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The structural alteration of gut microbiota in low-birth-weight mice undergoing accelerated postnatal growth.

ABSTRACT: The transient disruption of gut microbiota in infancy by antibiotics causes adult adiposity in mice. Accelerated postnatal growth (A) leads to a higher risk of adult metabolic syndrome in low birth-weight (LB) humans than in normal birth-weight (NB) individuals, but the underlying mechanism remains unclear. Here, we set up an experiment using LB + A mice, NB + A mice, and control mice with NB and normal postnatal growth. At 24 weeks of age (adulthood), while NB + A animals had a normal body fat content and glucose tolerance compared with controls, LB + A mice exhibited excessive adiposity and glucose intolerance. In infancy, more fecal bacteria implicated in obesity were increased in LB + A pups than in NB + A pups, including Desulfovibrionaceae, Enterorhabdus, and Barnesiella. One bacterium from the Lactobacillus genus, which has been implicated in prevention of adult adiposity, was enhanced only in NB + A pups. Besides, LB + A pups, but not NB + A pups, showed disrupted gut microbiota fermentation activity. After weaning, the fecal microbiota composition of LB + A mice, but not that of NB + A animals, became similar to that of controls by 24 weeks. In infancy, LB + A mice have a more dysbiotic gut microbiome compared to NB + A mice, which might increase their risk of adult metabolic syndrome.

SUBMITTER: Wang J

PROVIDER: S-EPMC4899793 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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The structural alteration of gut microbiota in low-birth-weight mice undergoing accelerated postnatal growth.

Wang Jingjing J Tang Huang H Wang Xiaoxin X Zhang Xu X Zhang Chenhong C Zhang Menghui M Zhao Yufeng Y Zhao Liping L Shen Jian J

Scientific reports 20160609

The transient disruption of gut microbiota in infancy by antibiotics causes adult adiposity in mice. Accelerated postnatal growth (A) leads to a higher risk of adult metabolic syndrome in low birth-weight (LB) humans than in normal birth-weight (NB) individuals, but the underlying mechanism remains unclear. Here, we set up an experiment using LB + A mice, NB + A mice, and control mice with NB and normal postnatal growth. At 24 weeks of age (adulthood), while NB + A animals had a normal body fat ...[more]

PMID: 27277748

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Project description:BackgroundThe gastrointestinal tract (GIT) microbiota is essential to metabolic health, and the prevalence of the Western diet (WD) high in fat and sugar is increasing, with evidence highlighting a negative interaction between the GIT and WD, resulting in liver dysfunction. Additionally, an adverse in utero environment such as placental insufficiency resulting in low birth weight (LBW) offspring, contributes to an increased risk of metabolic diseases such as fatty liver infiltration and liver dysfunction in later life. We sought to understand the potential interactive effects of exposure to a WD upon growing LBW offspring. We postulated that LBW offspring when challenged with a poor postnatal diet, would display an altered microbiota and more severe liver metabolic dysfunction.MethodsThe fecal microbiota of normal birth weight (NBW) and LBW young guinea pig offspring, weaned onto either a control diet (CD) or WD was determined with 16S rRNA gene next generation sequencing at young adulthood following the early rapid growth phase after weaning. A liver blood chemistry profile was also performed.ResultsThe life-long consumption of WD following weaning into young adulthood resulted in increased total cholesterol, triglycerides and alanine aminotransferase levels in association with an altered GIT microbiota when compared to offspring consuming CD. Neither birth weight nor sex were associated with any significant changes in microbiota alpha diversity, by measuring the Shannon's diversity index. One hundred forty-eight operational taxonomic units were statistically distinct between the diet groups, independent of birth weight. In the WD group, significant decreases were detected in Barnesiella, Methanobrevibacter smithii and relatives of Oscillospira guillermondii, while Butyricimonas and Bacteroides spp. were increased.DiscussionThese results describe the GIT microbiota in a guinea pig model of LBW and WD associated metabolic syndrome and highlight several WD specific GIT alterations associated with human metabolic disease.

