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Understanding the gut microbiota by considering human evolution: a story of fire, cereals, cooking, molecular ingenuity, and functional cooperation.
Tannock, GW
Microbiology and molecular biology reviews : MMBR. 2024;(1):e0012722
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SUMMARYThe microbial community inhabiting the human colon, referred to as the gut microbiota, is mostly composed of bacterial species that, through extensive metabolic networking, degrade and ferment components of food and human secretions. The taxonomic composition of the microbiota has been extensively investigated in metagenomic studies that have also revealed details of molecular processes by which common components of the human diet are metabolized by specific members of the microbiota. Most studies of the gut microbiota aim to detect deviations in microbiota composition in patients relative to controls in the hope of showing that some diseases and conditions are due to or exacerbated by alterations to the gut microbiota. The aim of this review is to consider the gut microbiota in relation to the evolution of Homo sapiens which was heavily influenced by the consumption of a nutrient-dense non-arboreal diet, limited gut storage capacity, and acquisition of skills relating to mastering fire, cooking, and cultivation of cereal crops. The review delves into the past to gain an appreciation of what is important in the present. A holistic view of "healthy" microbiota function is proposed based on the evolutionary pathway shared by humans and gut microbes.
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Building Robust Assemblages of Bacteria in the Human Gut in Early Life.
Tannock, GW
Applied and environmental microbiology. 2021;(22):e0144921
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The neonatal body provides a range of potential habitats, such as the gut, for microbes. These sites eventually harbor microbial communities (microbiotas). A "complete" (adult) gut microbiota is not acquired by the neonate immediately after birth. Rather, the exclusive, milk-based nutrition of the infant encourages the assemblage of a gut microbiota of low diversity, usually dominated by bifidobacterial species. The maternal fecal microbiota is an important source of bacterial species that colonize the gut of infants, at least in the short-term. However, development of the microbiota is influenced by the use of human milk (breast feeding), infant formula, preterm delivery of infants, caesarean delivery, antibiotic administration, family details and other environmental factors. Following the introduction of weaning (complementary) foods, the gut microbiota develops in complexity due to the availability of a diversity of plant glycans in fruits and vegetables. These glycans provide growth substrates for the bacterial families (such as members of the Ruminococcaceae and Lachnospiraceae) that, in due course, will dominate the gut microbiota of the adult. Although current data are often fragmentary and observational, it can be concluded that the nutrition that a child receives in early life is likely to impinge not only on the development of the microbiota at that time but also on the subsequent lifelong, functional relationships between the microbiota and the human host. The purpose of this review, therefore, is to discuss the importance of promoting the assemblage of functionally robust gut microbiotas at appropriate times in early life.
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Using compositional principal component analysis to describe children's gut microbiota in relation to diet and body composition.
