Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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Dietary fibre enrichment of supplemental feed modulates the development of the intestinal tract in suckling piglets
Hees, H.M.J. Van; Davids, M. ; Maes, D. ; Millet, S. ; Possemiers, S. ; Hartog, L.A. Den; Kempen, T.A.T.G. Van; Janssens, G.P.J. - \ 2019
Journal of Animal Science and Biotechnology 10 (2019)1. - ISSN 1674-9782
Dietary fibre - Gut maturation - Gut microbiota - Suckling piglets

Background: Commercial pre-weaning diets are formulated to be highly digestible and nutrient-dense and contain low levels of dietary fibre. In contrast, pigs in a natural setting are manipulating fibre-rich plant material from a young age. Moreover, dietary fibre affects gastrointestinal tract (GIT) development and health in older pigs. We hypothesised that supplemental diets that contain vegetal fibres are accelerating GIT development in suckling piglets in terms of size and functionality. From d 2 of life, sow-suckled piglets had access to a low fibre diet (CON), a diet with a fermentable long-chain arabinoxylan (lc-AXOS), a diet with a largely non-fermentable purified cellulose (CELL), or a diet containing both fibres. During the initial 2 weeks, the control diet was a high-density milk replacer, followed by a dry and highly digestible creep meal. Upon weaning at 25 d, 15 piglets from each treatment group, identified as eaters and originating from six or seven litters, were sacrificed for post-mortem examination of GIT morphology, small intestinal permeability and metabolic profile of the digesta. The microbiota composition of the mid-colon was evaluated in a sub-set of ten piglets. Results: No major statistical interactions between the fibre sources were observed. Piglets consumed the fibre-containing milk supplements and creep diets well. Stomach size and small intestinal permeability was not affected. Large intestinal fill was increased with lc-AXOS only, while relative large intestinal weight was increased with both fibre sources (P < 0.050). Also, CELL decreased ileal pH and tended to increase ileal DM content compared to CON (P < 0.050). Moreover, the concentration of volatile fatty acids was increased in the caecum (P < 0.100) and mid-colon (P < 0.050) by addition of CELL. lc-AXOS only stimulated caecal propionate (P < 0.050). The microbiota composition showed a high individual variation and limited dietary impact. Nonetheless, CELL induced minor shifts in specific genera, with notable reductions of Escherichia-Shigella. Conclusions: Adding dietary fibres to the supplemental diet of suckling piglets altered large intestinal morphology but not small intestinal permeability. Moreover, dietary fibre showed effects on fermentation and modest changes of microbial populations in the hindgut, with more prominent effects from the low-fermentable cellulose.

Using poly(β-hydroxybutyrate-β-hydroxyvalerate) as carbon source in biofloc-systems : Nitrogen dynamics and shift of Oreochromis niloticus gut microbiota
Liu, Gang ; Deng, Yale ; Verdegem, Marc ; Ye, Zhangying ; Zhu, Songming - \ 2019
Science of the Total Environment 694 (2019). - ISSN 0048-9697
Biodegradable polymers (BDPs) - Biofloc system - Carbohydrate - Gut microbiota - Nitrogen dynamic

Inorganic‑nitrogen removal is essential for the sustainable operation of aquaculture industry and also influences the health of aquatic animals, which may be accomplished by utilizing biofloc technology. In this paper, we studied the use of three different carbon sources 1) longan seed powder (LP), 2) Poly(β-hydroxybutyrate-β-hydroxyvalerate) (PHBV) and 3) synthesized PHBV and LP (PHBVL) in biofloc systems for 90 days to investigate the nitrogen dynamics and gut microbiota of Nile tilapia (Oreochromis niloticus). The PHBVL and PHBV groups had higher total inorganic‑nitrogen removal efficiencies (70.99 ± 19.45% and 63.54 ± 19.44%) than the LP group (35.02 ± 11.21%), which had an accumulation of nitrate. Meanwhile, the biofloc in PHBVL and PHBV group generally had a higher amino acid composition, particularly for methionine and lysine, but was not reflected in the tilapia muscle. High-throughput sequencing indicated that the different carbohydrates shaped different bacterial community compositions in the fish gut after exposure in the three environments for 90-day. These differences, which resulted in different gut digestive enzyme activities (amylase, lipase and trypsin), and growth performance, which the food conversion ratio in the PHBVL group was lower than LP and PHBV group, the final body weight in PHBVL group was average 4.33% and 3.65% bigger than in LP and PHBV group. Network analysis revealed that the keystone taxa (90.33%) were Proteobacteria, Chloroflexi, Actinobacteria, Planctomycetes, Verrucomicrobia and Bacteroidetes, which relative abundance varied in the fish gut in the three groups. The experiment verified the feasibility and advantage to use biodegradable polymers (BDPs) as carbohydrates for biofloc systems.

