Relative and contextual contribution of different sources to the composition and abundance of indoor air bacteria in residences

BackgroundThe study of the microbial communities in the built environment is of critical importance as humans spend the majority of their time indoors. While the microorganisms in living spaces, especially those in the air, can impact health and well-being, little is known of their identity and the processes that determine their assembly. We investigated the source-sink relationships of airborne bacteria in 29 homes in the San Francisco Bay Area. Samples taken in the sites expected to be source habitats for indoor air microbes were analyzed by 16S rRNA-based pyrosequencing and quantitative PCR. The community composition was related to the characteristics of the household collected at the time of sampling, including the number of residents and pets, activity levels, frequency of cooking and vacuum cleaning, extent of natural ventilation, and abundance and type of vegetation surrounding the building.ResultsIndoor air harbored a diverse bacterial community dominated by Diaphorobacter sp., Propionibacterium sp., Sphingomonas sp., and Alicyclobacillus sp. Source-sink analysis suggested that outdoor air was the primary source of indoor air microbes in most homes. Bacterial phylogenetic diversity and relative abundance in indoor air did not differ statistically from that in outdoor air. Moreover, the abundance of bacteria in outdoor air was positively correlated with that in indoor air, as would be expected if outdoor air was the main contributor to the bacterial community in indoor bioaerosols. The number of residents, presence of pets, and local tap water also influenced the diversity and size of indoor air microbes. The bacterial load in air increased with the number of residents, activity, and frequency of natural ventilation, and the proportion of bacteria putatively derived from skin increased with the number of residents. Vacuum cleaning increased the signature of pet- and floor-derived bacteria in indoor air, while the frequency of natural ventilation decreased the relative abundance of tap water-derived microorganisms in air.ConclusionsIndoor air in residences harbors a diverse bacterial community originating from both outdoor and indoor sources and is strongly influenced by household characteristics.

[1]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[2]  D. Lane.  16S/23S rRNA sequencing , 1991 .

[3]  R. Saranathan,et al.  The expanding spectrum of human infections caused by Kocuria species: a case report and literature review , 2013, Emerging microbes & infections.

[4]  Lidia Morawska,et al.  Vacuum cleaner emissions as a source of indoor exposure to airborne particles and bacteria. , 2012, Environmental Science and Technology.

[5]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[6]  M. Egert,et al.  A glimpse under the rim – the composition of microbial biofilm communities in domestic toilets , 2010, Journal of applied microbiology.

[7]  Se Jin Song,et al.  Cohabiting family members share microbiota with one another and with their dogs , 2013, eLife.

[8]  William W. Nazaroff,et al.  Human Occupancy as a Source of Indoor Airborne Bacteria , 2012, PloS one.

[9]  Jeff Kline,et al.  Architectural design influences the diversity and structure of the built environment microbiome , 2012, The ISME Journal.

[10]  J. Gent,et al.  Influence of housing characteristics on bacterial and fungal communities in homes of asthmatic children. , 2016, Indoor air.

[11]  M. Deloge-Abarkan,et al.  Detection of airborne Legionella while showering using liquid impingement and fluorescent in situ hybridization (FISH). , 2007, Journal of environmental monitoring : JEM.

[12]  H. Weon,et al.  Roseomonas aerophila sp. nov., isolated from air. , 2013, International journal of systematic and evolutionary microbiology.

[13]  Rob Knight,et al.  PyNAST: a flexible tool for aligning sequences to a template alignment , 2009, Bioinform..

[14]  M. Sekine,et al.  Complete Genome Sequence of the Soil Actinomycete Kocuria rhizophila , 2008, Journal of bacteriology.

[15]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[16]  Akira Yokota,et al.  Proposal of six species of moderately thermophilic, acidophilic, endospore-forming bacteria: Alicyclobacillus contaminans sp. nov., Alicyclobacillus fastidiosus sp. nov., Alicyclobacillus kakegawensis sp. nov., Alicyclobacillus macrosporangiidus sp. nov., Alicyclobacillus sacchari sp. nov. and Alicy , 2007, International journal of systematic and evolutionary microbiology.

[17]  M. Pitkäranta,et al.  Microbial communities associated with house dust. , 2013, Advances in applied microbiology.

[18]  B. Haas,et al.  Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. , 2011, Genome research.

[19]  M. McNutt.  New members of the family , 2016, Science.

[20]  Patrick K. H. Lee,et al.  Indoor air bacterial communities in Hong Kong households assemble independently of occupant skin microbiomes. , 2016, Environmental microbiology.

[21]  N. Pace,et al.  Molecular analysis of point-of-use municipal drinking water microbiology. , 2014, Water research.

[22]  Rob Knight,et al.  Microbial Biogeography of Public Restroom Surfaces , 2011, PloS one.

[23]  Jack A. Gilbert,et al.  Ecological Succession and Viability of Human-Associated Microbiota on Restroom Surfaces , 2014, Applied and Environmental Microbiology.

[24]  Steven E. Lindow,et al.  Airborne Bacterial Communities in Residences: Similarities and Differences with Fungi , 2014, PloS one.

[25]  Diaphorobacter ruginosibacter sp. nov., isolated from soybean root nodule, and emended description of the genus Diaphorobacter , 2015, Archives of Microbiology.

