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Emerging Pathogenic Links Between the Microbiota and the Gut–Lung Axis

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Emerging Pathogenic Links Between the Microbiota and the Gut–Lung Axis PERSPECTIVES Microbiota of the healthy gut and lungs MICROBIOME — OPINION The GIT remains, by far, the best-studied host-associated microbial ecosystem, partly Emerging pathogenic links between owing to its abundance of microorganisms and partly because the microbiota can be profiled through faeces, which is easily microbiota and the gut–lung axis obtainable. Both the abundance and diversity of the commensal microbiota Kurtis F. Budden, Shaan L. Gellatly, David L. A. Wood, Matthew A. Cooper, generally increase along the GIT, and there Mark Morrison, Philip Hugenholtz and Philip M. Hansbro are site-specific variations in the mucosa and the lumen13,14. These differences are Abstract | The microbiota is vital for the development of the immune system and governed by the prevailing environment, homeostasis. Changes in microbial composition and function, termed dysbiosis, in including pH, the concentration of bile the respiratory tract and the gut have recently been linked to alterations in immune acids, digesta retention time, mucin responses and to disease development in the lungs. In this Opinion article, we properties and host defence factors15. review the microbial species that are usually found in healthy gastrointestinal and Despite these variations, the GIT is dominated by members of only four respiratory tracts, their dysbiosis in disease and interactions with the gut–lung axis. bacterial phyla, Firmicutes, Bacteroidetes, Although the gut–lung axis is only beginning to be understood, emerging evidence Proteobacteria and Actinobacteria; indicates that there is potential for manipulation of the gut microbiota in the with lesser and sporadic representation treatment of lung diseases. of other phyla, including Fusobacteria, Verrucomicrobia and Spirochaetes. This ‘core’ gut microbial community comprises Chronic lung diseases, such as asthma which lack an appropriately developed up to 14 bacterial genera and 150 bacterial and chronic obstructive pulmonary disease immune system and show mucosal ‘species’, many of which have not yet (COPD), are common and often occur alterations, both of which can be restored been cultured16–18. together with chronic gastrointestinal through colonization with gut microbiota6,7. We are beginning to understand the tract (GIT) diseases, such as inflammatory The microbiota changes over time lung microbiota through programmes bowel disease (IBD) or irritable bowel from birth, to adulthood and into old such as the Lung HIV Microbiome Project, syndrome (IBS)1,2. Up to 50% of adults age, and in response to environmental which is a multi-centre study that examines with IBD and 33% of patients with IBS factors, such as diet, and drug and both individuals who are infected with have pulmonary involvement, such as environmental exposures8. HIV and uninfected individuals who inflammation or impaired lung function, In this ever-expanding field, researchers have varying histories of lung and/or although many patients have no history are now investigating how the local respiratory disease19. The lungs have a of acute or chronic respiratory disease3,4. microbiota influences immunity at distal large surface area with high environmental Furthermore, patients with COPD are sites, in particular how the gut microbiota exposure and are equipped with effective 2–3 times more likely to be diagnosed influences other organs, such as the brain, antimicrobial defences. Healthy lungs were with IBD4. Individuals with asthma have liver or lungs. This has led to the coining long considered to be sterile; however, the functional and structural alterations in of terms such as the ‘gut–brain axis’ and advent of culture-independent approaches their intestinal mucosa, and patients with ‘gut–lung axis’. For example, antibiotic- for microbial community profiling has COPD typically have increased intestinal induced alterations in the gut microbiota resulted in the detection of microbial DNA permeability2,5. Although the mature in early life increase the risk of developing in the lungs of healthy individuals19,20. GIT and respiratory tract have different allergic airway disease9–12; such findings These microorganisms probably reached environments and functions, they have the add to our understanding of the links the lungs from the oral cavity through same embryonic origin and, consequently, between exposure to microorganisms and microaspiration, as the taxonomic profiles have structural similarities. Thus, it is not allergy and autoimmunity (BOX 1). The of the two sites were similar19,20. Compared surprising that the two sites might interact mechanisms by which the gut microbiota with surrounding sites, the lungs had a in health