Leong, C, Haszard, JJ, Heath, AM, Tannock, GW, Lawley, B, Cameron, SL, Szymlek-Gay, EA, Gray, AR, Taylor, BJ, Galland, BC, et al
The American journal of clinical nutrition. 2020;(1):70-78
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BACKGROUND Gut microbiota data obtained by DNA sequencing are complex and compositional because of large numbers of detectable taxa, and because microbiota characteristics are described in relative terms. Nutrition researchers use principal component analysis (PCA) to derive dietary patterns from food data. Although compositional PCA methods are not commonly used to describe patterns from complex microbiota data, this approach would be useful for identifying gut microbiota patterns associated with diet and body composition. OBJECTIVES To use compositional PCA to describe the principal components (PCs) of gut microbiota in 5-y-old children and explore associations between microbiota components, diet, and BMI z-score. METHODS A fecal sample was provided by 319 children aged 5 y. Their primary caregiver completed a validated 123-item quantitative FFQ. Body composition was determined using DXA, and a BMI z-score was calculated. Compositional PCA identified characterizing taxa and weightings for calculation of gut microbiota PC scores at the genus level, and was examined in relation to diet and body size. RESULTS Three gut microbiota PCs were found. PC1 (negative loadings on uncultured Christensenellaceae and Ruminococcaceae) was related to lower BMI z-scores and longer duration of breastfeeding (per month) (β = -0.14; 95% CI: -0.26, -0.02; and β = 0.02; 95% CI: 0.003, 0.34, respectively). PC2 (positive loadings on Fusicatenibacter and Bifidobacterium; negative loadings on Bacteroides) was associated with a lower intake of nuts, seeds, and legumes (β = -0.05 per gram; 95% CI: -0.09, -0.01). When adjusted for fiber intake, PC2 was also associated with higher BMI z-scores (β = 0.12; 95% CI: 0.01, 0.24). PC3 (positive loadings on Faecalibacterium, Eubacterium, and Roseburia) was associated with higher intakes of fiber (β = 0.02 per gram; 95% CI: 0.003, 0.04) and total nonstarch polysaccharides (β = 0.02 per gram; 95% CI: 0.003, 0.04). CONCLUSIONS Our results suggest that specific gut microbiota components determined using compositional PCA are associated with diet and BMI z-score.This trial was registered at clinicaltrials.gov as NCT00892983.
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Bifidobacterium bifidum ATCC 15696 and Bifidobacterium breve 24b Metabolic Interaction Based on 2'-O-Fucosyl-Lactose Studied in Steady-State Cultures in a Freter-Style Chemostat.
Centanni, M, Ferguson, SA, Sims, IM, Biswas, A, Tannock, GW
Applied and environmental microbiology. 2019;(7)
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Infants fed breast milk harbor a gut microbiota in which bifidobacteria are generally predominant. The metabolic interactions of bifidobacterial species need investigation because they may offer insight into the colonization of the gut in early life. Bifidobacterium bifidum ATCC 15696 hydrolyzes 2'-O-fucosyl-lactose (2FL; a major fucosylated human milk oligosaccharide) but does not use fucose released into the culture medium. However, fucose is a growth substrate for Bifidobacterium breve 24b, and both strains utilize lactose for growth. The provision of fucose and lactose by B. bifidum (the donor) allowing the growth of B. breve (the beneficiary) conforms to the concept of syntrophy, but both strains will compete for lactose to multiply. To determine the metabolic impact of this syntrophic/competitive relationship on the donor, the transcriptomes of B. bifidum were determined and compared in steady-state monoculture and coculture using transcriptome sequencing (RNA-seq) and reverse transcription-quantitative PCR (RT-qPCR). B. bifidum genes upregulated in coculture included those encoding alpha-l-fucosidase and carbohydrate transporters and those involved in energy production and conversion. B. bifidum abundance was the same in coculture as in monoculture, but B. breve dominated the coculture numerically. Cocultures during steady-state growth in 2FL medium produced mostly acetate with little lactate (acetate:lactate molar ratio, 8:1) compared to that in monobatch cultures containing lactose (2:1), which reflected the maintenance of steady-state cells in log-phase growth. Darwinian competition is an implicit feature of bacterial communities, but syntrophy is a phenomenon putatively based on cooperation. Our results suggest that the regulation of syntrophy, in addition to competition, may shape bacterial communities.IMPORTANCE This study addresses the microbiology and function of a natural ecosystem (the infant bowel) using in vitro experimentation with bacterial cultures maintained under controlled growth and environmental conditions. We studied the growth of bifidobacteria whose nutrition centered on the hydrolysis of a human milk oligosaccharide. The results revealed responses relating to metabolism occurring in a Bifidobacterium bifidum strain when it provided nutrients that allowed the growth of Bifidobacterium breve, and so discovered biochemical features of these bifidobacteria in relation to metabolic interaction in the shared environment. These kinds of experiments are essential in developing concepts of bifidobacterial ecology that relate to the development of the gut microbiota in early life.
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Fecal Microbiotas of Indonesian and New Zealand Children Differ in Complexity and Bifidobacterial Taxa during the First Year of Life.
