噬菌体与乳酸乳球菌有很强的相关性和共存性,而 Crassvirales 噬菌体、大肠杆菌、粪肠杆菌和 UAG-readthrough crAss 支系与 copri 普雷沃特氏菌有相关性和共存性。总之,我们发现了两种密切相关的代谢性疾病的肠道噬菌体组特征,这两种疾病在全球造成了巨大的负担。这些噬菌体特征可能对这一高危人群的风险建模和疾病预防有用,并能确定噬菌体疗法的潜在细菌靶标。我们利用高风险墨西哥裔美国人的粪便样本,深入研究了与糖尿病和肝脂肪变性这两种密切相关的代谢性疾病有关的肠道噬菌体组变化。这两种疾病的共同点是伊诺维病毒科(Inoviridae)噬菌体的富集,伊诺维病毒科是一组能长期感染细菌宿主而不溶解的噬菌体,它们能显著影响细菌的生长、毒力、活力、生物膜的形成和水平基因转移。糖尿病还与大肠杆菌感染噬菌体的富集有关,其中一些噬菌体含有毒力因子。肝脏脂肪变性还与乳酸乳球菌感染噬菌体的减少和Crassvirales噬菌体的富集有关。这些噬菌体组特征可用于风险建模,并确定噬菌体疗法的潜在细菌靶标。
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Gut phageome in Mexican Americans: a population at high risk for metabolic dysfunction-associated steatotic liver disease and diabetes.

Mexican Americans are disproportionally affected by metabolic dysfunction-associated steatotic liver disease (MASLD), which often co-occurs with diabetes. Despite extensive evidence on the causative role of the gut microbiome in MASLD, studies determining the involvement of the gut phageome are scarce. In this cross-sectional study, we characterized the gut phageome in Mexican Americans of South Texas by stool shotgun metagenomic sequencing of 340 subjects, concurrently screened for liver steatosis by transient elastography. Inter-individual variations in the phageome were associated with gender, country of birth, diabetes, and liver steatosis. The phage signatures for diabetes and liver steatosis were subsequently determined. Enrichment of Inoviridae was associated with both diabetes and liver steatosis. Diabetes was further associated with the enrichment of predominantly temperate Escherichia phages, some of which possessed virulence factors. Liver steatosis was associated with the depletion of Lactococcus phages r1t and BK5-T, and enrichment of the globally prevalent Crassvirales phages, including members of genus cluster IX (Burzaovirus coli, Burzaovirus faecalis) and VI (Kahnovirus oralis). The Lactococcus phages showed strong correlations and co-occurrence with Lactococcus lactis, while the Crassvirales phages, B. coli, B. faecalis, and UAG-readthrough crAss clade correlated and co-occurred with Prevotella copri. In conclusion, we identified the gut phageome signatures for two closely linked metabolic diseases with significant global burden. These phage signatures may have utility in risk modeling and disease prevention in this high-risk population, and identification of potential bacterial targets for phage therapy.IMPORTANCEPhages influence human health and disease by shaping the gut bacterial community. Using stool samples from a high-risk Mexican American population, we provide insights into the gut phageome changes associated with diabetes and liver steatosis, two closely linked metabolic diseases with significant global burden. Common to both diseases was an enrichment of Inoviridae, a group of phages that infect bacterial hosts chronically without lysis, allowing them to significantly influence bacterial growth, virulence, motility, biofilm formation, and horizontal gene transfer. Diabetes was additionally associated with the enrichment of Escherichia coli-infecting phages, some of which contained virulence factors. Liver steatosis was additionally associated with the depletion of Lactococcus lactis-infecting phages, and enrichment of Crassvirales phages, a group of virulent phages with high global prevalence and persistence across generations. These phageome signatures may have utility in risk modeling, as well as identify potential bacterial targets for phage therapy.

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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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