and disease (FIG. 1); however, affects the immune responses in the lungs, decreased abundance of Prevotella-affiliated the underlying mechanisms are not and vice versa, are being uncovered, but taxa and an enrichment of Proteobacteria, well understood. many questions remain. In this Opinion specifically Enterobacteriaceae, An emerging area of intense interest article, we summarize the emerging role Ralstonia spp., and Haemophilus spp.19, is the influence of the host-associated of the microbiota in the gut–lung axis, which may have resulted from host microbiota on local and systemic immunity. highlighting gaps in our knowledge and the immunity and environment, such as redox This is exemplified in germ-free mice, potential for therapeutic intervention. state and oxygen availability. The lung NATURE REVIEWS | MICROBIOLOGY VOLUME 15 | JANUARY 2016 | 55 ©2016 Mac millan Publishers Li mited, part of Spri nger Nature. All ri ghts reserved. PERSPECTIVES microbiota might not be resident in the lungs22. Technical challenges, such as the gut and respiratory mucosa provide healthy individuals, but rather transiently low microbial biomass and bronchoscope a physical barrier against microbial recolonized through microaspiration and contamination, constant seeding from penetration, and colonization with the breathing. The lungs have a comparatively oral and GIT sites, and mucociliary and normal microbiota generates resistance low microbial biomass and remarkably immune clearance, have hindered the to pathogens; for example, through the similar composition to adjacent sites, identification of a viable and resident, production of bacteriocins15. Furthermore, even though the lungs are continuously or a transiently recolonizing, microbiota a rapidly expanding collection of exposed to entering microorganisms and in the lungs, as well as further research commensal gut bacteria, including their environmental conditions differ vastly into host–microorganism interactions. segmented filamentous bacteria (SFB), from other body sites. These observations Novel methods of sampling tissue with Bifidobacterium spp. and members of support the hypothesis that entry and minimal contamination23, longitudinal the colonic Bacteroides genus, induce the selective elimination of a transient studies to identify temporal changes in production of antimicrobial peptides, microbiota is the major determinant of the microbiota, and the increasing use secretory immunoglobulin A (sIgA) microbial composition in the lungs, rather of metagenomic analyses to facilitate the and pro-­inflammatory cytokines. than resident and viable microorganisms. cultivation of fastidious bacterial species24, Non-pathogenic Salmonella strains This does not negate the importance of will provide a clearer picture of the role of downregulate inflammatory responses host–microorganism interactions in the the respiratory microbiota and enable the in GIT epithelial cells by inhibiting lungs, as evidenced by correlations better design of interventional studies to the ubiquitylation of nuclear factor-κB between the composition of microbial develop a more complete understanding (NF-κB) inhibitor-α (IκBα)25, whereas communities and pulmonary inflammation of host–microorganism interactions in some Clostridium spp. promote and disease21. Rather, it highlights the the lungs. anti-­inflammatory regulatory T cell 26 delicate balance between microbial (Treg cell) responses . In the respiratory exposure and elimination; the possibility Interactions between the gut and lungs tract, Streptococcus pneumoniae and of dysbiosis at oral sites preceding and/or Interactions of microorganisms between Haemophilus influenzae synergistically causing dysbiosis in the lungs and the sites. The epithelial surfaces of the activate host p38 mitogen-activated contributing to disease pathogenesis19; GIT and respiratory tract are exposed to a protein kinase (MAPK) in a Toll-like and the importance in distinguishing wide variety of microorganisms; ingested receptor (TLR)-independent manner to whether microbial DNA that is detected microorganisms can access both sites amplify pro-inflammatory responses27. by culture-independent techniques is and the microbiota from the GIT can Conversely, non-pathogenic S. pneumoniae truly representative of viable bacteria in enter the lungs through aspiration. Both and other bacteria and their components Health Disease Inhalation or swallowing Triggers of dysbiosis • Infection • Antibiotics • Cigarette smoke • Healthy lung environment • Chronic lung disease • Effective clearance of infection • Poor clearance of infection Immune modulation Dysfunctional immune modulation Gastrointestinal • Bacterial ligands (for example, LPS) disease or symptoms • Bacterial metabolites (for example, SCFAs) Intestinal Dysbiosis of • Migrating immune cells microbiota microbiota Figure 1 | Principles of
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