Legitimate and reliable determination of the age-related intestinal microbiome in young piglets; rectal swabs and fecal samples provide comparable insights
Choudhury, R. ; Middelkoop, A. ; Bolhuis, J.E. ; Kleerebezem, M. - \ 2019
Frontiers in Microbiology 10 (2019)AUG. - ISSN 1664-302X
Early life - Feces - Gut microbiota - Pig - Rectal swab

A prerequisite for reliable microbiota analysis is having an effective and consistent sampling method. Fecal sampling, commonly used to study the intestinal microbiome, might not be suitable in all situations, especially considering the potential difficulties in obtaining fresh feces from young animals. Indeed, this study shows that the success rate of collecting fecal samples from young piglets (<2 weeks of age) was very low. Therefore, we evaluated rectal swabs as an alternative sample type (to feces) for studying porcine microbiome development and performed a comparative analysis of microbiome composition obtained from fresh fecal samples and rectal swabs in 15 healthy piglets at seven (6 piglets) and 20 (9 piglets) days of age. Three samples (fresh feces, rectal swab before and after defecation) were collected from individual piglets and microbiome composition was assessed by 16S rRNA gene sequencing. The results demonstrated that rectal swabs and fecal samples provide similar microbiome composition profiles, with samples clustering predominantly by individual animal rather than sample type. Furthermore, regardless of the sample type, the biological interpretation with respect to microbiota colonization patterns associated with different ages (7 and 20 days) was found to be comparable. Independent of sample type, we observed age-related changes like increasing microbiota diversity and alterations in relative abundances of the phyla Firmicutes, Bacteroidetes, and Fusobacteria, which was also reflected in consistent family-and genus-level microbiota changes. This study establishes that rectal swabs are a suitable alternative sample type to study the porcine microbiome development in early life, when fecal sampling is challenging.

Propolis modulates the gut microbiota and improves the intestinal mucosal barrier function in diabetic rats
Xue, Meilan ; Liu, Ying ; Xu, Hongwei ; Zhou, Zhitong ; Ma, Yan ; Sun, Ting ; Liu, Man ; Zhang, Huaqi ; Liang, Hui - \ 2019
Biomedicine and Pharmacotherapy 118 (2019). - ISSN 0753-3322
16S rDNA high-throughput sequencing - Diabetes - Gut microbiota - Propolis - Short chain fatty acid

Objective: Diabetes mellitus is associated with gut microbiota disturbance and intestinal mucosal injuries. This study investigated the influence of propolis on the gut microbiota and intestinal mucosa in rats with diabetes. Methods: Sprague-Dawley (SD) rats were randomly assigned to the control group, model group, and three propolis groups (supplemented with 80, 160, and 240 mg/kg·bw propolis, respectively). A high-fat diet combined with a streptozotocin (STZ) abdominal injection were used to induce diabetes in the rats. After 4 weeks, the intestinal histopathological analysis of the ileum was observed by transmission electron microscopy. The fasting blood glucose (FBG), plasma insulin, glucose tolerance (OGTT) and glycosylated hemoglobin (HbA1c) levels were measured. The expression of tight junction (TJ) proteins in the ileum was measured using western blotting. The molecular ecology of the fecal gut microbiota was analyzed by 16S rDNA high-throughput sequencing. The contents of the short-chain fatty acids (SCFAs) in feces were measured using high-performance liquid chromatography (HPLC). Results: After propolis treatment, compared to the model group, FBG and HbA1c levels declined, while the glucose tolerance and insulin sensitivity index (ISI) increased. The levels of TJ proteins in the ileum increased in the propolis groups. The tight junctions and gap junctions of the intestinal epithelium were also improved in the propolis groups. The contents of the feces acetic acid, propionic acid and butyrate were increased in the propolis groups. 16S rDNA high-throughput sequencing revealed that the composition of the gut microbiota of rats in the propolis supplement group was significantly improved. Conclusions: Compared to the model group, propolis exerted hypoglycemic effects in diabetic rats, and it repaired intestinal mucosal damage, benefited the communities of the gut microbiota and increased SCFA levels in diabetic rats.

A specific synbiotic-containing amino acid-based formula restores gut microbiota in non-IgE mediated cow's milk allergic infants: A randomized controlled trial
Wopereis, Harm ; Ampting, Marleen T.J. Van; Cetinyurek-Yavuz, Aysun ; Slump, Rob ; Candy, David C.A. ; Butt, Assad M. ; Peroni, Diego G. ; Vandenplas, Yvan ; Fox, Adam T. ; Shah, Neil ; Roeselers, Guus ; Harthoorn, Lucien F. ; Michaelis, Louise J. ; Knol, Jan ; West, Christina E. - \ 2019
Clinical and Translational Allergy 9 (2019)1. - ISSN 2045-7022
Cow's milk allergy - Gut microbiota - Pediatrics - Prebiotics - Probiotics

