The Food Additive Xanthan Gum Drives Adaptation of the Human Gut Microbiota

SummaryThe diets of industrialized countries reflect the increasing use of processed foods, often with the introduction of novel food additives. Xanthan gum is a complex polysaccharide with unique rheological properties that have established its use as a widespread stabilizer and thickening agent1. However, little is known about its direct interaction with the gut microbiota, which plays a central role in digestion of other, chemically-distinct dietary fiber polysaccharides. Here, we show that the ability to digest xanthan gum is surprisingly common in industrialized human gut microbiomes and appears to be contingent on the activity of a single bacterium that is a member of an uncultured bacterial genus in the family Ruminococcaceae. We used a combination of enrichment culture, multi-omics, and recombinant enzyme studies to identify and characterize a complete pathway in this uncultured bacterium for the degradation of xanthan gum. Our data reveal that this keystone degrader cleaves the xanthan gum backbone with a novel glycoside hydrolase family 5 (GH5) enzyme before processing the released oligosaccharides using additional enzymes. Surprisingly, some individuals harbor a Bacteroides species that is capable of consuming oligosaccharide products generated by the keystone Ruminococcaceae or a purified form of the GH5 enzyme. This Bacteroides symbiont is equipped with its own distinct enzymatic pathway to cross-feed on xanthan gum breakdown products, which still harbor the native linkage complexity in xanthan gum, but it cannot directly degrade the high molecular weight polymer. Thus, the introduction of a common food additive into the human diet in the past 50 years has promoted the establishment of a food chain involving at least two members of different phyla of gut bacteria.

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The Food Additive Xanthan Gum Drives Adaptation of the Human Gut Microbiota

10.21203/rs.3.rs-607163/v1 ◽

2021 ◽

Author(s):

Eric Martens ◽

Matthew Ostrowski ◽

Sabina La Rosa ◽

Benoit Kunath ◽

Andrew Robertson ◽

...

Keyword(s):

Gut Microbiota ◽

Xanthan Gum ◽

Enrichment Culture ◽

Food Additives ◽

Food Additive ◽

Glycoside Hydrolase Family ◽

Human Gut ◽

High Molecular Weight Polymer ◽

Molecular Weight Polymer ◽

Uncultured Bacterium

Abstract The diets of industrialized countries reflect the increasing use of processed foods, often with the introduction of novel food additives. Xanthan gum is a complex polysaccharide with unique rheological properties that have established its use as a widespread stabilizer and thickening agent1. However, little is known about its direct interaction with the gut microbiota, which plays a central role in digestion of other, chemically-distinct dietary fiber polysaccharides. Here, we show that the ability to digest xanthan gum is surprisingly common in industrialized human gut microbiomes and appears to be contingent on the activity of a single bacterium that is a member of an uncultured bacterial genus in the family Ruminococcaceae. We used a combination of enrichment culture, multi-omics, and recombinant enzyme studies to identify and characterize a complete pathway in this uncultured bacterium for the degradation of xanthan gum. Our data reveal that this keystone degrader cleaves the xanthan gum backbone with a novel glycoside hydrolase family 5 (GH5) enzyme before processing the released oligosaccharides using additional enzymes. Surprisingly, some individuals harbor a Bacteroides species that is capable of consuming oligosaccharide products generated by the keystone Ruminococcaceae or a purified form of the GH5 enzyme. This Bacteroides symbiont is equipped with its own distinct enzymatic pathway to cross-feed on xanthan gum breakdown products, which still harbor the native linkage complexity in xanthan gum, but it cannot directly degrade the high molecular weight polymer. Thus, the introduction of a common food additive into the human diet in the past 50 years has promoted the establishment of a food chain involving at least two members of different phyla of gut bacteria.

