|
|
Comparative analysis of impact of human occupancy on indoor microbiomes |
Liu Cao1, Lu Yang1, Clifford S. Swanson1, Shuai Li1( ), Qiang He1,2( ) |
1. Department of Civil and Environmental Engineering, The University of Tennessee, Knoxville, TN 37996, USA 2. Institute for a Secure and Sustainable Environment, The University of Tennessee, Knoxville, TN 37996, USA |
|
|
Abstract • Exposure to indoor microbiomes is a public health concern in educational facilities. • Indoor microbiomes were characterized in two multifunctional university buildings. • Human occupancy had significant impact on the composition of indoor microbiomes. • The skin microbiota of occupants represented important sources of indoor microbiomes. Educational facilities serve as community hubs and consequently hotspots for exposure to pathogenic microorganisms. Therefore, it is of critical importance to understand processes shaping the indoor microbiomes in educational facilities to protect public health by reducing potential exposure risks of students and the broader community. In this study, the indoor surface bacterial microbiomes were characterized in two multifunctional university buildings with contrasting levels of human occupancy, of which one was recently constructed with minimal human occupancy while the other had been in full operation for six years. Higher levels of human occupancy in the older building were shown to result in greater microbial abundance in the indoor environment and greater proportion of the indoor surface bacterial microbiomes contributed from human-associated microbiota, particularly the skin microbiota. It was further revealed that human-associated microbiota had greater influence on the indoor surface bacterial microbiomes in areas of high occupancy than areas of low occupancy. Consistent with minimal impact from human occupancy in a new construction, the indoor microbiomes in the new building exhibited significantly lower influence from human-associated microbiota than in the older building, with microbial taxa originating from soil and plants representing the dominant constituents of the indoor surface bacterial microbiomes. In contrast, microbial taxa in the older building with extensive human occupancy were represented by constituents of the human microbiota, likely from occupants. These findings provide insights into processes shaping the indoor microbiomes which will aid the development of effective strategies to control microbial exposure risks of occupants in educational facilities.
|
Keywords
Built environment
Indoor microbiome
Occupant
Building
Sequencing
|
Corresponding Author(s):
Shuai Li,Qiang He
|
Issue Date: 17 December 2020
|
|
1 |
R I Adams, A C Bateman, H M Bik, J F Meadow (2015). Microbiota of the indoor environment: A meta-analysis. Microbiome, 3: 49
https://doi.org/10.1186/s40168-015-0108-3
|
2 |
A Al Atrouni, M L Joly-Guillou, M Hamze, M Kempf (2016). Reservoirs of non-baumannii Acinetobacter species. Frontiers in Microbiology, 7: 49
https://doi.org/10.3389/fmicb.2016.00049
|
3 |
J G Allen, L C Marr (2020). Recognizing and controlling airborne transmission of SARS-CoV-2 in indoor environments. Indoor Air, 30(4): 557–558
https://doi.org/10.1111/ina.12697
|
4 |
S Q An, G Berg (2018). Stenotrophomonas maltophilia. Trends in Microbiology, 26(7): 637–638
https://doi.org/10.1016/j.tim.2018.04.006
|
5 |
A C Baird‐Parker (1990). The staphylococci: An introduction. Journal of Applied Bacteriology, 69: 1S–8S
https://doi.org/10.1111/j.1365-2672.1990.tb01793.x
|
6 |
K S Bell, J C Philp, D W J Aw, N Christofi (1998). The genus Rhodococcus. Journal of Applied Microbiology, 85(2): 195–210