Background: Altered gut microbiota is implicated in cow's milk allergy (CMA) and differs markedly from healthy, breastfed infants. Infants who suffer from severe CMA often rely on cow's milk protein avoidance and, when breastfeeding is not possible, on specialised infant formulas such as amino-acid based formulas (AAF). Herein, we report the effects of an AAF including specific synbiotics on oral and gastrointestinal microbiota of infants with non-IgE mediated CMA with reference to healthy, breastfed infants. Methods: In this prospective, randomized, double-blind controlled study, infants with suspected non-IgE mediated CMA received test or control formula. Test formula was AAF with synbiotics (prebiotic fructo-oligosaccharides and probiotic Bifidobacterium breve M-16V). Control formula was AAF without synbiotics. Healthy, breastfed infants were used as a separate reference group (HBR). Bacterial compositions of faecal and salivary samples were analysed by 16S rRNA-gene sequencing. Faecal analysis was complemented with the analysis of pH, short-chain fatty acids (SCFAs) and lactic acids. Results: The trial included 35 test subjects, 36 controls, and 51 HBR. The 16S rRNA-gene sequencing revealed moderate effects of test formula on oral microbiota. In contrast, the gut microbiota was substantially affected across time comparing test with control. In both groups bacterial diversity increased over time but was characterised by a more gradual increment in test compared to control. Compositionally this reflected an enhancement of Bifidobacterium spp. and Veillonella sp. in the test group. In contrast, the control-fed infants showed increased abundance of adult-like species, mainly within the Lachnospiraceae family, as well as within the Ruminococcus and Alistipes genus. The effects on Bifidobacterium spp. and Lachnospiraceae spp. were previously confirmed through enumeration by fluorescent in situ hybridization and were shown for test to approximate the proportions observed in the HBR. Additionally, microbial activity was affected as evidenced by an increase of l-lactate, a decrease of valerate, and reduced concentrations of branched-chain SCFAs in test versus control. Conclusions: The AAF including specific synbiotics effectively modulates the gut microbiota and its metabolic activity in non-IgE mediated CMA infants bringing it close to a healthy breastfed profile. Trial registration Registered on 1 May 2013 with Netherlands Trial Register Number NTR3979.

Effect of stock density on the microbial community in biofloc water and Pacific white shrimp (Litopenaeus vannamei) gut microbiota
Deng, Yale ; Xu, Xiangyang ; Yin, Xuwang ; Lu, Huifeng ; Chen, Guangshuo ; Yu, Jianhai ; Ruan, Yunjie - \ 2019
Applied Microbiology and Biotechnology 103 (2019)10. - ISSN 0175-7598 - p. 4241 - 4252.
Biofloc technology - Gut microbiota - Microbial community - Shrimp - Stock density

Biofloc technology is an efficient approach for intensive shrimp culture. However, the extent to which this process can influence the composition of intestinal microbial community is still unknown. Here, we surveyed the shrimp intestinal bacteria as well as the floc water from three biofloc systems with different stock densities. Our study revealed a similar variation trend in phylum taxonomy level between floc bacteria and gut microbiota. Microbial community varied notably in floc water from different stock densities, while a core genus with dominating relative abundance was detected in gut samples. Extensive variation was discovered in gut microbiota, but still clustered into groups according to stock density. Our results indicated that shrimp intestinal microbiota as well as bacteria aggregated in flocs assembled into distinct communities from different stock densities, and the intestinal communities were more similar with the surrounding environment as the increase of stock density and resulting high floc biomass. The high stock density changed the core gut microbiota by reducing the relative abundance of Paracoccus and increasing that of Nocardioides, which may negatively influence shrimp performance. Therefore, this study helps us to understand further bacteria and host interactions in biofloc system.

Degradation of fibres from fruit by-products allows selective modulation of the gut bacteria in an in vitro model of the proximal colon
Bussolo de Souza, Carlota ; Jonathan, Melliana ; Isay Saad, Susana Marta ; Schols, Henk A. ; Venema, Koen - \ 2019
Journal of Functional Foods 57 (2019). - ISSN 1756-4646 - p. 275 - 285.
Degradation - Fermentation - Fibre - Fruit by-products - Gut microbiota - SCFA

The potential prebiotic effect of fibres (alcohol insoluble solids fractions) from fruit by-products – orange bagasses and passion fruit peels – and their degradation by human gut microbiota was tested in an in vitro colon system. Standard medium and inulin were used as controls. Orange bagasses (A-OB1 and A-OB2) had similar chemical composition but differed regarding fermentation profile. A-OB2 resulted in a more diverse bacterial community than A-OB1 and produced more SCFA, with increased Ruminococcus and Lachnospira. Carbohydrate utilization was higher on A-OB2 probably due to higher ratio soluble to insoluble fibres. Isolated fibres from passion fruit peels presented similar chemical composition and fermentation profiling. Bacteroides and Ruminococcus were the main genera stimulated. Negligible lactate and succinate production represent slow fermentation, a protective feature against colon cancer. This study provided evidence that the tested fruit by-products have the potential to be used for selective modulation of the gut microbiota.

Biotechnology of health-promoting bacteria
Douillard, François P. ; Vos, Willem M. de - \ 2019
Biotechnology Advances 37 (2019)6. - ISSN 0734-9750
Applied genomics - Gut microbiota - Next-generation therapeutic bacteria - Probiotics

Over the last decade, there has been an increasing scientific and public interest in bacteria that may positively contribute to human gut health and well-being. This interest is reflected by the ever-increasing number of developed functional food products containing health-promoting bacteria and reaching the market place as well as by the growing revenue and profits of notably bacterial supplements worldwide. Traditionally, the origin of probiotic-marketed bacteria was limited to a rather small number of bacterial species that mostly belong to lactic acid bacteria and bifidobacteria. Intensifying research efforts on the human gut microbiome offered novel insights into the role of human gut microbiota in health and disease, while also providing a deep and increasingly comprehensive understanding of the bacterial communities present in this complex ecosystem and their interactions with the gut-liver-brain axis. This resulted in rational and systematic approaches to select novel health-promoting bacteria or to engineer existing bacteria with enhanced probiotic properties. In parallel, the field of gut microbiomics developed into a fertile framework for the identification, isolation and characterization of a phylogenetically diverse array of health-promoting bacterial species, also called next-generation therapeutic bacteria. The present review will address these developments with specific attention for the selection and improvement of a selected number of health-promoting bacterial species and strains that are extensively studied or hold promise for future food or pharma product development.

