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Approaches to Investigate Selective Dietary Polysaccharide Utilization by Human Gut Microbiota at a Functional Level.

ABSTRACT: The human diet is temporally and spatially dynamic, and influenced by culture, regional food systems, socioeconomics, and consumer preference. Such factors result in enormous structural diversity of ingested glycans that are refractory to digestion by human enzymes. To convert these glycans into metabolizable nutrients and energy, humans rely upon the catalytic potential encoded within the gut microbiome, a rich collective of microorganisms residing in the gastrointestinal tract. The development of high-throughput sequencing methods has enabled microbial communities to be studied with more coverage and depth, and as a result, cataloging the taxonomic structure of the gut microbiome has become routine. Efforts to unravel the microbial processes governing glycan digestion by the gut microbiome, however, are still in their infancy and will benefit by retooling our approaches to study glycan structure at high resolution and adopting next-generation functional methods. Also, new bioinformatic tools specialized for annotating carbohydrate-active enzymes and predicting their functions with high accuracy will be required for deciphering the catalytic potential of sequence datasets. Furthermore, physiological approaches to enable genotype-phenotype assignments within the gut microbiome, such as fluorescent polysaccharides, has enabled rapid identification of carbohydrate interactions at the single cell level. In this review, we summarize the current state-of-knowledge of these methods and discuss how their continued development will advance our understanding of gut microbiome function.

SUBMITTER: Klassen L

PROVIDER: S-EPMC7933471 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Approaches to Investigate Selective Dietary Polysaccharide Utilization by Human Gut Microbiota at a Functional Level.

Klassen Leeann L Xing Xiaohui X Tingley Jeffrey P JP Low Kristin E KE King Marissa L ML Reintjes Greta G Abbott D Wade DW

Frontiers in microbiology 20210219

The human diet is temporally and spatially dynamic, and influenced by culture, regional food systems, socioeconomics, and consumer preference. Such factors result in enormous structural diversity of ingested glycans that are refractory to digestion by human enzymes. To convert these glycans into metabolizable nutrients and energy, humans rely upon the catalytic potential encoded within the gut microbiome, a rich collective of microorganisms residing in the gastrointestinal tract. The development ...[more]

PMID: 33679661

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Project description:Dietary intake of specific non-digestible carbohydrates (including prebiotics) is increasingly seen as a highly effective approach for manipulating the composition and activities of the human gut microbiota to benefit health. Nevertheless, surprisingly little is known about the global response of the microbial community to particular carbohydrates. Recent in vivo dietary studies have demonstrated that the species composition of the human faecal microbiota is influenced by dietary intake. There is now potential to gain insights into the mechanisms involved by using in vitro systems that produce highly controlled conditions of pH and substrate supply.We supplied two alternative non-digestible polysaccharides as energy sources to three different human gut microbial communities in anaerobic, pH-controlled continuous-flow fermentors. Community analysis showed that supply of apple pectin or inulin resulted in the highly specific enrichment of particular bacterial operational taxonomic units (OTUs; based on 16S rRNA gene sequences). Of the eight most abundant Bacteroides OTUs detected, two were promoted specifically by inulin and six by pectin. Among the Firmicutes, Eubacterium eligens in particular was strongly promoted by pectin, while several species were stimulated by inulin. Responses were influenced by pH, which was stepped up, and down, between 5.5, 6.0, 6.4 and 6.9 in parallel vessels within each experiment. In particular, several experiments involving downshifts to pH 5.5 resulted in Faecalibacterium prausnitzii replacing Bacteroides spp. as the dominant sequences observed. Community diversity was greater in the pectin-fed than in the inulin-fed fermentors, presumably reflecting the differing complexity of the two substrates.We have shown that particular non-digestible dietary carbohydrates have enormous potential for modifying the gut microbiota, but these modifications occur at the level of individual strains and species and are not easily predicted a priori. Furthermore, the gut environment, especially pH, plays a key role in determining the outcome of interspecies competition. This makes it crucial to put greater effort into identifying the range of bacteria that may be stimulated by a given prebiotic approach. Both for reasons of efficacy and of safety, the development of prebiotics intended to benefit human health has to take account of the highly individual species profiles that may result.

Project description:Plasticity in the microbial community composition and function can permit the host to adapt to ecological, environmental, and physiological changes. Much of the information on the gut microbiota-host relationship to date derives from studies of laboratory model organisms, while little is known concerning wild animals and their ecological relevance to gut microbes. It is also unclear how microbial community composition and activity adapt to changes in diet and energy, nutritional requirements, and utilization induced by dietary expansion from invertebrates to vertebrates. The great evening bat (Ia io) is both an insectivore and an avivore (that is, a bird-eater), and thus provides an opportunity to investigate the diet-host-microbiota-physiology relationship. Here, we investigated this relationship by using 16S rRNA amplicon sequencing and functional prediction in adult males of I. io. We found that gut microbial diversity was similar, while microbial community structures were significantly different between insectivorous and avivorous diets. Moreover, increases in the relative abundance of Firmicutes and the Firmicutes-to-Bacteroidetes ratio, changes in carbohydrate and nucleotide metabolism, and a decrease in Pseudomonas were associated with higher energy demands for hunting birds and with fat storage for entering hibernation and migration. These findings demonstrated that seasonal dietary shifts drive a significant change in the composition and function of gut microbiomes, thereby facilitating adaptation to the challenging avian dietary niche in bats. These results suggest that the gut microbial communities can constantly respond to alterations in diets, potentially facilitating the diversity of wild animal dietary niches, and enhance our understanding of the diet-host-microbiota-physiology relationship. IMPORTANCE The coevolution between the host and its gut microbes can promote an animal's adaptation to its specific ecological niche and changes in energy and nutritional requirements. This study focused on an avivorous bat, the great evening bat (Ia io), to investigate how seasonal dietary shifts affect the gut microbial composition and function, thereby facilitating adaptation to an avian diet. We found that seasonal dietary shifts driving a significant change in the composition and function of gut microbiomes in I. io were associated with higher energy demands for hunting birds and fat storage for entering hibernation and migration. Our study provides novel insight into the role of gut bacteria in generating ecological diversity and flexibility in wild mammals. The results are valuable for clarifying the complicated host-microbiota-physiology relationship in a dietary niche expansion context.

Dataset Information

Approaches to Investigate Selective Dietary Polysaccharide Utilization by Human Gut Microbiota at a Functional Level.

Publications

Approaches to Investigate Selective Dietary Polysaccharide Utilization by Human Gut Microbiota at a Functional Level.

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