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Transmission of the gut microbiota: spreading of health

Nature Reviews Microbiology volume 15, pages 531–543 (2017)Cite this article

Subjects

Key Points

  • The human intestinal microbiota is dominated by anaerobic health-associated bacteria that are established and maintained in individuals through host-to-host transmission. The transmission process incorporates excretion from a host in faecal matter, survival and persistence in the external environment, and concludes with ingestion and subsequent colonization of a new host.

  • Studies of the routes of transmission of intestinal pathogens provide a useful framework to better understand intestinal commensal transmission. Both share some common transmission features, such as the use of the faecal–oral transmission route and similar survival mechanisms to persist in the external environment.

  • Environmental survival mechanisms that are used by the intestinal microbiota once expelled by a host include sporulation, aerotolerance and entering a viable but non-culturable (VBNC) dormancy state. For anaerobic bacteria, these mechanisms protect against harmful oxygen, and in the case of sporulation and VBNC states, can provide varying resistance against other environmental conditions, such as desiccation and a lack of nutrients.

  • Reservoirs are a source or a sink for bacteria during transmission. Other people in the community are the principal reservoirs of intestinal bacteria, but food, water, animals and the built environment may also facilitate transmission.

  • Transmission of commensal bacteria may be disrupted by human sanitation practices, through the use of antibiotics or a long-term change in diet, which can eliminate species within an individual thereby preventing their onward transmission. Direct interventions to restore a depleted microbiota, such as faecal microbiota transplantation (FMT), are effective in some cases.

  • A greater general awareness of the transmission of the commensal microbiota is facilitated by technological advances in different disciplines, including microbiology, bioinformatics and genomics. Fostering the transmission of commensal bacteria between people through the maintenance of a healthy lifestyle and the discerning use of antibiotics and sanitation processes may promote human health.

Abstract

Transmission of commensal intestinal bacteria between humans could promote health by establishing, maintaining and replenishing microbial diversity in the microbiota of an individual. Unlike pathogens, the routes of transmission for commensal bacteria remain unappreciated and poorly understood, despite the likely commonalities between both. Consequently, broad infection control measures that are designed to prevent pathogen transmission and infection, such as oversanitation and the overuse of antibiotics, may inadvertently affect human health by altering normal commensal transmission. In this Review, we discuss the mechanisms and factors that influence host-to-host transmission of the intestinal microbiota and examine how a better understanding of these processes will identify new approaches to nurture and restore transmission routes that are used by beneficial bacteria.

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Figure 1: Transmission of pathogenic and commensal intestinal bacteria.
Figure 2: Environmental survival mechanisms and sporulation transmission dynamics of the intestinal microbiota.
Figure 3: Inter-host transmission dynamics of spore-forming and non-spore-forming intestinal bacteria.
Figure 4: Transmission of commensal intestinal bacteria is influenced by donor health status.

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Acknowledgements

The authors thank A. Zhu for critical reading of the manuscript during preparation. H.P.B. is funded through a Medical Research Council (MRC) grant (PF451), B.A.N. is funded through a Wellcome Trust grant (098051), S.C.F. is funded through an Australian National Health and Medical Research Council (NHMRC) grant (1091097). Work in the Lawley laboratory is supported through a MRC grant (PF451) and a Wellcome Trust grant (098051).

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Authors and Affiliations

  1. Host–Microbiota Interactions Laboratory, Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, Cambridgeshire, UK

    Hilary P. Browne, B. Anne Neville, Samuel C. Forster & Trevor D. Lawley

  2. Centre for Innate Immunity and Infectious Diseases, Hudson Institute of Medical Research, Clayton, 3168, Victoria, Australia

    Samuel C. Forster

  3. Department of Molecular and Translational Sciences, Monash University, Clayton, 3800, Victoria, Australia

    Samuel C. Forster

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Correspondence to Trevor D. Lawley.

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Supplementary information

Supplementary information Table 1

Aerotolerance of non-spore forming intestinal bacteria. (PDF 195 kb)

PowerPoint slides

Glossary

Peritoneum

A membrane that lines the abdominal cavity and provides a supportive role to internal body organs, including those of the gastrointestinal tract.

Pathobionts

Members of the commensal microbiota that may become pathogenic under certain circumstances.

Facultative anaerobic bacteria

Species that can grow and survive in aerobic and anaerobic conditions.

Infectious dose

The minimum number of bacteria required to cause an infection in a host.

Colonization resistance

The capacity of the resident microbiota to prevent the establishment of new species within the community, particularly the establishment of pathogens. Colonization resistance is a feature of a stable health-associated microbiota.

Homeostasis

A stable state. The overall maintenance of precise conditions in the microbiota that promote colonization resistance, even when subjected to external perturbations or stresses.

Colonizing dose

The minimum number of bacteria required to stably colonize a new host.

Super-shedding state

A host state, typically associated with infection by pathogens, that results in the release of numerous bacteria or spores into the external environment.

Antimicrobial peptides

A diverse range of proteins that are secreted by the host as a defence mechanism against pathogens or by microorganisms to target other microorganisms in close proximity.

Siderophores

Low-molecular-weight, iron-chelating agents that are secreted by bacteria and fungi to acquire iron from the surrounding environment.

Dysbiosis

A low-diversity microbiota with reduced colonization resistance that is typically associated with inflammation and outgrowth of facultative anaerobic Proteobacteria and pathogens.

Fucosylated

The attachment of a fucose molecule to a protein. Fucosylation of epithelial cells by the host can provide a protective role through the subsequent recruitment of commensal bacteria.

Toll-like receptors

A family of transmembrane protein receptors, characterized by the presence of a Toll and interleukin-1 receptor (TIR) domain, that recognize specific microorganism-associated molecular patterns and initiate an immune response.

Nucleotide-binding oligomerization domain-like receptors

(NOD-like receptors). A family of intracellular protein receptors that recognize microorganism-associated molecular patterns and initiate an immune response.

Desiccation

The process of liquid removal or drying out, which is usually deleterious to a bacterial cell.

Vegetative cell

The form of a bacterial cell that reproduces through binary fission.

Aerobic bacteria

Species that can only grow and survive in the presence of oxygen.

Obligate anaerobic bacteria

Species that can only grow and survive in the absence of oxygen.

Flavin–thiol electron shuttle

A process that involves the transfer of electrons to oxygen through riboflavin and thiol, which enables survival and growth in the presence of oxygen.

Social grooming

Cleaning and grooming carried out by animals, particularly primates, on other individuals in their community, which has hygienic and social roles.

Horizontal gene transfer

The transfer of genetic material between different strains or species that occurs independently of vertical transmission during replication.

Probiotics

Live microorganisms that when administered in adequate amounts confer a health benefit to the host.

Indicator microorganisms

Microorganisms that are used to assay hygiene levels of foods or water, in which the quantity of the microorganisms present is inversely related to the quality or hygiene level of the product being tested.

Undernutrition

A situation whereby an individual does not consume enough nutrients, which can have adverse effects on health.

α-diversity

The ecological diversity at a single site, as measured by the number of different species and their abundance.

β-diversity

A measure of the difference in ecological diversity between different sites.

Functional foods

Foods that contain additional elements to promote health, such as probiotics, prebiotics, vitamins or minerals.

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Browne, H., Neville, B., Forster, S. et al. Transmission of the gut microbiota: spreading of health. Nat Rev Microbiol 15, 531–543 (2017). https://doi.org/10.1038/nrmicro.2017.50

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