A specific synbiotic-containing amino acid-based formula in dietary management of cow's milk allergy : A randomized controlled trial
Fox, Adam T. ; Wopereis, Harm ; Ampting, Marleen T.J. van; Oude Nijhuis, Manon M. ; Butt, Assad M. ; Peroni, Diego G. ; Vandenplas, Yvan ; Candy, David C.A. ; Shah, Neil ; West, Christina E. ; Garssen, Johan ; Harthoorn, Lucien F. ; Knol, Jan ; Michaelis, Louise J. - \ 2019
Clinical and Translational Allergy 9 (2019)1. - ISSN 2045-7022
Bifidobacterium breve M-16V - Cow's milk allergy - Gut microbiota - Prebiotic - Probiotic - Symptoms

Background: Here we report follow-up data from a double-blind, randomized, controlled multicenter trial, which investigated fecal microbiota changes with a new amino acid-based formula (AAF) including synbiotics in infants with non-immunoglobulin E (IgE)-mediated cow's milk allergy (CMA). Methods: Subjects were randomized to receive test product (AAF including fructo-oligosaccharides and Bifidobacterium breve M-16V) or control product (AAF) for 8 weeks, after which infants could continue study product until 26 weeks. Fecal percentages of bifidobacteria and Eubacterium rectale/Clostridium coccoides group (ER/CC) were assessed at 0, 8, 12, and 26 weeks. Additional endpoints included stool markers of gut immune status, clinical symptoms, and safety assessments including adverse events and medication use. Results: The trial included 35 test subjects, 36 controls, and 51 in the healthy reference group. Study product was continued by 86% and 92% of test and control subjects between week 8-12, and by 71% and 80%, respectively until week 26. At week 26 median percentages of bifidobacteria were significantly higher in test than control [47.0% vs. 11.8% (p < 0.001)], whereas percentages of ER/CC were significantly lower [(13.7% vs. 23.6% (p = 0.003)]. Safety parameters were similar between groups. Interestingly use of dermatological medication and reported ear infections were lower in test versus control, p = 0.019 and 0.011, respectively. Baseline clinical symptoms and stool markers were mild (but persistent) and low, respectively. Symptoms reduced towards lowest score in both groups. Conclusion: Beneficial effects of this AAF including specific synbiotics on microbiota composition were observed over 26 weeks, and shown suitable for dietary management of infants with non-IgE-mediated CMA.

A synbiotic mixture of scGOS/lcFOS and Bifidobacterium breve M-16V increases faecal Bifidobacterium in healthy young children
Kosuwon, P. ; Lao-Araya, M. ; Uthaisangsook, S. ; Lay, C. ; Bindels, J. ; Knol, J. ; Chatchatee, P. - \ 2018
Beneficial Microbes 9 (2018)4. - ISSN 1876-2883 - p. 541 - 552.
Bifidobacterium - Gut microbiota - Healthy toddlers - Stool consistency - Synbiotic

Little is known about the impact of nutrition on toddler gut microbiota. The plasticity of the toddler gut microbiota indicates that nutritional modulation beyond infancy could potentially impact its maturation. The objective of this study was to determine the effect of consuming Young Child Formula (YCF) supplemented with short chain galactooligosaccharides and long chain fructooligosaccharides (scGOS/lcFOS, ratio 9:1) and Bifidobacterium breve M-16V on the development of the faecal microbiota in healthy toddlers. A cohort of 129 Thai children aged 1-3 years were included in a randomised controlled clinical study. The children were assigned to receive either YCF with 0.95 g/100 ml of scGOS/lcFOS and 1.8×107 cfu/g of B. breve M-16V (Active-YCF) or Control-YCF for 12 weeks. The composition and metabolic activity of the faecal microbiota, and the level of secretory immunoglobulin A were determined in the stool samples. The consumption of Active-YCF increased the proportion of Bifidobacterium (mean 27.3% at baseline to 33.3%, at week 12, P=0.012) with a difference in change from baseline at week 12 between the Active and Control of 7.48% (P=0.030). The consumption of Active-YCF was accompanied with a more acidic intestinal milieu compared to the Control-YCF. The pH value decreased statistically significantly in the Active-YCF group from a median of 7.05 at baseline to 6.79 at week 12 (P < 0.001). The consumption of Active-YCF was associated with a softer pudding-like stool consistency compared to the Control-YCF. At week 6 and week 12, the betweengroup difference in stool consistency was statistically significant (P=0.004 and P < 0.001, respectively). A Young Child Formula supplemented with scGOS/lcFOS and B. breve M-16V positively influences the development of the faecal microbiota in healthy toddlers by supporting higher levels of Bifidobacterium. The synbiotic supplementation is also accompanied with a more acidic intestinal milieu and softer stools.

