Gut Bacteria-Mucus Interaction

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Gut Microbiota".

Deadline for manuscript submissions: closed (31 March 2018) | Viewed by 76274

Special Issue Editor

Quadram Institute Bioscience, The Gut Health and Food Safety Institute Strategic Programme, Norwich Research Park, Norwich NR4 7UA, UK
Interests: gut microbiota; mucin glycosylation; gastrointestinal mucus; carbohydrate recognition; adhesins; lectins; mucin degradation; mucus adhesion

Special Issue Information

Dear Colleagues,

The mucus layer covering the gastrointestinal tract plays a key role in maintaining a homeostatic relationship with our gut microbiota. The large intestine, which is home to most microbial species constituting the gut microbiota, is lined by a bi-layer of mucus. The outer layer providies a habitat for bacteria, whereas the inner layer maintains them at a safe distance from the epithelial surface. The terminal mucin O-glycans have been proposed to serve as attachment sites and metabolic substrates to the gut commensal bacteria, which have adapted to the mucosal environment. However, the molecular mechanisms underpinning gut bacteria-mucin glycan interactions remain poorly defined. Exploring the molecular basis of mucin adhesion and degradation of mucin glycans by predominant species of the gut microbiota is particularly important for the design of refined strategies to restore gut health. This issue will publish papers on the mechanistic aspects of gut bacteria-mucus interactions.

Dr. Nathalie Juge
Guest Editor

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Keywords

  • gut microbiota
  • mucin glycosylation
  • gastrointestinal mucus
  • carbohydrate recognition
  • adhesins
  • lectins
  • mucin degradation
  • mucus adhesion

Published Papers (9 papers)

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Editorial

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2 pages, 149 KiB  
Editorial
Special Issue: Gut Bacteria-Mucus Interaction
by Nathalie Juge
Microorganisms 2019, 7(1), 6; https://doi.org/10.3390/microorganisms7010006 - 04 Jan 2019
Cited by 7 | Viewed by 3536
Abstract
The mucus layer covering the gastrointestinal tract plays a critical role in maintaining a homeostatic relationship with our gut microbiota. [...] Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)