https://doi.org/10.1046/j.1365-2672.1998.00525.x
|
7 |
S Ben Maamar, J Hu, E M Hartmann (2020). Implications of indoor microbial ecology and evolution on antibiotic resistance. Journal of Exposure Science & Environmental Epidemiology, 30(1): 1–15
https://doi.org/10.1038/s41370-019-0171-0
|
8 |
C C C R de Carvalho, M M R da Fonseca (2005). The remarkable Rhodococcus erythropolis. Applied Microbiology and Biotechnology, 67(6): 715–726
https://doi.org/10.1007/s00253-005-1932-3
|
9 |
J A Gilbert, B Stephens (2018). Microbiology of the built environment. Nature Reviews. Microbiology, 16(11): 661–670
https://doi.org/10.1038/s41579-018-0065-5
|
10 |
J E Graham, J E Moore, X U Jiru, J E Moore, E A Goodall, J S Dooley, V E Hayes, D A Dartt, C S Downes, T C Moore (2007). Ocular pathogen or commensal: a PCR-based study of surface bacterial flora in normal and dry eyes. Investigative Ophthalmology & Visual Science, 48(12): 5616–5623
https://doi.org/10.1167/iovs.07-0588
|
11 |
A C Hayward, N Fegan, M Fegan, G R Stirling (2010). Stenotrophomonas and Lysobacter: Ubiquitous plant-associated gamma-proteobacteria of developing significance in applied microbiology. Journal of Applied Microbiology, 108(3): 756–770
https://doi.org/10.1111/j.1365-2672.2009.04471.x
|
12 |
K M Hewitt, C P Gerba, S L Maxwell, S T Kelley (2012). Office space bacterial abundance and diversity in three metropolitan areas. PLoS One, 7(5): e37849
https://doi.org/10.1371/journal.pone.0037849
|
13 |
Y Hirai (1991). Survival of bacteria under dry conditions; from a viewpoint of nosocomial infection. Journal of Hospital Infection, 19(3): 191–200
https://doi.org/10.1016/0195-6701(91)90223-U
|
14 |
A Hoisington, J P Maestre, K A Kinney, J A Siegel (2016). Characterizing the bacterial communities in retail stores in the United States. Indoor Air, 26(6): 857–868
https://doi.org/10.1111/ina.12273
|
15 |
S W Kembel, E Jones, J Kline, D Northcutt, J Stenson, A M Womack, B J Bohannan, G Z Brown, J L Green (2012). Architectural design influences the diversity and structure of the built environment microbiome. ISME Journal, 6(8): 1469–1479
https://doi.org/10.1038/ismej.2011.211
|
16 |
S W Kembel, J F Meadow, T K O’Connor, G Mhuireach, D Northcutt, J Kline, M Moriyama, G Z Brown, B J M Bohannan, J L Green (2014). Architectural design drives the biogeography of indoor bacterial communities. PLoS One, 9(1): e87093
https://doi.org/10.1371/journal.pone.0087093
|
17 |
N E Klepeis, W C Nelson, W R Ott, J P Robinson, A M Tsang, P Switzer, J V Behar, S C Hern, W H Engelmann (2001). The National Human Activity Pattern Survey (NHAPS): a resource for assessing exposure to environmental pollutants. Journal of Exposure Science & Environmental Epidemiology, 11(3): 231–252
https://doi.org/10.1038/sj.jea.7500165
|
18 |
D Knights, J Kuczynski, E S Charlson, J Zaneveld, M C Mozer, R G Collman, F D Bushman, R Knight, S T Kelley (2011). Bayesian community-wide culture-independent microbial source tracking. Nature Methods, 8(9): 761–763
https://doi.org/10.1038/nmeth.1650
|
19 |
B Krismer, C Weidenmaier, A Zipperer, A Peschel (2017). The commensal lifestyle of Staphylococcus aureus and its interactions with the nasal microbiota. Nature Reviews. Microbiology, 15(11): 675–687
https://doi.org/10.1038/nrmicro.2017.104
|
20 |
S Lax, J A Gilbert (2015). Hospital-associated microbiota and implications for nosocomial infections. Trends in Molecular Medicine, 21(7): 427–432
https://doi.org/10.1016/j.molmed.2015.03.005
|
21 |
S Lax, C R Nagler, J A Gilbert (2015). Our interface with the built environment: immunity and the indoor microbiota. Trends in Immunology, 36(3): 121–123
https://doi.org/10.1016/j.it.2015.01.001
