The interaction of <i>Akkermansia muciniphila</i> with host-derived substances, bacteria and diets

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Abstract

Trillions of microbes inhabit the human gut and build extremely complex communities. Gut microbes contribute to host metabolisms for better or worse and are widely studied and associated with health and disease. Akkermansia muciniphila is a gut microbiota member, which uses mucin as both carbon and nitrogen sources. Many studies on A. muciniphila have been conducted since this unique bacterium was first described in 2004. A. muciniphila can play an important role in our health because of its beneficial effects, such as improving type II diabetes and obesity and anti-inflammation. A. muciniphila establishes its position as a next-generation probiotic. Besides the effect of A. muciniphila on host health, a technique for boosting has been investigated. In this review, we show what factors can modulate the abundance of A. muciniphila focusing on the interaction with host-derived substances, other bacteria and diets. This review also refers to the possibility of the interaction between medicine and A. muciniphila; this will open up future treatment strategies that can increase A. muciniphila abundance in the gut.

Key points

• Host-derived substances such as bile, microRNA and melatonin as well as mucin have beneficial effects on A. muciniphila.

• Gut and probiotic bacteria and diet ingredients such as carbohydrates and phytochemicals could boost the abundance of A. muciniphila.

• Several medicines could affect the growth of A. muciniphila.

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Most cited references 81

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Diet rapidly and reproducibly alters the human gut microbiome

Lawrence A David, Corinne F. Maurice, Rachel Carmody … (2013)

Long-term diet influences the structure and activity of the trillions of microorganisms residing in the human gut 1–5 , but it remains unclear how rapidly and reproducibly the human gut microbiome responds to short-term macronutrient change. Here, we show that the short-term consumption of diets composed entirely of animal or plant products alters microbial community structure and overwhelms inter-individual differences in microbial gene expression. The animal-based diet increased the abundance of bile-tolerant microorganisms (Alistipes, Bilophila, and Bacteroides) and decreased the levels of Firmicutes that metabolize dietary plant polysaccharides (Roseburia, Eubacterium rectale, and Ruminococcus bromii). Microbial activity mirrored differences between herbivorous and carnivorous mammals 2 , reflecting trade-offs between carbohydrate and protein fermentation. Foodborne microbes from both diets transiently colonized the gut, including bacteria, fungi, and even viruses. Finally, increases in the abundance and activity of Bilophila wadsworthia on the animal-based diet support a link between dietary fat, bile acids, and the outgrowth of microorganisms capable of triggering inflammatory bowel disease 6 . In concert, these results demonstrate that the gut microbiome can rapidly respond to altered diet, potentially facilitating the diversity of human dietary lifestyles.

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Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation

Jacob O'Brien, Heyam Hayder, Yara Zayed … (2018)

MicroRNAs (miRNAs) are a class of non-coding RNAs that play important roles in regulating gene expression. The majority of miRNAs are transcribed from DNA sequences into primary miRNAs and processed into precursor miRNAs, and finally mature miRNAs. In most cases, miRNAs interact with the 3′ untranslated region (3′ UTR) of target mRNAs to induce mRNA degradation and translational repression. However, interaction of miRNAs with other regions, including the 5′ UTR, coding sequence, and gene promoters, have also been reported. Under certain conditions, miRNAs can also activate translation or regulate transcription. The interaction of miRNAs with their target genes is dynamic and dependent on many factors, such as subcellular location of miRNAs, the abundancy of miRNAs and target mRNAs, and the affinity of miRNA-mRNA interactions. miRNAs can be secreted into extracellular fluids and transported to target cells via vesicles, such as exosomes, or by binding to proteins, including Argonautes. Extracellular miRNAs function as chemical messengers to mediate cell-cell communication. In this review, we provide an update on canonical and non-canonical miRNA biogenesis pathways and various mechanisms underlying miRNA-mediated gene regulations. We also summarize the current knowledge of the dynamics of miRNA action and of the secretion, transfer, and uptake of extracellular miRNAs.

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Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity.

Amandine Everard, Clara Belzer, Lucie Geurts … (2013)

Obesity and type 2 diabetes are characterized by altered gut microbiota, inflammation, and gut barrier disruption. Microbial composition and the mechanisms of interaction with the host that affect gut barrier function during obesity and type 2 diabetes have not been elucidated. We recently isolated Akkermansia muciniphila, which is a mucin-degrading bacterium that resides in the mucus layer. The presence of this bacterium inversely correlates with body weight in rodents and humans. However, the precise physiological roles played by this bacterium during obesity and metabolic disorders are unknown. This study demonstrated that the abundance of A. muciniphila decreased in obese and type 2 diabetic mice. We also observed that prebiotic feeding normalized A. muciniphila abundance, which correlated with an improved metabolic profile. In addition, we demonstrated that A. muciniphila treatment reversed high-fat diet-induced metabolic disorders, including fat-mass gain, metabolic endotoxemia, adipose tissue inflammation, and insulin resistance. A. muciniphila administration increased the intestinal levels of endocannabinoids that control inflammation, the gut barrier, and gut peptide secretion. Finally, we demonstrated that all these effects required viable A. muciniphila because treatment with heat-killed cells did not improve the metabolic profile or the mucus layer thickness. In summary, this study provides substantial insight into the intricate mechanisms of bacterial (i.e., A. muciniphila) regulation of the cross-talk between the host and gut microbiota. These results also provide a rationale for the development of a treatment that uses this human mucus colonizer for the prevention or treatment of obesity and its associated metabolic disorders.

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Author and article information

Contributors

Tatsuro Hagi:

ORCID: http://orcid.org/0000-0002-0339-2236

thagi@affrc.go.jp

Clara Belzer: clara.belzer@wur.nl

Journal

Journal ID (nlm-ta): Appl Microbiol Biotechnol

Journal ID (iso-abbrev): Appl Microbiol Biotechnol

Title: Applied Microbiology and Biotechnology

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 0175-7598

ISSN (Electronic): 1432-0614

Publication date (Electronic): 14 June 2021

Publication date PMC-release: 14 June 2021

Publication date (Print): 2021

Volume: 105

Issue: 12

Pages: 4833-4841

Affiliations

[1 ]GRID grid.419600.a, ISNI 0000 0000 9191 6962, Institute of Livestock and Grassland Science, , National Agriculture and Food Research Organisation (NARO), ; 2 Ikenodai, Tsukuba, Ibaraki, 305-0901 Japan

[2 ]GRID grid.4818.5, ISNI 0000 0001 0791 5666, Laboratory of Microbiology, , Wageningen University and Research, ; 6708 WE Wageningen, The Netherlands

Author information

Tatsuro Hagi http://orcid.org/0000-0002-0339-2236

Article

Publisher ID: 11362

DOI: 10.1007/s00253-021-11362-3

PMC ID: 8236039

PubMed ID: 34125276

SO-VID: 20fc13ba-e562-4db2-b707-f1f1c2eed6b8

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 18 March 2021

Date revision received : 11 May 2021

Date accepted : 20 May 2021

Custom metadata

ScienceOpen disciplines: Biotechnology

Keywords: akkermansia muciniphila,bile acid,diet,gut bacteria,host-derived substances,prebiotic,medicine

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ScienceOpen disciplines: Biotechnology

Keywords: akkermansia muciniphila, bile acid, diet, gut bacteria, host-derived substances, prebiotic, medicine

The interaction of Akkermansia muciniphila with host-derived substances, bacteria and diets

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Most cited references 81

Diet rapidly and reproducibly alters the human gut microbiome

Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation

Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity.

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