Lawley, B, Otal, A, Moloney-Geany, K, Diana, A, Houghton, L, Heath, AM, Taylor, RW, Tannock, GW
Applied and environmental microbiology. 2019;(19)
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The biological succession that occurs during the first year of life in the gut of infants in Western countries is broadly predictable in terms of the increasing complexity of the composition of microbiotas. Less information is available about microbiotas in Asian countries, where environmental, nutritional, and cultural influences may differentially affect the composition and development of the microbial community. We compared the fecal microbiotas of Indonesian (n = 204) and New Zealand (NZ) (n = 74) infants 6 to 7 months and 12 months of age. Comparisons were made by analysis of 16S rRNA gene sequences and derivation of community diversity metrics, relative abundances of bacterial families, enterotypes, and cooccurrence correlation networks. Abundances of Bifidobacterium longum subsp. infantis and B. longum subsp. longum were determined by quantitative PCR. All observations supported the view that the Indonesian and NZ infant microbiotas developed in complexity over time, but the changes were much greater for NZ infants. B. longum subsp. infantis dominated the microbiotas of Indonesian children, whereas B. longum subsp. longum was dominant in NZ children. Network analysis showed that the niche model (in which trophic adaptation results in preferential colonization) of the assemblage of microbiotas was supported in Indonesian infants, whereas the neutral (stochastic) model was supported by the development of the microbiotas of NZ infants. The results of the study show that the development of the fecal microbiota is not the same for infants in all countries, and they point to the necessity of obtaining a better understanding of the factors that control the colonization of the gut in early life.IMPORTANCE This study addresses the microbiology of a natural ecosystem (the infant bowel) for children in a rural setting in Indonesia and in an urban environment in New Zealand. Analysis of DNA sequences generated from the microbial community (microbiota) in the feces of the infants during the first year of life showed marked differences in the composition and complexity of the bacterial collections. The differences were most likely due to differences in the prevalence and duration of breastfeeding of infants in the two countries. These kinds of studies are essential for developing concepts of microbial ecology related to the influence of nutrition and environment on the development of the gut microbiota and for determining the long-term effects of microbiological events in early life on human health and well-being.
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Sleep, nutrition, and physical activity interventions to prevent obesity in infancy: follow-up of the Prevention of Overweight in Infancy (POI) randomized controlled trial at ages 3.5 and 5 y.
Taylor, RW, Gray, AR, Heath, AM, Galland, BC, Lawrence, J, Sayers, R, Healey, D, Tannock, GW, Meredith-Jones, KA, Hanna, M, et al
The American journal of clinical nutrition. 2018;(2):228-236
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BACKGROUND Our Prevention of Overweight in Infancy (POI) study suggested that a brief sleep intervention in infancy reduced the risk of obesity at age 2 y. In contrast, we observed no benefit from the nutrition and activity intervention. OBJECTIVE The objective of the study was to determine how these interventions influenced growth at ages 3.5 and 5 y compared with usual care (Control). DESIGN A follow-up of a parallel, 4-arm, single-blind, 2-y, randomized controlled trial in 802 women (86% European, 48% primiparous) recruited in pregnancy (58% response rate) was undertaken. All groups received standard Well-Child care with additional support for 3 intervention groups: FAB (promotion of breastfeeding, healthy eating, physical activity: 8 contacts, antenatal, 18 mo); Sleep (prevention of sleep problems: antenatal, 3 wk); Combination (both interventions). Follow-up measures were collected by staff blinded to group allocation. The primary outcome was child body mass index (BMI) z score, and secondary outcomes were prevalence of obesity (BMI ≥95th percentile), self-regulation (psychological measures), sleep, physical activity (accelerometry, questionnaires), and dietary intake (food-frequency questionnaire). Analyses were conducted through the use of multiple imputation. RESULTS Retention was 77% at age 3.5 y and 69% at age 5 y. Children in the FAB group had significantly higher BMI z scores than did Controls at age 5 y (adjusted difference: 0.25; 95% CI: 0.04, 0.47) but not at age 3.5 y (0.15; 95% CI: -0.04, 0.34). Children who received the Sleep intervention (Sleep and Combination groups) had significantly lower BMI z scores at age 3.5 y (-0.24; 95% CI: -0.38, -0.10) and at age 5 y (-0.23; 95% CI: -0.38, -0.07) than children who did not (Control and FAB groups). CONCLUSIONS A conventional intervention had unexpected adverse long-term weight outcomes, whereas positive outcomes from a less conventional sleep intervention remained promising at age 5 y. More intensive or extended sleep intervention might have larger or longer-lasting effects and should be investigated. This trial was registered at clinicaltrials.gov as NCT00892983.