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Adaptation of Syntenic Xyloglucan Utilization Loci of Human Gut Bacteroidetes to Polysaccharide Side Chain Diversity

Applied and Environmental Microbiology ◽

10.1128/aem.01491-19 ◽

2019 ◽

Vol 85 (20) ◽

Cited By ~ 6

Author(s):

Guillaume Déjean ◽

Alexandra S. Tauzin ◽

Stuart W. Bennett ◽

A. Louise Creagh ◽

Harry Brumer

Keyword(s):

Gut Microbiota ◽

Community Dynamics ◽

Gene Clusters ◽

Individual Species ◽

Glycoside Hydrolase Family ◽

Backbone Cleavage ◽

Structural Variations ◽

Human Gut ◽

Complex Carbohydrates

ABSTRACT Genome sequencing has revealed substantial variation in the predicted abilities of individual species within animal gut microbiota to metabolize the complex carbohydrates comprising dietary fiber. At the same time, a currently limited body of functional studies precludes a richer understanding of how dietary glycan structures affect the gut microbiota composition and community dynamics. Here, using biochemical and biophysical techniques, we identified and characterized differences among recombinant proteins from syntenic xyloglucan utilization loci (XyGUL) of three Bacteroides and one Dysgonomonas species from the human gut, which drive substrate specificity and access to distinct polysaccharide side chains. Enzymology of four syntenic glycoside hydrolase family 5 subfamily 4 (GH5_4) endo-xyloglucanases revealed surprising differences in xyloglucan (XyG) backbone cleavage specificity, including the ability of some homologs to hydrolyze congested branched positions. Further, differences in the complement of GH43 alpha-l-arabinofuranosidases and GH95 alpha-l-fucosidases among syntenic XyGUL confer distinct abilities to fully saccharify plant species-specific arabinogalactoxyloglucan and/or fucogalactoxyloglucan. Finally, characterization of highly sequence-divergent cell surface glycan-binding proteins (SGBPs) across syntenic XyGUL revealed a novel group of XyG oligosaccharide-specific SGBPs encoded within select Bacteroides. IMPORTANCE The catabolism of complex carbohydrates that otherwise escape the endogenous digestive enzymes of humans and other animals drives the composition and function of the gut microbiota. Thus, detailed molecular characterization of dietary glycan utilization systems is essential both to understand the ecology of these complex communities and to manipulate their compositions, e.g., to benefit human health. Our research reveals new insight into how ubiquitous members of the human gut microbiota have evolved a set of microheterogeneous gene clusters to efficiently respond to the structural variations of plant xyloglucans. The data here will enable refined functional prediction of xyloglucan utilization among diverse environmental taxa in animal guts and beyond.

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Unusual active site location and catalytic apparatus in a glycoside hydrolase family

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1701130114 ◽

2017 ◽

Vol 114 (19) ◽

pp. 4936-4941 ◽

Cited By ~ 26

Author(s):

Jose Munoz-Munoz ◽

Alan Cartmell ◽

Nicolas Terrapon ◽

Bernard Henrissat ◽

Harry J. Gilbert

Keyword(s):

Gut Microbiota ◽

Active Site ◽

Glycoside Hydrolase ◽

Glycoside Hydrolase Family ◽

Potential Contribution ◽

Site Location ◽

Human Gut ◽

Human Gut Microbiota ◽

Substantial Resource ◽

Major Nutrients

The human gut microbiota use complex carbohydrates as major nutrients. The requirement for an efficient glycan degrading systems exerts a major selection pressure on this microbial community. Thus, we propose that these bacteria represent a substantial resource for discovering novel carbohydrate active enzymes. To test this hypothesis, we focused on enzymes that hydrolyze rhamnosidic bonds, as cleavage of these linkages is chemically challenging and there is a paucity of information on l-rhamnosidases. Here we screened the activity of enzymes derived from the human gut microbiota bacterium Bacteroides thetaiotaomicron, which are up-regulated in response to rhamnose-containing glycans. We identified an α-l-rhamnosidase, BT3686, which is the founding member of a glycoside hydrolase (GH) family, GH145. In contrast to other rhamnosidases, BT3686 cleaved l-Rha-α1,4–d-GlcA linkages through a retaining double-displacement mechanism. The crystal structure of BT3686 showed that the enzyme displayed a type A seven-bladed β-propeller fold. Mutagenesis and crystallographic studies, including the structure of BT3686 in complex with the reaction product GlcA, revealed a location for the active site among β-propeller enzymes cited on the posterior surface of the rhamnosidase. In contrast to the vast majority of GH, the catalytic apparatus of BT3686 does not comprise a pair of carboxylic acid residues but, uniquely, a single histidine functions as the only discernable catalytic amino acid. Intriguingly, the histidine, His48, is not invariant in GH145; however, when engineered into structural homologs lacking the imidazole residue, α-l-rhamnosidase activity was established. The potential contribution of His48 to the catalytic activity of BT3686 is discussed.