Research

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18 pages, 3209 KiB  
Article
A Sensitive and Rapid Method to Determine the Adhesion Capacity of Probiotics and Pathogenic Microorganisms to Human Gastrointestinal Mucins
by Bélinda Ringot-Destrez, Zéa D’Alessandro, Jean-Marie Lacroix, Muriel Mercier-Bonin, Renaud Léonard and Catherine Robbe-Masselot
Microorganisms 2018, 6(2), 49; https://doi.org/10.3390/microorganisms6020049 - 29 May 2018
Cited by 17 | Viewed by 5231
Abstract
Mucus is the habitat for the microorganisms, bacteria and yeast that form the commensal flora. Mucins, the main macromolecules of mucus, and more specifically, the glycans that cover them, play essential roles in microbial gastrointestinal colonization. Probiotics and pathogens must also colonize mucus [...] Read more.
Mucus is the habitat for the microorganisms, bacteria and yeast that form the commensal flora. Mucins, the main macromolecules of mucus, and more specifically, the glycans that cover them, play essential roles in microbial gastrointestinal colonization. Probiotics and pathogens must also colonize mucus to have lasting positive or deleterious effects. The question of which mucin-harboured glycan motifs favour the adhesion of specific microorganisms remains very poorly studied. In the current study, a simple test based on the detection of fluorescent-labeled microorganisms raised against microgram amounts of mucins spotted on nitrocellulose was developed. The adhesion of various probiotic, commensal and pathogenic microorganisms was evaluated on a panel of human purified gastrointestinal mucins and compared with that of commercially available pig gastric mucins (PGM) and of mucins secreted by the colonic cancer cell line HT29-MTX. The latter two proved to be very poor indicators of adhesion capacity on intestinal mucins. Our results show that the nature of the sialylated cores of O-glycans, determined by MALDI MS-MS analysis, potentially enables sialic acid residues to modulate the adhesion of microorganisms either positively or negatively. Other identified factors affecting the adhesion propensity were O-glycan core types and the presence of blood group motifs. This test should help to select probiotics with enhanced adhesion capabilities as well as deciphering the role of specific mucin glycotopes on microbial adhesion. Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)
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15 pages, 2929 KiB  
Article
Binding of Helicobacter pylori to Human Gastric Mucins Correlates with Binding of TFF1
by Ciara Dunne, Julie Naughton, Gina Duggan, Catherine Loughrey, Michelle Kilcoyne, Lokesh Joshi, Stephen Carrington, Helen Earley, Steffen Backert, Catherine Robbe Masselot, Felicity E. B. May and Marguerite Clyne
Microorganisms 2018, 6(2), 44; https://doi.org/10.3390/microorganisms6020044 - 18 May 2018
Cited by 13 | Viewed by 5065
Abstract
Helicobacter pylori binds to the gastric mucin, MUC5AC, and to trefoil factor, TFF1, which has been shown to interact with gastric mucin. We examined the interactions of TFF1 and H. pylori with purified gastrointestinal mucins from different animal species and from humans printed [...] Read more.
Helicobacter pylori binds to the gastric mucin, MUC5AC, and to trefoil factor, TFF1, which has been shown to interact with gastric mucin. We examined the interactions of TFF1 and H. pylori with purified gastrointestinal mucins from different animal species and from humans printed on a microarray platform to investigate whether TFF1 may play a role in locating H. pylori in gastric mucus. TFF1 bound almost exclusively to human gastric mucins and did not interact with human colonic mucins. There was a strong correlation between binding of TFF1 and H. pylori to human gastric mucins, and between binding of both TFF1 and H. pylori to gastric mucins with that of Griffonia simplicifolia lectin-II, which is specific for terminal non-reducing α- or β-linked N-acetyl-d-glucosamine. These results suggest that TFF1 may help to locate H. pylori in a discrete layer of gastric mucus and hence restrain their interactions with epithelial cells. Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)
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Review