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SunGold Kiwifruit Supplementation of Individuals with Prediabetes Alters Gut Microbiota and Improves Vitamin C Status, Anthropometric and Clinical Markers.
Wilson, R, Willis, J, Gearry, RB, Hughes, A, Lawley, B, Skidmore, P, Frampton, C, Fleming, E, Anderson, A, Jones, L, et al
Nutrients. 2018;10(7)
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Increased plasma glucose levels are linked with increased oxidative stress. An increase in the uptake of antioxidants such as vitamin C through diet has been demonstrated by several studies as contributing to the maintenance of normal glucose levels and reducing the risk factors for Type 2 diabetes. The aim of this study was to investigate the vitamin C status, anthropometric measurements and faecal microbiota of an individual on consumption of high vitamin C kiwi fruit for a period of 12 weeks. Baseline measures were compared at the end of 12 weeks resulting in significant increase in plasma vitamin C status (14 µmol/L, p < 0.001). Significant reduction in blood pressure measurement (4 mmHg, p = 0.029), reduction in waist- to- hip ratio and waist- circumference, decrease in blood glucose marker HbA1c (1 mmol/mol, p = 0.005) and increase in fasting glucose (0.1 mmol/L, p = 0.046) were also observed at the end of twelve weeks. Faecal microbiota composition showed an increase in the abundance of uncharacterised bacterial family. The authors concluded that these result were not sufficiently significant to draw conclusions and further studies with larger sample sizes are required to confirm the outcomes of this study.
Abstract
Kiwifruit are a nutrient dense food and an excellent source of vitamin C. Supplementation of the diet with kiwifruit enhances plasma vitamin C status and epidemiological studies have shown an association between vitamin C status and reduced insulin resistance and improved blood glucose control. In vitro experiments suggest that eating kiwifruit might induce changes to microbiota composition and function; however, human studies to confirm these findings are lacking. The aim of this study was to investigate the effect of consuming two SunGold kiwifruit per day over 12 weeks on vitamin C status, clinical and anthropometric measures and faecal microbiota composition in people with prediabetes. This pilot intervention trial compared baseline measurements with those following the intervention. Participants completed a physical activity questionnaire and a three-day estimated food diary at baseline and on completion of the trial. Venous blood samples were collected at each study visit (baseline, 6, 12 weeks) for determination of glycaemic indices, plasma vitamin C concentrations, hormones, lipid profiles and high-sensitivity C-reactive protein. Participants provided a faecal sample at each study visit. DNA was extracted from the faecal samples and a region of the 16S ribosomal RNA gene was amplified and sequenced to determine faecal microbiota composition. When week 12 measures were compared to baseline, results showed a significant increase in plasma vitamin C (14 µmol/L, p < 0.001). There was a significant reduction in both diastolic (4 mmHg, p = 0.029) and systolic (6 mmHg, p = 0.003) blood pressure and a significant reduction in waist circumference (3.1 cm, p = 0.001) and waist-to-hip ratio (0.01, p = 0.032). Results also showed a decrease in HbA1c (1 mmol/mol, p = 0.005) and an increase in fasting glucose (0.1 mmol/L, p = 0.046), however, these changes were small and were not clinically significant. Analysis of faecal microbiota composition showed an increase in the relative abundance of as yet uncultivated and therefore uncharacterised members of the bacterial family Coriobacteriaceae. Novel bacteriological investigations of Coriobacteriaceae are required to explain their functional relationship to kiwifruit polysaccharides and polyphenols.
