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      The microbiota of the respiratory tract: gatekeeper to respiratory health

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          Key Points

          • The anatomical development and maturation of the human respiratory tract is a complex multistage process that occurs not only in prenatal life but also postnatally. This maturation process depends, in part, on exposure to microbial and environmental triggers, and results in a highly specialized organ system that contains several distinct niches, each of which is subjected to specific microbial, cellular and physiological gradients.

          • The respiratory microbiome during early life is dynamic and its development is affected by a range of host and environmental factors, including mode of birth, feeding type, antibiotic treatment and crowding conditions, such as the presence of siblings and day-care attendance.

          • The upper respiratory tract is colonized by specialized resident bacterial, viral and fungal assemblages, which presumably prevent potential pathogens from overgrowing and disseminating towards the lungs, thereby functioning as gatekeepers to respiratory health.

          • The upper respiratory tract is the primary source of the lung microbiome. In healthy individuals, the lung microbiome seems to largely consist of transient microorganisms and its composition is determined by the balance between microbial immigration and elimination.

          • Next-generation sequencing has identified intricate interbacterial association networks that comprise true mutualistic, commensal or antagonistic direct or indirect relationships. Alternatively, bacterial co-occurrence seems to be driven by host and environmental factors, as well as by interactions with viruses and fungi.

          • The respiratory microbiome provides cues to the host immune system that seem to be vital for immune training, organogenesis and the maintenance of immune tolerance. Increasing evidence supports the existence of a window of opportunity early in life, during which adequate microbiota sensing is essential for immune maturation and consecutive respiratory health.

          • Future studies should focus on large-scale, multidisciplinary holistic approaches and adequately account for host and environmental factors. Associations that are identified by these studies can then be corroborated in reductionist surveys; for example, by using in vitro or animal studies.

          Supplementary information

          The online version of this article (doi:10.1038/nrmicro.2017.14) contains supplementary material, which is available to authorized users.

          Abstract

          The respiratory tract spans from the nostrils to the lung alveoli and these distinct niches host a diverse microbiota. In this Review, Man, de Steenhuijsen Piters and Bogaert discuss the role of the respiratory microbiota in the maintenance of human health.

          Supplementary information

          The online version of this article (doi:10.1038/nrmicro.2017.14) contains supplementary material, which is available to authorized users.

          Abstract

          The respiratory tract is a complex organ system that is responsible for the exchange of oxygen and carbon dioxide. The human respiratory tract spans from the nostrils to the lung alveoli and is inhabited by niche-specific communities of bacteria. The microbiota of the respiratory tract probably acts as a gatekeeper that provides resistance to colonization by respiratory pathogens. The respiratory microbiota might also be involved in the maturation and maintenance of homeostasis of respiratory physiology and immunity. The ecological and environmental factors that direct the development of microbial communities in the respiratory tract and how these communities affect respiratory health are the focus of current research. Concurrently, the functions of the microbiome of the upper and lower respiratory tract in the physiology of the human host are being studied in detail. In this Review, we will discuss the epidemiological, biological and functional evidence that support the physiological role of the respiratory microbiota in the maintenance of human health.

          Supplementary information

          The online version of this article (doi:10.1038/nrmicro.2017.14) contains supplementary material, which is available to authorized users.

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          Most cited references113

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          Microbiota regulates immune defense against respiratory tract influenza A virus infection.

          Although commensal bacteria are crucial in maintaining immune homeostasis of the intestine, the role of commensal bacteria in immune responses at other mucosal surfaces remains less clear. Here, we show that commensal microbiota composition critically regulates the generation of virus-specific CD4 and CD8 T cells and antibody responses following respiratory influenza virus infection. By using various antibiotic treatments, we found that neomycin-sensitive bacteria are associated with the induction of productive immune responses in the lung. Local or distal injection of Toll-like receptor (TLR) ligands could rescue the immune impairment in the antibiotic-treated mice. Intact microbiota provided signals leading to the expression of mRNA for pro-IL-1β and pro-IL-18 at steady state. Following influenza virus infection, inflammasome activation led to migration of dendritic cells (DCs) from the lung to the draining lymph node and T-cell priming. Our results reveal the importance of commensal microbiota in regulating immunity in the respiratory mucosa through the proper activation of inflammasomes.
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            Alveolar macrophages: plasticity in a tissue-specific context.

            Alveolar macrophages exist in a unique microenvironment and, despite historical evidence showing that they are in close contact with the respiratory epithelium, have until recently been investigated in isolation. The microenvironment of the airway lumen has a considerable influence on many aspects of alveolar macrophage phenotype, function and turnover. As the lungs adapt to environmental challenges, so too do alveolar macrophages adapt to accommodate the ever-changing needs of the tissue. In this Review, we discuss the unique characteristics of alveolar macrophages, the mechanisms that drive their adaptation and the direct and indirect influences of epithelial cells on them. We also highlight how airway luminal macrophages function as sentinels of a healthy state and how they do not respond in a pro-inflammatory manner to antigens that do not disrupt lung structure. The unique tissue location and function of alveolar macrophages distinguish them from other macrophage populations and suggest that it is important to classify macrophages according to the site that they occupy.
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              The maternal microbiota drives early postnatal innate immune development.

              Postnatal colonization of the body with microbes is assumed to be the main stimulus to postnatal immune development. By transiently colonizing pregnant female mice, we show that the maternal microbiota shapes the immune system of the offspring. Gestational colonization increases intestinal group 3 innate lymphoid cells and F4/80(+)CD11c(+) mononuclear cells in the pups. Maternal colonization reprograms intestinal transcriptional profiles of the offspring, including increased expression of genes encoding epithelial antibacterial peptides and metabolism of microbial molecules. Some of these effects are dependent on maternal antibodies that potentially retain microbial molecules and transmit them to the offspring during pregnancy and in milk. Pups born to mothers transiently colonized in pregnancy are better able to avoid inflammatory responses to microbial molecules and penetration of intestinal microbes.
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                Author and article information

                Contributors
                D.Bogaert@ed.ac.uk
                Journal
                Nat Rev Microbiol
                Nat. Rev. Microbiol
                Nature Reviews. Microbiology
                Nature Publishing Group UK (London )
                1740-1526
                1740-1534
                20 March 2017
                2017
                : 15
                : 5
                : 259-270
                Affiliations
                [1 ]GRID grid.417100.3, ISNI 0000 0004 0620 3132, Department of Pediatric Immunology and Infectious Diseases, , Wilhelmina Children's Hospital, University Medical Center Utrecht, ; Lundlaan 6, Utrecht, 3584 EA The Netherlands
                [2 ]GRID grid.416219.9, ISNI 0000 0004 0568 6419, Spaarne Gasthuis Academy, ; Spaarnepoort 1, Hoofddorp, 2134 TM The Netherlands
                [3 ]GRID grid.4305.2, ISNI 0000 0004 1936 7988, The University of Edinburgh/MRC Centre for Inflammation Research, The Queen's Medical Research Institute, ; 47 Little France Crescent, Edinburgh, EH16 4TJ UK
                Article
                BFnrmicro201714
                10.1038/nrmicro.2017.14
                7097736
                28316330
                5c8a700b-d53d-46c3-a8f3-0a69bbd09e8a
                © Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. 2017

                This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.

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                © Springer Nature Limited 2017

                pathogens,microbiome,respiratory tract diseases,clinical microbiology,symbiosis,infectious-disease epidemiology

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