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  • Review Article
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Gastrointestinal biofilms in health and disease

Nature Reviews Gastroenterology & Hepatology volume 18, pages 314–334 (2021)Cite this article

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Abstract

Microorganisms colonize various ecological niches in the human habitat, as they do in nature. Predominant forms of multicellular communities called biofilms colonize human tissue surfaces. The gastrointestinal tract is home to a profusion of microorganisms with intertwined, but not identical, lifestyles: as isolated planktonic cells, as biofilms and in biofilm-dispersed form. It is therefore of major importance in understanding homeostatic and altered host–microorganism interactions to consider not only the planktonic lifestyle, but also biofilms and biofilm-dispersed forms. In this Review, we discuss the natural organization of microorganisms at gastrointestinal surfaces, stratification of microbiota taxonomy, biogeographical localization and trans-kingdom interactions occurring within the biofilm habitat. We also discuss existing models used to study biofilms. We assess the contribution of the host–mucosa biofilm relationship to gut homeostasis and to diseases. In addition, we describe how host factors can shape the organization, structure and composition of mucosal biofilms, and how biofilms themselves are implicated in a variety of homeostatic and pathological processes in the gut. Future studies characterizing biofilm nature, physical properties, composition and intrinsic communication could shed new light on gut physiology and lead to potential novel therapeutic options for gastrointestinal diseases.

Key points

  • Bacteria adopt different lifestyles in their natural habitats, from single planktonic cells to biofilm communities.

  • Polymicrobial biofilms naturally grow throughout the gastrointestinal tract, both at the epithelial surface and in the lumen as mucin-attached and food particle-attached colonies.

  • The biofilm lifestyle influences metabolic behaviour of the microbiota but more research is needed to characterize gut biofilm-specific metabolites and their effects on the host response in health and disease.

  • Polymicrobial and trans-kingdom interactions occur in gut biofilms; deciphering the nature of such interactions might improve our current understanding of the homeostatic relationship between the host and its gut microbiota.

  • Abnormal biofilm features are associated with gastrointestinal diseases; characterization of biofilm alterations and cause-to-effect studies are warranted to elucidate their role in pathophysiology.

  • Investigating biogeographical redistribution of biofilms at mucosal surfaces might provide new tools to characterize microbial alterations associated with gastrointestinal diseases and options for therapeutic intervention.

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Fig. 1: Schematic representation of the three possible bacterial lifestyles at the gut mucosal surface under healthy conditions and their relationship with the host.
Fig. 2: Homeostatic gut microbiota biofilms throughout the gastrointestinal tract.
Fig. 3: Schematic of biofilm biogeography: a marker of mucosal health in the distal colon.
Fig. 4: Endogenous actors in biofilm–host interactions.
Fig. 5: Mucosa-associated biofilms: a biological factory.

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Authors and Affiliations

  1. Institute of Digestive Health Research, IRSD, INSERM U1220, Toulouse, France

    Jean-Paul Motta, Céline Deraison & Nathalie Vergnolle

  2. Department of Physiology & Pharmacology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada

    John L. Wallace & Nathalie Vergnolle

  3. Antibe Therapeutics Inc., Toronto, ON, Canada

    John L. Wallace

  4. Department of Biological Sciences, University of Calgary, Calgary, AB, Canada

    André G. Buret

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J.-P.M. and N.V. researched data for the article, made substantial contributions to discussion of content, wrote the article, and reviewed/edited the manuscript before submission. C.D. made a substantial contribution to discussion of content, and reviewed/edited the manuscript before submission. J.L.W. and A.G.B. reviewed/edited the manuscript before submission.

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J.L.W. is Chief Science Officer of Antibe Therapeutics. J.-P.M. received salary support from Antibe Therapeutics and from CVasThera. The other authors declare no competing interests.

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Glossary

Biofilm

A microbial lifestyle in which microorganisms are embedded in a biopolymer matrix, attached to surfaces, engaged in collective behaviour (for example, communication, cooperation, competition and differentiation) and able to persist even in hostile environments.

Planktonic

Free-swimming, free-floating, single-cell mode of life of microorganisms.

Biofilm matrix

The biopolymer substance containing communities of microorganisms assembled as a biofilm. The chemical complexity of the matrix is not fully appreciated for in vivo biofilms.

Polymicrobial

A microbial community that harbours diversity in terms of species and/or strain content.

Inflammatory bowel disease

(IBD). Chronic inflammatory disorder of the gastrointestinal tract, with multifactorial aetiology that includes genetic susceptibility and environmental factors. Associated with a displacement of gut ecology and an uncontrolled activation of the immune system.

Oxygen tension

Variable oxygenation profile over the intestinal landscape, affecting host immunity and gut microbiota.

Mucins

A class of epithelial gel-forming and non-gel-forming proteins that confer to mucus its viscous hydrophobic property, making it a physical barrier to microorganisms.

Microbial biogeography

Spatial organization of microbial taxa at mucosal surfaces.

Biofilm-dispersed bacteria

Microorganisms that naturally disperse from a biofilm, thereby acquiring biological characteristics distinct from those of their planktonic or biofilm counterparts.

Commensal

A microorganism within the digestive tract that resides in a neutral or beneficial relationship with the host.

Pathobionts

Potentially disease-causing commensals that otherwise (in healthy circumstances) live as non-harmful microorganisms.

Microbiota stability

Reflects the ability of the microbiota to resist environmental stressor-associated perturbations.

Microbiota resilience

Reflects the ability of the microbiota to recover after environmental stressor-associated perturbations.

Probiotic

Microorganisms providing health benefits through direct or indirect effects on intestinal pathobionts, pathogens or host cells.

Dysbiosis

A term used to describe taxonomic, metabolic or structural imbalances that characterize the microbiota associated with a disease condition.

Substratum

The biotic or abiotic surface on which a biofilm can form.

Quorum sensing

Density-dependent cell–cell communication, in which a signal informs the community of a threshold concentration and triggers collective group behaviour and biofilm formation.

Keystone pathogen

A low-abundance pathogen that can trigger a disproportionate effect on tissue by provoking microbiota dysbiosis.

Gut biofilm biomarkers

A molecule, gene or other biological characteristic of gut biofilms that might be used to predict a specific intestinal disease status.

Xenobiotics

Chemical substances that are not naturally produced within the organism.

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Motta, JP., Wallace, J.L., Buret, A.G. et al. Gastrointestinal biofilms in health and disease. Nat Rev Gastroenterol Hepatol 18, 314–334 (2021). https://doi.org/10.1038/s41575-020-00397-y

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