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Food additives, contaminants and other minor components: effects on human gut microbiota—a review

Journal of Physiology and Biochemistry ◽

10.1007/s13105-017-0564-2 ◽

2017 ◽

Vol 74 (1) ◽

pp. 69-83 ◽

Cited By ~ 59

Author(s):

Paula Roca-Saavedra ◽

Veronica Mendez-Vilabrille ◽

Jose Manuel Miranda ◽

Carolina Nebot ◽

Alejandra Cardelle-Cobas ◽

...

Keyword(s):

Gut Microbiota ◽

Food Additives ◽

Minor Components ◽

Human Gut ◽

Human Gut Microbiota

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Studies on the method for determination of some polysaccharide food additives by fourier transform infrared spectrum (FTIR)

Heavy metals and arsenic concentrations in water, agricultural soil, and rice in Ngan Son district, Bac Kan province, Vietnam ◽

10.47866/2615-9252/vjfc.96 ◽

2020 ◽

Vol 3 (1) ◽

pp. 46-53

Author(s):

Huyen Trang Luu Thi ◽

Thuy Le Thi ◽

Giang Tran Hoang ◽

Trang Vu Thi ◽

Minh Loi Nguyen Thi ◽

...

Keyword(s):

Infrared Spectrum ◽

Xanthan Gum ◽

Near Infrared ◽

Guar Gum ◽

Food Additives ◽

Volume Ratio ◽

Food Additive ◽

Experimental Conditions ◽

Mixture Samples

In this study, the simultaneous quantitative analysis of samples using multivarite linear regression based on near infrared spectrum has been developed. The model of partial least squares (PLS) matrix with seven value vectors is built with a standard matrix of samples (24 samples containing four analytes together with a total number of excipients) are applied for individual and/or simultaneous determination of guar gum, CMC, carrageenan, xanthan gum in real samples. A matrix of test samples including 10 samples created by fouranalytes to assess the accuracy of the PLS model. The results indicated that the relative error varied from 1.1 to 15%. The optimum experimental conditions were: spectral region: 1700 - 900 cm-1; volume ratio of sample/KBr: 2/98 (w/w); weight per capsule was 15 mg. The method was applied to identify four analytes in 15 material samples and food additive mixture samples.

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Inorganic Nanoparticles as Food Additives and their Influence on the Human Gut Microbiota

Environmental Science Nano ◽

10.1039/d1en00025j ◽

2021 ◽

Author(s):

Sheeana Gangadoo ◽

Huu Nguyen ◽

Piumie Rajapaksha ◽

Hala Zreiqat ◽

Kay Latham ◽

...

Keyword(s):

Gut Microbiota ◽

Food Processing ◽

Food Production ◽

Food Additives ◽

Inorganic Nanoparticles ◽

Human Gut ◽

Human Gut Microbiota ◽

Nano Additives

The use of various aspects of food processing, including the direct inclusion of nano-additives, are rapidly increasing in the field of nanotechnology to enhance the desired qualities in food production,...