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Mediation Analysis as a Means of Identifying Dietary Components That Differentially Affect the Fecal Microbiota of Infants Weaned by Modified Baby-Led and Traditional Approaches.
Leong, C, Haszard, JJ, Lawley, B, Otal, A, Taylor, RW, Szymlek-Gay, EA, Fleming, EA, Daniels, L, Fangupo, LJ, Tannock, GW, et al
Applied and environmental microbiology. 2018;(18)
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The introduction of "solids" (i.e., complementary foods) to the milk-only diet in early infancy affects the development of the gut microbiota. The aim of this study was to determine whether a "baby-led" approach to complementary feeding that encourages the early introduction of an adult-type diet results in alterations of the gut microbiota composition compared to traditional spoon-feeding. The Baby-Led Introduction to SolidS (BLISS) study randomized 206 infants to BLISS (a modified version of baby-led weaning [BLW], the introduction of solids at 6 months of age, followed by self-feeding of family foods) or control (traditional spoon-feeding of purées) groups. Fecal microbiotas and 3-day weighed-diet records were analyzed for a subset of 74 infants at 7 and 12 months of age. The composition of the microbiota was determined by sequencing of 16S rRNA genes amplified by PCR from bulk DNA extracted from feces. Diet records were used to estimate food and dietary fiber intake. Alpha diversity (number of operational taxonomic units [OTUs]) was significantly lower in BLISS infants at 12 months of age (difference [95% confidence interval {CI}] of 31 OTUs [3.4 to 58.5]; P = 0.028), and while there were no significant differences between control and BLISS infants in relative abundances of Bifidobacteriaceae, Enterobacteriaceae, Veillonellaceae, Bacteroidaceae, Erysipelotrichaceae, Lachnospiraceae, or Ruminococcaceae at 7 or 12 months of age, OTUs representing the genus Roseburia were less prevalent in BLISS microbiotas at 12 months. Mediation models demonstrated that the intake of "fruit and vegetables" and "dietary fiber" explained 29% and 25%, respectively, of the relationship between group (BLISS versus control) and alpha diversity.IMPORTANCE The introduction of solid foods (complementary feeding or weaning) to infants leads to more-complex compositions of microbial communities (microbiota or microbiome) in the gut. In baby-led weaning (BLW), infants are given only finger foods that they can pick up and feed themselves-there is no parental spoon-feeding of puréed baby foods-and infants are encouraged to eat family meals. BLW is a new approach to infant feeding that is increasing in popularity in the United States, New Zealand, the United Kingdom, and Canada. We used mediation modeling, commonly used in health research but not in microbiota studies until now, to identify particular dietary components that affected the development of the infant gut microbiota.
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Three-year follow-up of a randomised controlled trial to reduce excessive weight gain in the first two years of life: protocol for the POI follow-up study.