Flux, impact, and fate of halogenated xenobiotic compounds in the gut
Atashgahi, Siavash ; Shetty, Sudarshan A. ; Smidt, Hauke ; Vos, Willem M. de - \ 2018
Frontiers in Physiology 9 (2018)JUL. - ISSN 1664-042X
Dehalogenation genes - Gut microbiota - Halogenated compounds - Metagenomics - Xenobiotic-microbiota interaction - Xenobiotics

Humans and their associated microbiomes are exposed to numerous xenobiotics through drugs, dietary components, personal care products as well as environmental chemicals. Most of the reciprocal interactions between the microbiota and xenobiotics, such as halogenated compounds, occur within the human gut harboring diverse and dense microbial communities. Here, we provide an overview of the flux of halogenated compounds in the environment, and diverse exposure routes of human microbiota to these compounds. Subsequently, we review the impact of halogenated compounds in perturbing the structure and function of gut microbiota and host cells. In turn, cultivation-dependent and metagenomic surveys of dehalogenating genes revealed the potential of the gut microbiota to chemically alter halogenated xenobiotics and impact their fate. Finally, we provide an outlook for future research to draw attention and attract interest to study the bidirectional impact of halogenated and other xenobiotic compounds and the gut microbiota.

Effects of different solid carbon sources on water quality, biofloc quality and gut microbiota of Nile tilapia (Oreochromis niloticus) larvae
Li, Jiawei ; Liu, Gang ; Li, Changwei ; Deng, Yale ; Tadda, Musa Abubakar ; Lan, Lihua ; Zhu, Songming ; Liu, Dezhao - \ 2018
Aquaculture 495 (2018). - ISSN 0044-8486 - p. 919 - 931.
Biofloc technology - Gut microbiota - Solid carbon source - Water quality

External carbon source is needed for biofloc system to maintain an optimal C/N ratio for the growth of bacteria biomass. In this study, three solid-phase biodegradable compounds, including Longan powder (LP), polyhydroxybutyrate-hydroxyvalerate/LP (PHBVL) and Poly(butylene succinate)/LP (PBSL), were utilized to feed biofloc-based aquaculture systems in triplicates for nine Nile tilapia (Oreochromis niloticus) larvae culture tanks. LP was applied in the in-situ biofloc system as a “control group” (3 tanks), while PHBVL and PBSL were used in the ex-situ biofloc systems (6 tanks). During the 120-days experiment, the C/N ratio was maintained at 24.87 ± 5.66, 22.93 ± 3.20 and 23.12 ± 3.54 for the LP, PHBVL and PBSL groups, respectively. There were no significant differences (P >.05) of the averaged total ammonia nitrogen (TAN) concentration among the LP, PHBVL and PBSL groups (1.10 ± 1.18, 0.67 ± 0.38 and 1.18 ± 1.40 mg L−1). Significant differences of the averaged NO2 -N concentrations (0.26 ± 0.38, 0.01 ± 0.01 and 0.08 ± 0.12 mg L−1) were detected among the LP, PHBVL and PBSL groups (P <.05). The accumulation of NO3 -N in LP group (>40 mg L−1 on day 120) was significantly higher than that of PHBVL and PBSL groups (about 2–3 mg L−1 on day 120) (P <.05). To characterize the quality of biofloc, the median diameters (D50) and essential amino acids index (EAAI) were measured for three treatments. The D50 (124.7 ± 4.24, 131.6 ± 2.83 and 175.5 ± 9.19 μm) and EAAI (0.969 ± 0.011, 1.007 ± 0.014 and 0.995 ± 0.012) showed that the high quality bioflocs in the LP, PHBVL and PBSL groups could meet the requirement for feeding the aquatic animals. In addition, high throughput sequencing test showed that solid carbon source not only had a significant effect on the microbial community in bioflocs, but also on the composition of fish gut microbiota. Bacillus was the dominating genus discovered in all treatments (48.34% in LP, 49.24% in PHBVL and 50.47% in PBSL) by 16S rRNA sequencing. Overall, blending LP with biodegradable polymers as carbon source showed significantly higher removal efficiency of nitrate and nitrite nitrogen, and higher biofloc quality than using LP as the only carbon source. How exactly various solid carbon sources influence fish growth performance and health need further study.

Integrative analysis of gut microbiota composition, host colonic gene expression and intraluminal metabolites in aging C57BL/6J mice
Lugt, Benthe van der; Rusli, Fenni ; Lute, Carolien ; Lamprakis, Andreas ; Salazar, Ethel ; Boekschoten, Mark V. ; Hooiveld, Guido J. ; Müller, Michael ; Vervoort, Jacques ; Kersten, Sander ; Belzer, Clara ; Kok, Dieuwertje E.G. ; Steegenga, Wilma T. - \ 2018
Aging-US 10 (2018)5. - ISSN 1945-4589 - p. 930 - 950.
Aging - Colonic gene expression - Gut microbiota - Host-microbe interactions - Metabolites

The aging process is associated with diminished colonic health. In this study, we applied an integrative approach to reveal potential interactions between determinants of colonic health in aging C57BL/6J mice. Analysis of gut microbiota composition revealed an enrichment of various potential pathobionts, including Desulfovibrio spp., and a decline of the health-promoting Akkermansia spp. and Lactobacillus spp. during aging. Intraluminal concentrations of various metabolites varied between ages and we found evidence for an increased gut permeability at higher age. Colonic gene expression analysis suggested that during the early phase of aging (between 6 and 12 months), expression of genes involved in epithelial-to-mesenchymal transition and (re)organization of the extracellular matrix were increased. Differential expression of these genes was strongly correlated with Bifidobacterium spp. During the later phase of aging (between 12 and 28 months), gene expression profiles pointed towards a diminished antimicrobial defense and were correlated with an uncultured Gastranaerophilales spp. This study demonstrates that aging is associated with pronounced changes in gut microbiota composition and colonic gene expression. Furthermore, the strong correlations between specific bacterial genera and host gene expression may imply that orchestrated interactions take place in the vicinity of the colonic wall and potentially mediate colonic health during aging.

