Implications of indoor microbial ecology and evolution on antibiotic resistance

Abstract

The indoor environment is an important source of microbial exposures for its human occupants. While we naturally want to favor positive health outcomes, built environment design and operation may counter-intuitively favor negative health outcomes, particularly with regard to antibiotic resistance. Indoor environments contain microbes from both human and non-human origins, providing a unique venue for microbial interactions, including horizontal gene transfer. Furthermore, stressors present in the built environment could favor the exchange of genetic material in general and the retention of antibiotic resistance genes in particular. Intrinsic and acquired antibiotic resistance both pose a potential threat to human health; these phenomena need to be considered and controlled separately. The presence of both environmental and human-associated microbes, along with their associated antibiotic resistance genes, in the face of stressors, including antimicrobial chemicals, creates a unique opportunity for the undesirable spread of antibiotic resistance. In this review, we summarize studies and findings related to various interactions between human-associated bacteria, environmental bacteria, and built environment conditions, and particularly their relation to antibiotic resistance, aiming to guide "healthy" building design.

Fig. 1

Bacteria from indoor and outdoor sources encounter various stressors in the built environment. The flux of bacteria in the built environment (black arrows), includes sources such as humans (and pets if any) and outdoor air or outdoor environments. While in the built environment, these bacteria from different origins may experience specific selective pressures or stressors (red), including exposure to UV light or luminance in general, low humidity, temperature variation, and the presence of various chemicals such as antimicrobials. Exposure to these stressors may induce the transfer of mobile genetic elements (center)

Fig. 2

Climate change has implications for indoor environmental quality, including the indoor microbiome. Climate change has prompted innovations in building design and operation to increase energy efficiency. These innovations, such as increased natural lighting and tightened building envelopes may change the conditions experienced by microbes, e.g., illuminance and exposure to chemical stressors. At the same time, changing climate conditions are causing an increase in extreme weather events, leading to increased moisture damage in buildings. Buildings without adequate temperature control may also be subject to more intense variations in indoor temperatures

Fig. 3

The circulation of bacteria, genes, and antibiotic resistance in the built environment. Indoor bacteria come from both human and environmental sources (1). Once deposited in the indoor environment, there is potential for human exposure (2). In the built environment, mobile genetic elements can be transferred from environmental to host-associated bacteria and vice versa; genetic material can also be taken up by human-associated bacteria upon contact with the indoor microbiome (3). Antimicrobial resistance can be transferred between viable, active bacteria (green) or from nonviable bacteria (white) to viable, inactive bacteria. Viable, inactive bacteria are unlikely to participate in the transfer of mobile genetic elements but may nevertheless be phenotypically resistant to antimicrobials

Fig. 4

Stress may increase the human health risk posed by bacteria, but exposure to a diverse microbiome likely confers benefits. a Many stresses can induce horizontal gene transfer in bacteria, potentially increasing the spread of antibiotic resistance even when those genes do not confer a direct benefit. However, horizontal gene transfer can only occur until the intensity of the stress becomes high enough to inhibit bacterial survival. b A previously unexposed human (i.e., neonate) benefits rapidly from a high diversity of microbial exposures, as it allows acquired immunity to develop. Regular exposure to a relatively high-bacterial alpha-diversity helps maintain the acquired immunity over time. However, continued exposure to a high diversity of bacteria increases the chance of exposure to pathogens