Taylor, RW, Heath, AL, Galland, BC, Cameron, SL, Lawrence, JA, Gray, AR, Tannock, GW, Lawley, B, Healey, D, Sayers, RM, et al
BMC public health. 2016;(1):771
Abstract
BACKGROUND The Prevention of Overweight in Infancy (POI) study was a four-arm randomised controlled trial (RCT) in 802 families which assessed whether additional education and support on sleep (Sleep group); food, physical activity and breastfeeding (FAB group); or both (Combination group), reduced excessive weight gain from birth to 2 years of age, compared to usual care (Control group). The study had high uptake at recruitment (58 %) and retention at 2 years (86 %). Although the FAB intervention produced no significant effect on BMI or weight status at 2 years, the odds of obesity were halved in those who received the sleep intervention, despite no apparent effect on sleep duration. We speculate that enhanced self-regulatory behaviours may exist in the Sleep group. Self-regulation was not measured in our initial intervention, but extensive measures have been included in this follow-up study. Thus, the overall aim of the POI follow-up is to determine the extent to which augmented parental support and education on infant sleep, feeding, diet, and physical activity in the first 2 years of life reduces BMI at 3.5 and 5 years of age, and to determine the role of self-regulation in any such relationship. METHODS/DESIGN We will contact all 802 families and seek renewed consent to participate in the follow-up study. The families have received no POI intervention since the RCT finished at 2 years of age. Follow-up data collection will occur when the children are aged 3.5 and 5 years (i.e. up to 3 years post-intervention). Outcomes of interest include child anthropometry, body composition (DXA scan), diet (validated food frequency questionnaire), physical activity (accelerometry), sleep (questionnaire and accelerometry), and self-regulation (questionnaires and neuropsychological assessment). DISCUSSION Our follow-up study has been designed primarily to enable us to determine whether the intriguing benefit of the sleep intervention suggested at 2 years of age remains as children approach school age. However, cohort analyses will also investigate how BMI, self-regulation, and sleep consolidation develop during the early years. This information will be valuable to researchers and policy makers progressing the field of early childhood obesity prevention. TRIAL REGISTRATION ClinicalTrials.gov number NCT00892983 .
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Treatment and secondary prevention effects of the probiotics Lactobacillus paracasei or Bifidobacterium lactis on early infant eczema: randomized controlled trial with follow-up until age 3 years.
Gore, C, Custovic, A, Tannock, GW, Munro, K, Kerry, G, Johnson, K, Peterson, C, Morris, J, Chaloner, C, Murray, CS, et al
Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology. 2012;(1):112-22
Abstract
BACKGROUND Allergic disease has been associated with altered intestinal microbiota. Therefore, probiotics have been suggested as a potential treatment for eczema. OBJECTIVE We investigated whether dietary supplementation of infants with eczema at age 3-6 months with Lactobacillus paracasei CNCM I-2116 or Bifidobacterium lactis CNCM I-3446 had a treatment effect or altered allergic disease progression. METHODS Primary outcome included eczema severity (SCORing Atopic Dermatitis, SCORAD) 3 months post-randomization. Secondary: SCORAD (other visits); infant dermatitis quality of life (IDQoL); gastrointestinal permeability; urinary eosinophilic protein X; allergen-sensitization; allergic symptoms (age 12, 18, 36 months). A total of 208 infants aged 3-6 months with physician-diagnosed eczema were recruited; 137/208 (SCORAD ≥ 10, consuming ≥ 200 mL standard formula/day) were randomized to daily supplements containing L. paracasei or B. lactis or placebo for a 3-month period, while receiving extensively hydrolysed whey-formula (dairy-free diet). There were two open observational groups, one group exclusively breastfed (n = 22) and the other, standard formula-fed (n = 49). TRIAL NUMBER ISRCTN41490500. RESULTS Eczema severity decreased significantly over time in all groups. No significant difference was observed between randomized groups after 12-week treatment-period (SCORAD-score pre-/post-intervention: B. lactis 25.9 [95% CI: 22.8-29.2] to 12.8 [9.4-16.6]; L. paracasei 25.4 [22.1-29] to 12.5 [9.2-16.4]; placebo 26.9 [23.4-30.6] to 11.8 [9.6-14.3]; P = 0.7). Results were similar when analysis was controlled for allergen-sensitization, or when only sensitized infants were analysed. No differences were found for secondary outcomes. No difference was observed in SCORAD-score between randomized and observational groups. CONCLUSION AND CLINICAL RELEVANCE We found no benefit from supplementation with B. lactis or L. paracasei in the treatment of eczema, when given as an adjunct to basic topical treatment, and no effect on the progression of allergic disease from age 1 to 3 years.