Loss of angiopoietin-like 4 (ANGPTL4) in mice with diet-induced obesity uncouples visceral obesity from glucose intolerance partly via the gut microbiota
Janssen, Aafke W.F. ; Katiraei, Saeed ; Bartosinska, Barbara ; Eberhard, Daniel ; Willems van Dijk, Ko ; Kersten, Sander - \ 2018
Diabetologia 61 (2018)6. - ISSN 0012-186X - p. 1447 - 1458.
Angiopoietin-like 4 - Antibiotics - Glucose tolerance - Gut microbiota - Insulin secretion - White adipose tissue
Aims/hypothesis: Angiopoietin-like 4 (ANGPTL4) is an important regulator of triacylglycerol metabolism, carrying out this role by inhibiting the enzymes lipoprotein lipase and pancreatic lipase. ANGPTL4 is a potential target for ameliorating cardiometabolic diseases. Although ANGPTL4 has been implicated in obesity, the study of the direct role of ANGPTL4 in diet-induced obesity and related metabolic dysfunction is hampered by the massive acute-phase response and development of lethal chylous ascites and peritonitis in Angptl4−/− mice fed a standard high-fat diet. The aim of this study was to better characterise the role of ANGPTL4 in glucose homeostasis and metabolic dysfunction during obesity. Methods: We chronically fed wild-type (WT) and Angptl4−/− mice a diet rich in unsaturated fatty acids and cholesterol, combined with fructose in drinking water, and studied metabolic function. The role of the gut microbiota was investigated by orally administering a mixture of antibiotics (ampicillin, neomycin, metronidazole). Glucose homeostasis was assessed via i.p. glucose and insulin tolerance tests. Results: Mice lacking ANGPTL4 displayed an increase in body weight gain, visceral adipose tissue mass, visceral adipose tissue lipoprotein lipase activity and visceral adipose tissue inflammation compared with WT mice. However, they also unexpectedly had markedly improved glucose tolerance, which was accompanied by elevated insulin levels. Loss of ANGPTL4 did not affect glucose-stimulated insulin secretion in isolated pancreatic islets. Since the gut microbiota have been suggested to influence insulin secretion, and because ANGPTL4 has been proposed to link the gut microbiota to host metabolism, we hypothesised a potential role of the gut microbiota. Gut microbiota composition was significantly different between Angptl4−/− mice and WT mice. Interestingly, suppression of the gut microbiota using antibiotics largely abolished the differences in glucose tolerance and insulin levels between WT and Angptl4−/− mice. Conclusions/interpretation: Despite increasing visceral fat mass, inactivation of ANGPTL4 improves glucose tolerance, at least partly via a gut microbiota-dependent mechanism.
Lifelong calorie restriction affects indicators of colonic health in aging C57Bl/6J mice
Kok, Dieuwertje E.G. ; Rusli, Fenni ; Lugt, Benthe van der; Lute, Carolien ; Laghi, Luca ; Salvioli, Stefano ; Picone, Gianfranco ; Franceschi, Claudio ; Smidt, Hauke ; Vervoort, Jacques ; Kampman, Ellen ; Müller, Michael ; Steegenga, Wilma T. - \ 2018
Journal of Nutritional Biochemistry 56 (2018). - ISSN 0955-2863 - p. 152 - 164.
Aging - Calorie restriction - Colonic health - Gene expression - Gut microbiota - Metabolites
Diminished colonic health is associated with various age-related pathologies. Calorie restriction (CR) is an effective strategy to increase healthy lifespan, although underlying mechanisms are not fully elucidated. Here, we report the effects of lifelong CR on indicators of colonic health in aging C57Bl/6J mice. Compared to an ad libitum control and moderate-fat diet, 30% energy reduction was associated with attenuated immune- and inflammation-related gene expression in the colon. Furthermore, expression of genes involved in lipid metabolism was higher upon CR, which may point towards efficient regulation of energy metabolism. The relative abundance of bacteria considered beneficial to colonic health, such as Bifidobacterium and Lactobacillus, increased in the mice exposed to CR for 28 months as compared to the other diet groups. We found lower plasma levels of interleukin-6 and lower levels of various metabolites, among which are bile acids, in the colonic luminal content of CR-exposed mice as compared to the other diet groups. Switching from CR to an ad libitum moderate-fat diet at old age (24 months) revealed remarkable phenotypic plasticity in terms of gene expression, microbiota composition and metabolite levels, although expression of a subset of genes remained CR-associated. This study demonstrated in a comprehensive way that CR affects indicators of colonic health in aging mice. Our findings provide unique leads for further studies that need to address optimal and feasible strategies for prolonged energy deprivation, which may contribute to healthy aging.
Host and environmental factors affecting the intestinal microbiota in chickens
Kers, Jannigje G. ; Velkers, Francisca C. ; Fischer, Egil A.J. ; Hermes, Gerben D.A. ; Stegeman, J.A. ; Smidt, Hauke - \ 2018
Frontiers in Microbiology 9 (2018)FEB. - ISSN 1664-302X
16S rRNA - Confounding factors - Gut health - Gut microbiota - Microbiome - Poultry
