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      Cohabiting family members share microbiota with one another and with their dogs

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          Abstract

          Human-associated microbial communities vary across individuals: possible contributing factors include (genetic) relatedness, diet, and age. However, our surroundings, including individuals with whom we interact, also likely shape our microbial communities. To quantify this microbial exchange, we surveyed fecal, oral, and skin microbiota from 60 families (spousal units with children, dogs, both, or neither). Household members, particularly couples, shared more of their microbiota than individuals from different households, with stronger effects of co-habitation on skin than oral or fecal microbiota. Dog ownership significantly increased the shared skin microbiota in cohabiting adults, and dog-owning adults shared more ‘skin’ microbiota with their own dogs than with other dogs. Although the degree to which these shared microbes have a true niche on the human body, vs transient detection after direct contact, is unknown, these results suggest that direct and frequent contact with our cohabitants may significantly shape the composition of our microbial communities.

          DOI: http://dx.doi.org/10.7554/eLife.00458.001

          eLife digest

          The human body is home to many different microorganisms, with a range of bacteria, fungi and archaea living on the skin, in the intestine and at various other sites in the body. While many of these microorganisms are beneficial to their human hosts, we know very little about most of them. Early research focused primarily on comparing the microorganisms found in healthy individuals with those found in individuals suffering from a particular illness. More recently researchers have become interested in more general issues, such as understanding how these collections of microorganisms, which are also known as the human microbiota or the human microbiome, become established, and exploring the causes of similarities and differences between the microbiota of individuals.

          We now know that the communities of microorganisms found in the intestines of genetically related people tend to be more similar than those of people who are not related. Moreover, the communities of microorganisms found in the intestines of non-related adults living in the same household are more similar than those of unrelated adults living in different households. We also know that the range of microorganisms found in the intestine changes dramatically between birth and the age of 3 years. However, these studies have focused on the intestine, and little is known about the effect of relatedness, cohabitation and age on the microbiota at other body sites.

          Song et al. compared the microorganisms found on the skin, on the tongue and in the intestines of 159 people—and 36 dogs—in 60 families. They found that co-habitation resulted in the communities of microorganisms being more similar to each other, with those on the skin being the most similar. This was true for all comparisons, including human pairs, dog pairs and human–dog pairs. This suggests that humans probably acquire many of the microorganisms on their skin through direct contact with their surroundings, and that humans tend to share more microbes with individuals, including their pets, with which they are in frequent contact. Song et al. also discovered that, unlike what happens in the intestine, the microbial communities on the skin and tongue of infants and children were relatively similar to those of adults. Overall, these findings suggest that the communities of microorganisms found in the intestine changes with age in a way that differs significantly from those found on the skin and tongue.

          DOI: http://dx.doi.org/10.7554/eLife.00458.002

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          Most cited references10

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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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            Diversity of the human gastrointestinal tract microbiota revisited.

            Since the early days of microbiology, more than a century ago, representatives of over 400 different microbial species have been isolated and fully characterized from human gastrointestinal samples. However, during the past decade molecular ecological studies based on ribosomal RNA (rRNA) sequences have revealed that cultivation has been able only to access a small fraction of the microbial diversity within the gastrointestinal tract. The increasing number of deposited rRNA sequences calls for the setting up a curated database that allows handling of the excessive degree of redundancy that threatens the usability of public databases. The integration of data from cultivation-based studies and molecular inventories of small subunit (SSU) rRNA diversity, presented here for the first time, provides a systematic framework of the microbial diversity in the human gastrointestinal tract of more than 1000 different species-level phylogenetic types (phylotypes). Such knowledge is essential for the design of high-throughput approaches such as phylogenetic DNA microarrays for the comprehensive analysis of gastrointestinal tract microbiota at multiple levels of taxonomic resolution. Development of such approaches is likely to be pivotal to generating novel insights in microbiota functionality in health and disease.
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              Microbial Biogeography of Public Restroom Surfaces