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Cell-surface xyloglucan recognition and hydrolysis by the human gut commensal Bacteroides uniformis

Applied and Environmental Microbiology ◽

10.1128/aem.01566-21 ◽

2021 ◽

Author(s):

Julie M. Grondin ◽

Guillaume Déjean ◽

Filip Van Petegem ◽

Harry Brumer

Keyword(s):

Cell Wall ◽

Gut Microbiota ◽

Plant Cell ◽

Binding Proteins ◽

Plant Cell Wall ◽

Binding Capacity ◽

Gene Clusters ◽

Titration Calorimetry ◽

Glycoside Hydrolase Family ◽

Human Gut

Xyloglucan (XyG) is a ubiquitous plant cell wall hemicellulose that is targeted by a range of syntenic, microheterogeneous xyloglucan utilization loci (XyGUL) in Bacteroidetes species of the human gut microbiota (HGM), including Bacteroides ovatus and B. uniformis . Comprehensive biochemical and biophysical analyses have identified key differences in the protein complements of each locus that confer differential access to structurally-diverse XyG sidechain variants. A second, non-syntenic XyGUL was previously identified in B. uniformis , although its function in XyG utilization compared to its syntenic counterpart was unclear. Here, complimentary enzymatic product profiles and bacterial growth curves showcase the notable preference of Bu XyGUL2 surface glycan-binding proteins (SGBPs) to bind full-length XyG, as well as a range of oligosaccharides produced by the glycoside hydrolase family 5 (GH5_4) endo -xyloglucanase from this locus. We use isothermal titration calorimetry (ITC) to characterize this binding capacity and pinpoint the specific contributions of each protein to nutrient capture. The high-resolution structure of Bu XyGUL2 SGBP-B reveals remarkable putative binding site conservation with the canonical XyG-binding Bo XyGUL SGBP-B, supporting similar roles for these proteins in glycan capture. Together, these data underpin the central role of complimentary XyGUL function in B. uniformis , and broaden our systems-based and mechanistic understanding of XyG utilization in the HGM. Importance The omnipresence of xyloglucans in the human diet has led to the evolution of heterogeneous gene clusters in several Bacteroidetes species in the HGM, each specially tuned to respond to the structural variations of these complex plant cell wall polysaccharides. Our research illuminates the complimentary roles of syntenic and non-syntenic XyGUL in B. uniformis in conferring growth on a variety of XyG-derived substrates, providing evidence of glycan-binding protein microadaptation within a single species. These data serve as a comprehensive overview of the binding capacities of the SGBPs from a non-syntenic B. uniformis XyGUL and will inform future studies on the roles of complimentary loci in glycan targeting by key HGM species. Keywordshuman gut microbiota, microbiome, carbohydrate-active enzymes, carbohydrate-binding proteins, Bacteroidetes, CAZymes, polysaccharide utilization loci, xyloglucan

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Food Additives and Contaminants: Effects on Human Gut Microbiota—A Review

10.20944/preprints201612.0119.v1 ◽

2016 ◽

Cited By ~ 1

Author(s):

Paula Roca-Saavedra ◽

Veronica Mendez-Vilabrille ◽

Jose Manuel Miranda ◽

Alexandre Lamas ◽

Carolina Nebot ◽

...

Keyword(s):

Gut Microbiota ◽

Fatty Liver Disease ◽

Current Knowledge ◽

Food Additives ◽

Climatic Conditions ◽

Dietary Factors ◽

Human Gut ◽

Human Gut Microbiota ◽

As Stress ◽

Microbiota Diversity

Gut bacteria play an important role in several metabolic processes and human diseases, such as obesity and its co-morbidities, like fatty liver disease, insulin resistance/diabetes and cardiovascular events. Among several factors, dietary patterns, probiotics, prebiotics, synbiotics, antimicrobials and non-dietary factors, such as stress, age, exercise and climatic conditions, can dramatically impact the human gut microbiota diversity and equilibrium. However, the effect of minor food constituents, including food additives and trace contaminants, on human gut microbiota has received less attention. Consequently, the present review aimed to provide an objective perspective of the current knowledge regarding the impacts of minor food constituents on human gut microbiota and consequently, on human health.

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