The initial development of intestinal microbiota in poultry plays an important role in production performance, overall health and resistance against microbial infections. Multiplexed sequencing of 16S ribosomal RNA gene amplicons is often used in studies, such as feed intervention or antimicrobial drug trials, to determine corresponding effects on the composition of intestinal microbiota. However, considerable variation of intestinal microbiota composition has been observed both within and across studies. Such variation may in part be attributed to technical factors, such as sampling procedures, sample storage, DNA extraction, the choice of PCR primers and corresponding region to be sequenced, and the sequencing platforms used. Furthermore, part of this variation in microbiota composition may also be explained by different host characteristics and environmental factors. To facilitate the improvement of design, reproducibility and interpretation of poultry microbiota studies, we have reviewed the literature on confounding factors influencing the observed intestinal microbiota in chickens. First, it has been identified that host-related factors, such as age, sex, and breed, have a large effect on intestinal microbiota. The diversity of chicken intestinal microbiota tends to increase most during the first weeks of life, and corresponding colonization patterns seem to differ between layer- and meat-type chickens. Second, it has been found that environmental factors, such as biosecurity level, housing, litter, feed access and climate also have an effect on the composition of the intestinal microbiota. As microbiota studies have to deal with many of these unknown or hidden host and environmental variables, the choice of study designs can have a great impact on study outcomes and interpretation of the data. Providing details on a broad range of host and environmental factors in articles and sequence data repositories is highly recommended. This creates opportunities to combine data from different studies for meta-analysis, which will facilitate scientific breakthroughs toward nutritional and husbandry associated strategies to improve animal health and performance.
The first microbial colonizers of the human gut : Composition, activities, and health implications of the infant gut microbiota
Milani, Christian ; Duranti, Sabrina ; Bottacini, Francesca ; Casey, Eoghan ; Turroni, Francesca ; Mahony, Jennifer ; Belzer, Clara ; Palacio, Susana Delgado ; Montes, Silvia Arboleya ; Mancabelli, Leonardo ; Lugli, Gabriele Andrea ; Rodriguez, Juan Miguel ; Bode, Lars ; Vos, Willem De; Gueimonde, Miguel ; Margolles, Abelardo ; Sinderen, Douwe Van; Ventura, Marco - \ 2017
Microbiology and Molecular Biology Reviews 81 (2017)4. - ISSN 1092-2172
Bifidobacteria - Gut commensals - Gut microbiota - Infants - Metagenomics - Microbiome - Microbiota - Probiotics - Virome
The human gut microbiota is engaged in multiple interactions affecting host health during the host's entire life span. Microbes colonize the neonatal gut immediately following birth. The establishment and interactive development of this early gut microbiota are believed to be (at least partially) driven and modulated by specific compounds present in human milk. It has been shown that certain genomes of infant gut commensals, in particular those of bifidobacterial species, are genetically adapted to utilize specific glycans of this human secretory fluid, thus representing a very intriguing example of host-microbe coevolution, where both partners are believed to benefit. In recent years, various metagenomic studies have tried to dissect the composition and functionality of the infant gut microbiome and to explore the distribution across the different ecological niches of the infant gut biogeography of the corresponding microbial consortia, including those corresponding to bacteria and viruses, in healthy and ill subjects. Such analyses have linked certain features of the microbiota/microbiome, such as reduced diversity or aberrant composition, to intestinal illnesses in infants or disease states that are manifested at later stages of life, including asthma, inflammatory bowel disease, and metabolic disorders. Thus, a growing number of studies have reported on how the early human gut microbiota composition/development may affect risk factors related to adult health conditions. This concept has fueled the development of strategies to shape the infant microbiota composition based on various functional food products. In this review, we describe the infant microbiota, the mechanisms that drive its establishment and composition, and how microbial consortia may be molded by natural or artificial interventions. Finally, we discuss the relevance of key microbial players of the infant gut microbiota, in particular bifidobacteria, with respect to their role in health and disease.
The effect of fiber and prebiotics on children’s gastrointestinal disorders and microbiome
Wegh, Carrie A.M. ; Schoterman, Margriet H.C. ; Vaughan, Elaine E. ; Belzer, Clara ; Benninga, Marc A. - \ 2017
Expert Review of Gastroenterology and Hepatology 11 (2017)11. - ISSN 1747-4124 - p. 1031 - 1045.
children - dietary fiber - functional gastrointestinal disorders - Gut microbiota - oligosaccharides - prebiotics