[26]  John R. Battista,et al.  Extensive Diversity of Ionizing-Radiation-Resistant Bacteria Recovered from Sonoran Desert Soil and Description of Nine New Species of the Genus Deinococcus Obtained from a Single Soil Sample , 2005, Applied and Environmental Microbiology.

[27]  L. Hildemann,et al.  The effects of human activities on exposure to particulate matter and bioaerosols in residential homes. , 2009, Environmental science & technology.

[28]  A. Ventosa,et al.  Roseomonas aquatica sp. nov., isolated from drinking water. , 2006, International journal of systematic and evolutionary microbiology.

[29]  Campbell O. Webb,et al.  Picante: R tools for integrating phylogenies and ecology , 2010, Bioinform..

[30]  James F. Meadow,et al.  Indoor airborne bacterial communities are influenced by ventilation, occupancy, and outdoor air source , 2013, Indoor air.

[31]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[32]  D. Balkwill,et al.  Sphingomonas and related genera , 2003 .

[33]  John W Taylor,et al.  Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. , 2013, The ISME journal.

[34]  Rob Knight,et al.  The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. , 2010, Environmental microbiology.

[35]  M. Takeuchi,et al.  Proposal of six new species in the genus Microbacterium and transfer of Flavobacterium marinotypicum ZoBell and Upham to the genus Microbacterium as Microbacterium maritypicum comb. nov. , 1998, International journal of systematic bacteriology.

[36]  P. Kämpfer,et al.  Classification of three airborne bacteria and proposal of Hymenobacter aerophilus sp. nov. , 2002, International journal of systematic and evolutionary microbiology.

[37]  Patrick K. H. Lee,et al.  Indoor-Air Microbiome in an Urban Subway Network: Diversity and Dynamics , 2014, Applied and Environmental Microbiology.

[38]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[39]  K. Schleifer,et al.  The Genera Staphylococcus and Macrococcus , 2006, The Prokaryotes.

[40]  William W. Nazaroff,et al.  Chamber Bioaerosol Study: Outdoor Air and Human Occupants as Sources of Indoor Airborne Microbes , 2015, PloS one.

[41]  Claudine Médigue,et al.  Genome Sequence of Radiation-Resistant Modestobacter marinus Strain BC501, a Representative Actinobacterium That Thrives on Calcareous Stone Surfaces , 2012, Journal of bacteriology.

[42]  D. Fennell,et al.  Substrate-Dependent rRNA Production in an Airborne Bacterium , 2014 .

[43]  W W Nazaroff,et al.  Chamber bioaerosol study: human emissions of size-resolved fluorescent biological aerosol particles. , 2016, Indoor air.

[44]  F. Rainey,et al.  The genus paracoccus , 2002 .

[45]  Katherine H. Huang,et al.  Structure, Function and Diversity of the Healthy Human Microbiome , 2012, Nature.

[46]  D. Lovley,et al.  Molecular Analysis of the Metabolic Rates of Discrete Subsurface Populations of Sulfate Reducers , 2011, Applied and Environmental Microbiology.

[47]  K. R. Clarke,et al.  Non‐parametric multivariate analyses of changes in community structure , 1993 .

[48]  J. Janda.  New Members of the Family Enterobacteriaceae , 2006 .

[49]  James F. Meadow,et al.  Mobile phones carry the personal microbiome of their owners , 2014, PeerJ.

[50]  Jason Stenson,et al.  Humans differ in their personal microbial cloud , 2015, PeerJ.

[51]  Rob Knight,et al.  Bayesian community-wide culture-independent microbial source tracking , 2011, Nature Methods.

[52]  J. Gilbert,et al.  Athletic equipment microbiota are shaped by interactions with human skin , 2015, Microbiome.

[53]  Noah Fierer,et al.  Home Life: Factors Structuring the Bacterial Diversity Found within and between Homes , 2013, PloS one.

[54]  R. Knight,et al.  Forensic identification using skin bacterial communities , 2010, Proceedings of the National Academy of Sciences.

[55]  M. L. Laucks,et al.  Aerosol Technology Properties, Behavior, and Measurement of Airborne Particles , 2000 .

[56]  K. Jones,et al.  Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review , 2008, Journal of applied microbiology.

[57]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[58]  Rob Knight,et al.  Longitudinal analysis of microbial interaction between humans and the indoor environment , 2014, Science.

[59]  E. Stackebrandt,et al.  Friedmanniella antarctica gen. nov., sp. nov., an LL-diaminopimelic acid-containing actinomycete from Antarctic sandstone. , 1997, International journal of systematic bacteriology.

[60]  G. Berg,et al.  Beneficial effects of plant-associated microbes on indoor microbiomes and human health? , 2014, Front. Microbiol..

[61]  B. Bohannan,et al.  Biodiversity and biogeography of the atmosphere , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[62]  Leah M. Feazel,et al.  Opportunistic pathogens enriched in showerhead biofilms , 2009, Proceedings of the National Academy of Sciences.

[63]  Rob Knight,et al.  Diversity, distribution and sources of bacteria in residential kitchens. , 2013, Environmental microbiology.

[64]  Christine Wiedinmyer,et al.  Seasonal variability in bacterial and fungal diversity of the near-surface atmosphere. , 2013, Environmental science & technology.

[65]  M. Gillis,et al.  The genera Chromobacterium and Janthinobacterium. , 1992 .