Alterations in the Gut (<i>Gallus gallus</i>) Microbiota Following the Consumption of Zinc Biofortified Wheat (<i>Triticum aestivum</i>)-Based Diet

Reed, Spenser; Knez, Marija; Uzan, Atara; Stangoulis, James; Glahn, Raymond P.; Koren, Omry; Tako, Elad

doi:10.1021/acs.jafc.8b01481

Cited by 58 publications

(77 citation statements)

References 66 publications

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“…Reed et al showed that broiler chickens that were fed a Zn-biofortified, wheat-based diet had increased microbial beta-diversity, with concomitant increases in beneficial short chain fatty acid-producing lactic acid bacteria--suggesting that this type of diet beneficially restructures the gut microbiota. 102 In line with our present study, 2 weeks of dietary supplementation with manganese was recently demonstrated to alleviate DSS-induced colitis in adult mice in the absence of changes in the gut microbiome. 107 It was recently reported that excess dietary Zn causes oxidative stress, enhances gut permeability, and modifies the microbiota in mouse pups.…”

supporting

confidence: 91%

“…99 Zinc's direct impact on the gut microbiota and subsequent host growth has been evaluated in several studies of young livestock animals (piglets, calves, and broiler chickens) that differed in their design (dose levels, measurement time points, etc) and methods. [100][101][102] Most studies have reported small, beneficial effects-suggesting that Zn may shape the intestinal microbiota. However, a consensus is currently lacking.…”

mentioning

confidence: 99%

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High‐dose dietary supplementation with zinc prevents gut inflammation: Investigation of the role of metallothioneins and beyond by transcriptomic and metagenomic studies

et al. 2020

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Although it is known that zinc has several beneficial roles in the context of gut inflammation, the underlying mechanisms have not been extensively characterized. Zinc (Zn) is known to be the primary physiological inducer of the expression of the metallothionein (MT) superfamily of small stress‐responsive proteins. The expression of MTs in various tissues is induced or enhanced (including the gastrointestinal tract (GIT)) by a variety of stimuli, including infection and inflammation. However, the MTs’ exact role in inflammation is still subject to debate. In order to establish whether or not MTs are the sole vectors in the Zn‐based modulation of intestinal inflammation, we used transcriptomic and metagenomic approaches to assess the potential effect of dietary Zn, the mechanisms underlying the MTs’ beneficial effects, and the induction of previously unidentified mediators. We found that the expression of endogenous MTs in the mouse GIT was stimulated by an optimized dietary supplementation with Zn. The protective effects of dietary supplementation with Zn were then evaluated in mouse models of chemically induced colitis. The potential contribution of MTs and other pathways was explored via transcriptomic analyses of the ileum and colon in Zn‐treated mice. The microbiota’s role was also assessed via fecal 16S rRNA sequencing. We found that high‐dose dietary supplementation with Zn induced the expression of MT‐encoding genes in the colon of healthy mice. We next demonstrated that the Zn diet significantly protected mice in the two models of induced colitis. When comparing Zn‐treated and control mice, various genes were found to be differentially expressed in the colon and the ileum. Finally, we found that Zn supplementation did not modify the overall structure of the fecal microbiota, with the exception of (i) a significant increase in endogenous Clostridiaceae, and (ii) some subtle but specific changes at the family and genus levels. Our results emphasize the beneficial effects of excess dietary Zn on the prevention of colitis and inflammatory events in mouse models. The main underlying mechanisms were driven by the multifaceted roles of MTs and the other potential molecular mediators highlighted by our transcriptomic analyses although we cannot rule out contributions by other factors from the host and/or the microbiota.

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confidence: 91%

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confidence: 99%

High‐dose dietary supplementation with zinc prevents gut inflammation: Investigation of the role of metallothioneins and beyond by transcriptomic and metagenomic studies

et al. 2020

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“…The 7.5% teff group demonstrated a significantly lower LA:DGLA ratio, signifying a relative increase in Zn status, compared to both control groups ( p < 0.05). We have previously demonstrated the LA:DGLA ratio as a novel physiological biomarker of zinc status [ 19 , 21 ].…”

Section: Resultsmentioning

confidence: 99%

“…Given the nutritional advantages of teff, especially its high concentration of trace minerals, it is important to evaluate other intrinsic factors that influence absorption and bioavailability. Therefore, using the validated, well-established Gallus gallus in vivo model [ 6 , 12 , 13 , 14 , 15 , 19 , 20 ], we sought to assess the effects of the intra-amniotic administration of teff seed extracts on serum and tissue Fe and Zn status, as well as on multiple parameters that influence trace mineral absorption and bioavailability, i.e., intrinsic phytate and polyphenolic concentration, enterocyte gene expression of various trace mineral dependent proteins, and brush border membrane morphology. Additionally, 16S rRNA gene sequencing of cecal contents was utilized to analyze potential alterations in intestinal microbiota structure and function from teff extracts.…”