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17 pages, 1203 KiB  
Review
Dietary Nutrients, Proteomes, and Adhesion of Probiotic Lactobacilli to Mucin and Host Epithelial Cells
by Hasan Ufuk Celebioglu and Birte Svensson
Microorganisms 2018, 6(3), 90; https://doi.org/10.3390/microorganisms6030090 - 21 Aug 2018
Cited by 33 | Viewed by 6746
Abstract
The key role of diet and environment in human health receives increasing attention. Thus functional foods, probiotics, prebiotics, and synbiotics with beneficial effects on health and ability to prevent diseases are in focus. The efficacy of probiotic bacteria has been connected with their [...] Read more.
The key role of diet and environment in human health receives increasing attention. Thus functional foods, probiotics, prebiotics, and synbiotics with beneficial effects on health and ability to prevent diseases are in focus. The efficacy of probiotic bacteria has been connected with their adherence to the host epithelium and residence in the gut. Several in vitro techniques are available for analyzing bacterial interactions with mucin and intestinal cells, simulating adhesion to the host in vivo. Proteomics has monitored and identified proteins of probiotic bacteria showing differential abundance elicited in vitro by exposure to food components, including potential prebiotics (e.g., certain carbohydrates, and plant polyphenols). While adhesion of probiotic bacteria influenced by various environmental factors relevant to the gastrointestinal tract has been measured previously, this was rarely correlated with changes in the bacterial proteome induced by dietary nutrients. The present mini-review deals with effects of selected emerging prebiotics, food components and ingredients on the adhesion of probiotic lactobacilli to mucin and gut epithelial cells and concomitant abundancy changes of specific bacterial proteins. Applying this in vitro synbiotics-like approach enabled identification of moonlighting and other surface-located proteins of Lactobacillus acidophilus NCFM that are possibly associated with the adhesive mechanism. Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)
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57 pages, 17224 KiB  
Review
The Interaction of the Gut Microbiota with the Mucus Barrier in Health and Disease in Human
by Anthony P. Corfield
Microorganisms 2018, 6(3), 78; https://doi.org/10.3390/microorganisms6030078 - 02 Aug 2018
Cited by 94 | Viewed by 10461
Abstract
Glycoproteins are major players in the mucus protective barrier in the gastrointestinal and other mucosal surfaces. In particular the mucus glycoproteins, or mucins, are responsible for the protective gel barrier. They are characterized by their high carbohydrate content, present in their variable number, [...] Read more.
Glycoproteins are major players in the mucus protective barrier in the gastrointestinal and other mucosal surfaces. In particular the mucus glycoproteins, or mucins, are responsible for the protective gel barrier. They are characterized by their high carbohydrate content, present in their variable number, tandem repeat domains. Throughout evolution the mucins have been maintained as integral components of the mucosal barrier, emphasizing their essential biological status. The glycosylation of the mucins is achieved through a series of biosynthetic pathways processes, which generate the wide range of glycans found in these molecules. Thus mucins are decorated with molecules having information in the form of a glycocode. The enteric microbiota interacts with the mucosal mucus barrier in a variety of ways in order to fulfill its many normal processes. How bacteria read the glycocode and link to normal and pathological processes is outlined in the review. Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)
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26 pages, 1066 KiB  
Review
Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How?
by Sharon Y. Geerlings, Ioannis Kostopoulos, Willem M. De Vos and Clara Belzer
Microorganisms 2018, 6(3), 75; https://doi.org/10.3390/microorganisms6030075 - 23 Jul 2018
Cited by 257 | Viewed by 21753
Abstract
Akkermansia muciniphila is a mucin-degrading bacterium of the phylum Verrucomicrobia. Its abundance in the human intestinal tract is inversely correlated to several disease states. A. muciniphila resides in the mucus layer of the large intestine, where it is involved in maintaining intestinal integrity. [...] Read more.
Akkermansia muciniphila is a mucin-degrading bacterium of the phylum Verrucomicrobia. Its abundance in the human intestinal tract is inversely correlated to several disease states. A. muciniphila resides in the mucus layer of the large intestine, where it is involved in maintaining intestinal integrity. We explore the presence of Akkermansia-like spp. based on its 16S rRNA sequence and metagenomic signatures in the human body so as to understand its colonization pattern in time and space. A. muciniphila signatures were detected in colonic samples as early as a few weeks after birth and likely could be maintained throughout life. The sites where Akkermansia-like sequences (including Verrucomicrobia phylum and/or Akkermansia spp. sequences found in the literature) were detected apart from the colon included human milk, the oral cavity, the pancreas, the biliary system, the small intestine, and the appendix. The function of Akkermansia-like spp. in these sites may differ from that in the mucosal layer of the colon. A. muciniphila present in the appendix or in human milk could play a role in the re-colonization of the colon or breast-fed infants, respectively. In conclusion, even though A. muciniphila is most abundantly present in the colon, the presence of Akkermansia-like spp. along the digestive tract indicates that this bacterium might have more functions than those currently known. Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)
