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      Ecological Analyses of Mycobacteria in Showerhead Biofilms and Their Relevance to Human Health

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          Abstract

          Bacteria thrive in showerheads and throughout household water distribution systems. While most of these bacteria are innocuous, some are potential pathogens, including members of the genus Mycobacterium that can cause nontuberculous mycobacterial (NTM) lung infection, an increasing threat to public health. We found that showerheads in households across the United States and Europe often harbor abundant mycobacterial communities that vary in composition depending on geographic location, water chemistry, and water source, with households receiving water treated with chlorine disinfectants having particularly high abundances of certain mycobacteria. The regions in the United States where NTM lung infections are most common were the same regions where pathogenic mycobacteria were most prevalent in showerheads, highlighting the important role of showerheads in the transmission of NTM infections.

          ABSTRACT

          Bacteria within the genus Mycobacterium can be abundant in showerheads, and the inhalation of aerosolized mycobacteria while showering has been implicated as a mode of transmission in nontuberculous mycobacterial (NTM) lung infections. Despite their importance, the diversity, distributions, and environmental predictors of showerhead-associated mycobacteria remain largely unresolved. To address these knowledge gaps, we worked with citizen scientists to collect showerhead biofilm samples and associated water chemistry data from 656 households located across the United States and Europe. Our cultivation-independent analyses revealed that the genus Mycobacterium was consistently the most abundant genus of bacteria detected in residential showerheads, and yet mycobacterial diversity and abundances were highly variable. Mycobacteria were far more abundant, on average, in showerheads receiving municipal water than in those receiving well water and in U.S. households than in European households, patterns that are likely driven by differences in the use of chlorine disinfectants. Moreover, we found that water source, water chemistry, and household location also influenced the prevalence of specific mycobacterial lineages detected in showerheads. We identified geographic regions within the United States where showerheads have particularly high abundances of potentially pathogenic lineages of mycobacteria, and these “hot spots” generally overlapped those regions where NTM lung disease is most prevalent. Together, these results emphasize the public health relevance of mycobacteria in showerhead biofilms. They further demonstrate that mycobacterial distributions in showerhead biofilms are often predictable from household location and water chemistry, knowledge that advances our understanding of NTM transmission dynamics and the development of strategies to reduce exposures to these emerging pathogens.

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          Most cited references 47

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          Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex.

          We constructed error-correcting DNA barcodes that allow one run of a massively parallel pyrosequencer to process up to 1,544 samples simultaneously. Using these barcodes we processed bacterial 16S rRNA gene sequences representing microbial communities in 286 environmental samples, corrected 92% of sample assignment errors, and thus characterized nearly as many 16S rRNA genes as have been sequenced to date by Sanger sequencing.
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            Rapid identification of mycobacteria to the species level by polymerase chain reaction and restriction enzyme analysis.

             A Telenti,  F Bally,  M Balz (1993)
            A method for the rapid identification of mycobacteria to the species level was developed on the basis of evaluation by the polymerase chain reaction (PCR) of the gene encoding for the 65-kDa protein. The method involves restriction enzyme analysis of PCR products obtained with primers common to all mycobacteria. Using two restriction enzymes, BstEII and HaeIII, medically relevant and other frequent laboratory isolates were differentiated to the species or subspecies level by PCR-restriction enzyme pattern analysis. PCR-restriction enzyme pattern analysis was performed on isolates (n = 330) from solid and fluid culture media, including BACTEC, or from frozen and lyophilized stocks. The procedure does not involve hybridization steps or the use of radioactivity and can be completed within 1 working day.
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              Opportunistic pathogens enriched in showerhead biofilms.

              The environments we humans encounter daily are sources of exposure to diverse microbial communities, some of potential concern to human health. In this study, we used culture-independent technology to investigate the microbial composition of biofilms inside showerheads as ecological assemblages in the human indoor environment. Showers are an important interface for human interaction with microbes through inhalation of aerosols, and showerhead waters have been implicated in disease. Although opportunistic pathogens commonly are cultured from shower facilities, there is little knowledge of either their prevalence or the nature of other microorganisms that may be delivered during shower usage. To determine the composition of showerhead biofilms and waters, we analyzed rRNA gene sequences from 45 showerhead sites around the United States. We find that variable and complex, but specific, microbial assemblages occur inside showerheads. Particularly striking was the finding that sequences representative of non-tuberculous mycobacteria (NTM) and other opportunistic human pathogens are enriched to high levels in many showerhead biofilms, >100-fold above background water contents. We conclude that showerheads may present a significant potential exposure to aerosolized microbes, including documented opportunistic pathogens. The health risk associated with showerhead microbiota needs investigation in persons with compromised immune or pulmonary systems.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                30 October 2018
                Sep-Oct 2018
                : 9
                : 5
                Affiliations
                [a ]Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA
                [b ]Departamento de Biología y Geología, Física y Química Inorgánica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Móstoles, Spain
                [c ]Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA
                [d ]Department of Applied Ecology, North Carolina State University, Raleigh, North Carolina, USA
                [e ]Department of Biomedical Research, Center for Genes, Environment, and Health, National Jewish Health, Denver, Colorado, USA
                [f ]Department of Medicine, National Jewish Health, Denver, Colorado, USA
                [g ]Division of Pulmonary Sciences and Critical Care Medicine, University of Colorado Denver, Aurora, Colorado, USA
                [h ]Denver Veterans Affairs Medical Center, Denver, Colorado, USA
                [i ]National Institute of Allergy and Infectious Diseases, Bethesda, Maryland, USA
                [j ]United States Public Health Service Commissioned Corps, Rockville, Maryland, USA
                [k ]Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
                University of Georgia
                Author notes
                Address correspondence to Noah Fierer, Noah.Fierer@ 123456colorado.edu .
                Article
                mBio01614-18
                10.1128/mBio.01614-18
                6212831
                30377276
                Copyright © 2018 Gebert et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                Page count
                supplementary-material: 10, Figures: 5, Tables: 0, Equations: 0, References: 70, Pages: 15, Words: 10600
                Product
                Funding
                Funded by: U.S. Department of Defense (DOD), https://doi.org/10.13039/100000005;
                Award Recipient :
                Categories
                Research Article
                Ecological and Evolutionary Science
                Custom metadata
                September/October 2018

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