Introduction: The bacteria received upon birth are the start of colonization of the approximately 1014 bacteria that are present in the mature human gastrointestinal tract, better known as the microbiota. The gut microbiota is implicated in gastrointestinal health, nutrient metabolism and benefits such as prevention of infection. Dietary fiber, including prebiotics, escape digestion in the small intestine and reach the colon intact, where they are partially or completely fermented by the gut microbiota. Areas covered: The possible interactions between dietary fiber, prebiotics and microbiota are discussed as well as how this relates to functional gastrointestinal disorders. During the first years of life the microbiota have not yet reached a stable state and is sensitive to disturbance by environmental factors. An imbalance in the microbiota early in life is found to be associated with several functional gastrointestinal disorders such as colic, functional abdominal pain, irritable bowel syndrome and constipation. Expert commentary: A better understanding of how gut microbial changes in early-life can impact gastrointestinal health might lead to new treatments or disease prevention. Nutritional strategies with fiber or prebiotics may support health due to modification of colonic microbiota composition and metabolic activity, for example by growth stimulation of Bifidobacterium and Lactobacillus.

Genome-scale model and omics analysis of metabolic capacities of Akkermansia muciniphila reveal a preferential mucin-degrading lifestyle
Ottman, Noora ; Davids, Mark ; Suarez-Diez, Maria ; Boeren, Sjef ; Schaap, Peter J. ; Martins dos Santos, Vitor ; Smidt, Hauke ; Belzer, Clara ; Vos, Willem M. de - \ 2017
Applied and Environmental Microbiology 83 (2017)18. - ISSN 0099-2240
Acetate - Akkermansia - Gut microbiota - Metabolic modeling - Mucin - Propionate - Proteomics - Transcriptomics
The composition and activity of the microbiota in the human gastrointestinal tract are primarily shaped by nutrients derived from either food or the host. Bacteria colonizing the mucus layer have evolved to use mucin as a carbon and energy source. One of the members of the mucosa-associated microbiota is Akkermansia muciniphila, which is capable of producing an extensive repertoire of mucindegrading enzymes. To further study the substrate utilization abilities of A. muciniphila, we constructed a genome-scale metabolic model to test amino acid auxotrophy, vitamin biosynthesis, and sugar-degrading capacities. The model-supported predictions were validated by in vitro experiments, which showed A. muciniphila to be able to utilize the mucin-derived monosaccharides fucose, galactose, and N-acetylglucosamine. Growth was also observed on N-acetylgalactosamine, even though the metabolic model did not predict this. The uptake of these sugars, as well as the nonmucin sugar glucose, was enhanced in the presence of mucin, indicating that additional mucin-derived components are needed for optimal growth. An analysis of whole-transcriptome sequencing (RNA-Seq) comparing the gene expression of A. muciniphila grown on mucin with that of the same bacterium grown on glucose confirmed the activity of the genes involved in mucin degradation and revealed most of these to be upregulated in the presence of mucin. The transcriptional response was confirmed by a proteome analysis, altogether revealing a hierarchy in the use of sugars and reflecting the adaptation of A. muciniphila to the mucosal environment. In conclusion, these findings provide molecular insights into the lifestyle of A. muciniphila and further confirm its role as a mucin specialist in the gut.
Immunomodulating effects of probiotics for microbiota modulation, gut health and disease resistance in pigs
Roselli, Marianna ; Pieper, Robert ; Rogel-Gaillard, Claire ; Vries, Hugo de; Bailey, Mick ; Smidt, Hauke ; Lauridsen, Charlotte - \ 2017
Animal Feed Science and Technology 233 (2017). - ISSN 0377-8401 - p. 104 - 119.
Gut health - Gut microbiota - Immunomodulation - Pig diarrhea prevention - Prebiotics - Probiotics
Probiotics are live microorganisms that can confer a health benefit on the host, and amongst various mechanisms probiotics are believed to exert their effects by production of antimicrobial substances, competition with pathogens for adhesion sites and nutrients, enhancement of mucosal barrier integrity and immune modulation. Through these activities probiotics can support three core benefits for the host: supporting a healthy gut microbiota, a healthy digestive tract and a healthy immune system. More recently, the concept of combining probiotics and prebiotics, i.e. synbiotics, for the beneficial effect on gut health of pigs has attracted major interest, and examples of probiotic and prebiotic benefits for pigs are pathogen inhibition and immunomodulation. Yet, it remains to be defined in pigs, what exactly is a healthy gut. Because of the high level of variability in growth and feed conversion between individual pigs in commercial production systems, measuring the impact of probiotics on gut health defined by improvements in overall productivity requires large experiments. For this reason, many studies have concentrated on measuring the effects of the feed additives on proxies of gut health including many immunological measures, in more controlled experiments. With the major focus of studying the balance between gut microbiology, immunology and physiology, and the potential for prevention of intestinal disorders in pigs, we therefore performed a literature review of the immunomodulatory effects of probiotics, either alone or in combination with prebiotics, based on in vivo, in vitro and ex vivo porcine experiments. A consistent number of studies showed the potential capacity in terms of immunomodulatory activities of these feed additives in pigs, but contrasting results can also be obtained from the literature. Reasons for this are not clear but could be related to differences with respect to the probiotic strain used, experimental settings, diets, initial microbiota colonization, administration route, time and frequency of administration of the probiotic strain and sampling for analysis. Hence, the use of proxy measurements of enteric health based on observable immunological parameters presents significant problems at the moment, and cannot be considered robust, reliable predictors of the probiotic activity in vivo, in relation to pig gut health. In conclusion, more detailed understanding of how to select and interpret these proxy measurements will be necessary in order to allow a more rational prediction of the effect of specific probiotic interventions in the future.
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