              We spend the majority of our lives indoors where we are constantly exposed to bacteria residing on surfaces. However, the diversity of these surface-associated communities is largely unknown. We explored the biogeographical patterns exhibited by bacteria across ten surfaces within each of twelve public restrooms. Using high-throughput barcoded pyrosequencing of the 16 S rRNA gene, we identified 19 bacterial phyla across all surfaces. Most sequences belonged to four phyla: Actinobacteria, Bacteriodetes, Firmicutes and Proteobacteria. The communities clustered into three general categories: those found on surfaces associated with toilets, those on the restroom floor, and those found on surfaces routinely touched with hands. On toilet surfaces, gut-associated taxa were more prevalent, suggesting fecal contamination of these surfaces. Floor surfaces were the most diverse of all communities and contained several taxa commonly found in soils. Skin-associated bacteria, especially the Propionibacteriaceae, dominated surfaces routinely touched with our hands. Certain taxa were more common in female than in male restrooms as vagina-associated Lactobacillaceae were widely distributed in female restrooms, likely from urine contamination. Use of the SourceTracker algorithm confirmed many of our taxonomic observations as human skin was the primary source of bacteria on restroom surfaces. Overall, these results demonstrate that restroom surfaces host relatively diverse microbial communities dominated by human-associated bacteria with clear linkages between communities on or in different body sites and those communities found on restroom surfaces. More generally, this work is relevant to the public health field as we show that human-associated microbes are commonly found on restroom surfaces suggesting that bacterial pathogens could readily be transmitted between individuals by the touching of surfaces. Furthermore, we demonstrate that we can use high-throughput analyses of bacterial communities to determine sources of bacteria on indoor surfaces, an approach which could be used to track pathogen transmission and test the efficacy of hygiene practices.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                16 April 2013
                2013
                : 2
                : e00458
                Affiliations
                [1 ]Department of Ecology and Evolutionary Biology, University of Colorado, Boulder , Boulder, United States
                [2 ]Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder , Boulder, United States
                [3 ]Department of Microbiology and Immunology, Stanford University School of Medicine , Stanford, United States
                [4 ]Department of Chemistry and Biochemistry, University of Colorado, Boulder , Boulder, United States
                [5 ]Department of Computer Science, Northern Arizona University , Flagstaff, United States
                [6 ]Argonne National Laboratory, Institute for Genomics and Systems Biology , Argonne, United States
                [7 ]Department of Computer Science and Engineering, University of Minnesota , Minneapolis, United States
                [8 ]BioTechnology Institute, University of Minnesota , Saint Paul, United States
                [9 ]Department of Biochemistry and Biophysics, Howard Hughes Medical Institute, University of California, San Francisco , San Francisco, United States
                [10 ]Center for Genome Sciences and Systems Biology, Washington University School of Medicine , St. Louis, United States
                [11 ]Department of Chemistry and Biochemistry, Howard Hughes Medical Institute, University of Colorado, Boulder , Boulder, United States
                [12 ]Biofrontiers Institute, University of Colorado, Boulder , Boulder, United States
                Max Planck Institute for Developmental Biology , Germany
                Max Planck Institute for Developmental Biology , Germany
                Author notes
                [* ]For correspondence: rob.knight@ 123456colorado.edu
                [a]

                Mount Sinai School of Medicine, New York, United States.

                [b]

                Division of Biomedical Informatics and Personalized Medicine, Department of Medicine, Anschutz Medical Campus, University of Colorado, Denver, United States.

                Article
                00458
                10.7554/eLife.00458
                3628085
                23599893
                f8d65185-00bb-48ed-bc11-5ca899612923
                Copyright © 2013, Song et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 13 December 2012
                : 03 March 2013
                Funding
                Funded by: Howard Hughes Medical Institute
                Award Recipient :
                Funded by: Crohn's and Colitis Foundation of America
                Award Recipient :
                Funded by: National Institutes of Health
                Award ID: HG4872, HG4866
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Microbiology and Infectious Disease
                Custom metadata
                1.0
                Research on humans and dogs reveals that the communities of microorganisms found on the skin, on the tongue and in the intestine are affected differently by age and cohabitation.

                Life sciences
                metagenomics,microbial community transmission,environmental microbial reservoirs,family structure,companion animals,human

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