Section: Introductionmentioning

confidence: 99%

Alterations in the Intestinal Morphology, Gut Microbiota, and Trace Mineral Status Following Intra-Amniotic Administration (Gallus gallus) of Teff (Eragrostis tef) Seed Extracts

et al. 2020

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The consumption of teff (Eragrostis tef), a gluten-free cereal grain, has increased due to its dense nutrient composition including complex carbohydrates, unsaturated fatty acids, trace minerals (especially Fe), and phytochemicals. This study utilized the clinically-validated Gallus gallus intra amniotic feeding model to assess the effects of intra-amniotic administration of teff extracts versus controls using seven groups: (1) non-injected; (2) 18Ω H2O injected; (3) 5% inulin; (4) teff extract 1%; (5) teff extract 2.5%; (6) teff extract 5%; and (7) teff extract 7.5%. The treatment groups were compared to each other and to controls. Our data demonstrated a significant improvement in hepatic iron (Fe) and zinc (Zn) concentration and LA:DGLA ratio without concomitant serum concentration changes, up-regulation of various Fe and Zn brush border membrane proteins, and beneficial morphological changes to duodenal villi and goblet cells. No significant taxonomic alterations were observed using 16S rRNA sequencing of the cecal microbiota. Several important bacterial metabolic pathways were differentially enriched in the teff group, likely due to teff’s high relative fiber concentration, demonstrating an important bacterial-host interaction that contributed to improvements in the physiological status of Fe and Zn. Therefore, teff appeared to represent a promising staple food crop and should be further evaluated.

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“…Total RNA extraction from duodenal and heart tissue (30 mg) using Qiagen RNeasy Mini Kit (RNeasy Mini Kit, Qiagen Inc., Valencia, CA, USA), cDNA synthesis and real time-polymerase chain reaction (RT-PCR) analysis were performed as previously described 38,81 with minor adjustments. In brief, the cycle product (Cp) of each gene (2020) 10:2297 | https://doi.org/10.1038/s41598-020-57598-3 www.nature.com/scientificreports www.nature.com/scientificreports/ was quantified using a seven-point standard curve in duplicate.…”

Section: Gene Expression Analysis (Tissue Harvesting Rna Isolation mentioning

confidence: 99%

Nicotianamine-chelated iron positively affects iron status, intestinal morphology and microbial populations in vivo (Gallus gallus)

Beasley

Johnson

Kolba

et al. 2020

Sci Rep

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Wheat flour iron (Fe) fortification is mandatory in 75 countries worldwide yet many Fe fortificants, such as Fe-ethylenediaminetetraacetate (EDTA), result in unwanted sensory properties and/or gastrointestinal dysfunction and dysbiosis. Nicotianamine (NA) is a natural chelator of Fe, zinc (Zn) and other metals in higher plants and NA-chelated Fe is highly bioavailable in vitro. In graminaceous plants NA serves as the biosynthetic precursor to 2′-deoxymugineic acid (DMA), a related Fe chelator and enhancer of Fe bioavailability, and increased NA/DMA biosynthesis has proved an effective Fe biofortification strategy in several cereal crops. Here we utilized the chicken (Gallus gallus) model to investigate impacts of NA-chelated Fe on Fe status and gastrointestinal health when delivered to chickens through intraamniotic administration (short-term exposure) or over a period of six weeks as part of a biofortified wheat diet containing increased NA, Fe, Zn and DMA (long-term exposure). Striking similarities in host Fe status, intestinal functionality and gut microbiome were observed between the short-term and long-term treatments, suggesting that the effects were largely if not entirely due to consumption of NA-chelated Fe. These results provide strong support for wheat with increased NA-chelated Fe as an effective biofortification strategy and uncover novel impacts of NAchelated Fe on gastrointestinal health and functionality. Iron (Fe) supplementation and fortification are the two most widely used strategies to combat human Fe deficiencies that affect over 2 billion people worldwide 1-3. Iron supplementation involves large dose delivery of highly absorbable (bioavailable) Fe to humans and is effective in treating severe cases of Fe deficiency anemia 2,4,5. Iron fortification involves low dose delivery of bioavailable Fe fortificants to food products during manufacture (or point-of-use) and is an effective population-based strategy to boost Fe intakes. Iron fortification of wheat flour is now mandatory in 75 countries worldwide (Flour Fortification Initiative; https://fortificationdata.org/), however, the tendency of Fe fortificants such as ferrous sulfate (FeSO 4) to oxidize and cause undesired organoleptic and sensory properties pose significant challenges 6,7. Almost 90% of countries utilize fortificants with poor bioavailability or fortify at sub-optimal concentrations, although recent evidence suggests that Fe fortification can effectively reduce symptoms of Fe-deficiency anemia when correctly implemented 8-10. Iron chelated by ethylenediaminetetraacetate (EDTA) is a commonly recommended fortificant for cereal flour to minimize sensory alterations while providing Fe in a bioavailable form 3,6,8,11,12. Fortificants that utilize micro-and/or nanoencapsulation can further improve bioavailability 12-14 although the cost of using appropriately chelated and/or encapsulated Fe fortificants ($2 USD per ton to fortify wheat flour with EDTA-chelated Fe alone), and the requirement for centralized cereal processing and indust...

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Alterations in the Gut (Gallus gallus) Microbiota Following the Consumption of Zinc Biofortified Wheat (Triticum aestivum)-Based Diet

Cited by 58 publications

References 66 publications

High‐dose dietary supplementation with zinc prevents gut inflammation: Investigation of the role of metallothioneins and beyond by transcriptomic and metagenomic studies

High‐dose dietary supplementation with zinc prevents gut inflammation: Investigation of the role of metallothioneins and beyond by transcriptomic and metagenomic studies

Alterations in the Intestinal Morphology, Gut Microbiota, and Trace Mineral Status Following Intra-Amniotic Administration (Gallus gallus) of Teff (Eragrostis tef) Seed Extracts

Nicotianamine-chelated iron positively affects iron status, intestinal morphology and microbial populations in vivo (Gallus gallus)

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