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21 pages, 317 KiB  
Review
Mucus-Pathogen Interactions in the Gastrointestinal Tract of Farmed Animals
by Macarena P. Quintana-Hayashi, Médea Padra, János Tamás Padra, John Benktander and Sara K. Lindén
Microorganisms 2018, 6(2), 55; https://doi.org/10.3390/microorganisms6020055 - 18 Jun 2018
Cited by 48 | Viewed by 6534
Abstract
Gastrointestinal infections cause significant challenges and economic losses in animal husbandry. As pathogens becoming resistant to antibiotics are a growing concern worldwide, alternative strategies to treat infections in farmed animals are necessary in order to decrease the risk to human health and increase [...] Read more.
Gastrointestinal infections cause significant challenges and economic losses in animal husbandry. As pathogens becoming resistant to antibiotics are a growing concern worldwide, alternative strategies to treat infections in farmed animals are necessary in order to decrease the risk to human health and increase animal health and productivity. Mucosal surfaces are the most common route used by pathogens to enter the body. The mucosal surface that lines the gastrointestinal tract is covered by a continuously secreted mucus layer that protects the epithelial surface. The mucus layer is the first barrier the pathogen must overcome for successful colonization, and is mainly composed of densely glycosylated proteins called mucins. The vast array of carbohydrate structures present on the mucins provide an important setting for host-pathogen interactions. This review summarizes the current knowledge on gastrointestinal mucins and their role during infections in farmed animals. We examine the interactions between mucins and animal pathogens, with a focus on how pathogenic bacteria can modify the mucin environment in the gut, and how this in turn affects pathogen adhesion and growth. Finally, we discuss analytical challenges and complexities of the mucus-based defense, as well as its potential to control infections in farmed animals. Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)
18 pages, 848 KiB  
Review
Mucus: An Underestimated Gut Target for Environmental Pollutants and Food Additives
by Kévin Gillois, Mathilde Lévêque, Vassilia Théodorou, Hervé Robert and Muriel Mercier-Bonin
Microorganisms 2018, 6(2), 53; https://doi.org/10.3390/microorganisms6020053 - 15 Jun 2018
Cited by 54 | Viewed by 9181
Abstract
Synthetic chemicals (environmental pollutants, food additives) are widely used for many industrial purposes and consumer-related applications, which implies, through manufactured products, diet, and environment, a repeated exposure of the general population with growing concern regarding health disorders. The gastrointestinal tract is the first [...] Read more.
Synthetic chemicals (environmental pollutants, food additives) are widely used for many industrial purposes and consumer-related applications, which implies, through manufactured products, diet, and environment, a repeated exposure of the general population with growing concern regarding health disorders. The gastrointestinal tract is the first physical and biological barrier against these compounds, and thus their first target. Mounting evidence indicates that the gut microbiota represents a major player in the toxicity of environmental pollutants and food additives; however, little is known on the toxicological relevance of the mucus/pollutant interplay, even though mucus is increasingly recognized as essential in gut homeostasis. Here, we aimed at describing how environmental pollutants (heavy metals, pesticides, and other persistent organic pollutants) and food additives (emulsifiers, nanomaterials) might interact with mucus and mucus-related microbial species; that is, “mucophilic” bacteria such as mucus degraders. This review highlights that intestinal mucus, either directly or through its crosstalk with the gut microbiota, is a key, yet underestimated gut player that must be considered for better risk assessment and management of environmental pollution. Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)
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26 pages, 14577 KiB  
Review
The Role of Glycans in Bacterial Adhesion to Mucosal Surfaces: How Can Single-Molecule Techniques Advance Our Understanding?
by Cécile Formosa-Dague, Mickaël Castelain, Hélène Martin-Yken, Karen Dunker, Etienne Dague and Marit Sletmoen
Microorganisms 2018, 6(2), 39; https://doi.org/10.3390/microorganisms6020039 - 04 May 2018
Cited by 27 | Viewed by 6458
Abstract
Bacterial adhesion is currently the subject of increased interest from the research community, leading to fast progress in our understanding of this complex phenomenon. Resent research within this field has documented the important roles played by glycans for bacterial surface adhesion, either through [...] Read more.
Bacterial adhesion is currently the subject of increased interest from the research community, leading to fast progress in our understanding of this complex phenomenon. Resent research within this field has documented the important roles played by glycans for bacterial surface adhesion, either through interaction with lectins or with other glycans. In parallel with this increased interest for and understanding of bacterial adhesion, there has been a growth in the sophistication and use of sensitive force probes for single-molecule and single cell studies. In this review, we highlight how the sensitive force probes atomic force microscopy (AFM) and optical tweezers (OT) have contributed to clarifying the mechanisms underlying bacterial adhesion to glycosylated surfaces in general and mucosal surfaces in particular. We also describe research areas where these techniques have not yet been applied, but where their capabilities appear appropriate to advance our understanding. Full article
(This article belongs to the Special Issue Gut Bacteria-Mucus Interaction)
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