Project description:ObjectiveThe aim of this study is to comprehensively investigate the temporal dynamics of faecal gut microbiota and metabonomics in early postnatal with a focus on very low or extremely low birth weight (VLBW/ELBW) infants.MethodsWe collected faecal samples from 157 VLBW/ELBW infants at three time points: days 1, 14, and 28 in a prospective cohort study. The faecal microbial diversity, abundance, composition, and metabolomic analyses were determined using 16S rRNA sequencing and liquid chromatography tandem mass spectrometry (LC-MS/MS). Microbiome functional analyses were conducted utilizing PICRUSt2. The ecological association networks were employed to investigate the interactions between gut microbiota and identify the core genus within 28 days of birth, as well as to unveil correlations between taxa and metabolites.Result(1) The alpha diversity of gut microbiota significantly decreased from D1 to D28, accompanied by an interrupted trajectory lacking obligate anaerobes. At the phylum level, the 16S RNA sequencing results showed an increase in Proteobacteria and a decrease in Firmicutes and Bacteroidota from D1 to D28. At the genus level, there was a decrease in the relative abundance of Staphylococcus, Acinetobacter and Ureaplasma, with Klebsiella and Enterococcus emerging as the most abundant genera. (2) The analysis revealed a total of 561 metabolic markers that exhibited significant and distinct alterations between D1 and D14. (3) Ecological association networks revealed that the gut microbiota in D1 exhibited a significantly higher degree of microbial interactions compared to those in D14 and D28. Additionally, Enterococcus, Klebsiella, and Enterobacter were major contributors to the co-occurring network at these three time points. (4) Steroid hormone biosynthesis, including tetrahydrocortisone, androsterone glucuronide, androstenedione and etiocholanolone glucuronide, decreased within 28 days after birth.ConclusionWe have successfully demonstrated a significant dysbiosis in the gut microbiota and a subsequent decrease in its diversity within 4 weeks postpartum in VLBW/ELBW infants. Monitoring the gut microbiota of VLBW/ELBW infants and promptly rectifying dysbiosis in the early stages may represent a potential therapeutic strategy.

Project description:BackgroundInfants born prematurely, particularly extremely low birth weight infants (ELBW) have altered gut microbial communities. Factors such as maternal health, gut immaturity, delivery mode, and antibiotic treatments are associated with microbiota disturbances, and are linked to an increased risk of certain diseases such as necrotising enterocolitis. Therefore, there is a requirement to optimally characterise microbial profiles in this at-risk cohort, via standardisation of methods, particularly for studying the influence of microbiota therapies (e.g. probiotic supplementation) on community profiles and health outcomes. Profiling of faecal samples using the 16S rRNA gene is a cost-efficient method for large-scale clinical studies to gain insights into the gut microbiota and additionally allows characterisation of cohorts were sample quantities are compromised (e.g. ELBW infants). However, DNA extraction method, and the 16S rRNA region targeted can significantly change bacterial community profiles obtained, and so confound comparisons between studies. Thus, we sought to optimise a 16S rRNA profiling protocol to allow standardisation for studying ELBW infant faecal samples, with or without probiotic supplementation.MethodsUsing ELBW faecal samples, we compared three different DNA extraction methods, and subsequently PCR amplified and sequenced three hypervariable regions of the 16S rRNA gene (V1 + V2 + V3), (V4 + V5) and (V6 + V7 + V8), and compared two bioinformatics approaches to analyse results (OTU and paired end). Paired shotgun metagenomics was used as a 'gold-standard'.ResultsResults indicated a longer bead-beating step was required for optimal bacterial DNA extraction and that sequencing regions (V1 + V2 + V3) and (V6 + V7 + V8) provided the most representative taxonomic profiles, which was confirmed via shotgun analysis. Samples sequenced using the (V4 + V5) region were found to be underrepresented in specific taxa including Bifidobacterium, and had altered diversity profiles. Both bioinformatics 16S rRNA pipelines used in this study (OTU and paired end) presented similar taxonomic profiles at genus level.ConclusionsWe determined that DNA extraction from ELBW faecal samples, particularly those infants receiving probiotic supplementation, should include a prolonged beat-beating step. Furthermore, use of the 16S rRNA (V1 + V2 + V3) and (V6 + V7 + V8) regions provides reliable representation of ELBW microbiota profiles, while inclusion of the (V4 + V5) region may not be appropriate for studies where Bifidobacterium constitutes a resident microbiota member.

Dataset Information

The structural alteration of gut microbiota in low-birth-weight mice undergoing accelerated postnatal growth.

Publications

The structural alteration of gut microbiota in low-birth-weight mice undergoing accelerated postnatal growth.

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