|
22 |
S Lax, D P Smith, J Hampton-Marcell, S M Owens, K M Handley, N M Scott, S M Gibbons, P Larsen, B D Shogan, S Weiss, J L Metcalf, L K Ursell, Y Vazquez-Baeza, W Van Treuren, N A Hasan, M K Gibson, R Colwell, G Dantas, R Knight, J A Gilbert (2014). Longitudinal analysis of microbial interaction between humans and the indoor environment. Science, 345(6200): 1048–1052
https://doi.org/10.1126/science.1254529
|
23 |
C Masson-Boivin, E Giraud, X Perret, J Batut (2009). Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends in Microbiology, 17(10): 458–466
https://doi.org/10.1016/j.tim.2009.07.004
|
24 |
J F Meadow, A E Altrichter, S W Kembel, M Moriyama, T K O’Connor, A M Womack, G Z Brown, J L Green, B J Bohannan (2014). Bacterial communities on classroom surfaces vary with human contact. Microbiome, 2: 7
https://doi.org/10.1186/2049-2618-2-7
|
25 |
D J Reasoner (2004). Heterotrophic plate count methodology in the United States. International Journal of Food Microbiology, 92(3): 307–315
https://doi.org/10.1016/j.ijfoodmicro.2003.08.008
|
26 |
C J C Rodrigues, C C C R de Carvalho (2015). Rhodococcus erythropolis cells adapt their fatty acid composition during biofilm formation on metallic and non-metallic surfaces. FEMS Microbiology Ecology, 91(12): fiv135
https://doi.org/10.1093/femsec/fiv135
|
27 |
L Rose, B Jensen, A Peterson, S N Banerjee, M J Arduino (2004). Swab materials and Bacillus anthracis spore recovery from nonporous surfaces. Emerging Infectious Diseases, 10(6): 1023–1029
https://doi.org/10.3201/eid1006.030716
|
28 |
R P Ryan, S Monchy, M Cardinale, S Taghavi, L Crossman, M B Avison, G Berg, D Van Der Lelie, J M Dow (2009). The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nature Reviews. Microbiology, 7(7): 514–525
https://doi.org/10.1038/nrmicro2163
|
29 |
H Sawada, L D Kuykendall, J M Young (2003). Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. Journal of General and Applied Microbiology, 49(3): 155–179
https://doi.org/10.2323/jgam.49.155
|
30 |
H Sbihi, R C Boutin, C Cutler, M Suen, B B Finlay, S E Turvey (2019). Thinking bigger: How early-life environmental exposures shape the gut microbiome and influence the development of asthma and allergic disease. Allergy, 74(11): 2103–2115
https://doi.org/10.1111/all.13812
|
31 |
C Schweizer, R D Edwards, L Bayer-Oglesby, W J Gauderman, V Ilacqua, M Juhani H K Jantunen, M Lai, N Nieuwenhuijsen, Künzli (2007). Indoor time–microenvironment–activity patterns in seven regions of Europe. Journal of Exposure Science & Environmental Epidemiology, 17(2): 170–181
https://doi.org/10.1038/sj.jes.7500490
|
32 |
L Song, C Wang, Y Wang (2020). Optimized determination of airborne tetracycline resistance genes in laboratory atmosphere. Frontiers of Environmental Science and Engineering, 14(6): 95
|
33 |
K J Towner (2009). Acinetobacter: an old friend, but a new enemy. Journal of Hospital Infection, 73(4): 355–363
https://doi.org/10.1016/j.jhin.2009.03.032
|
34 |
L Treu, P G Kougias, B de Diego-Díaz, S Campanaro, I Bassani, J Fernández-Rodríguez, I Angelidaki (2018). Two-year microbial adaptation during hydrogen-mediated biogas upgrading process in a serial reactor configuration. Bioresource Technology, 264: 140–147
https://doi.org/10.1016/j.biortech.2018.05.070
|
35 |
US Census Bureau (2018). Classrooms More Racially and Ethnically Diverse. Suitland,: US Census Bureau
|
36 |
K N Wyckoff, S Chen, A J Steinman, Q He (2017). Impact of roadway stormwater runoff on microbial contamination in the receiving stream. Journal of Environmental Quality, 46(5): 1065–1071
https://doi.org/10.2134/jeq2017.03.0116
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|