Microbiology of the Built Environment
Like any ecosystem on earth, microorganisms have been found in every part of the built environment that has been studied. They exist in the air, on surfaces and on building materials, usually dispersed by humans, animals, and outdoor sources. Those microbial communities and their metabolites have been implied to cause (or exacerbate) and prevent (or mitigate) human disease. In this Review, Jack Gilbert and I outline the history of the field of microbiology of the built environment and discuss recent insights that have been gained into microbial ecology, adaptation, and evolution.
Jack Gilbert has been studying the microbial ecology of natural environments for most of his career, starting primarily with marine microbial communities and eventually migrating to less exotic locations like kitchen countertops, door knobs, armpits, and feet. I have been studying how buildings work for most of my career, trying to understand the physics, chemistry, and microbiology of what’s in air and on surfaces in the buildings in which we spend the vast majority of our time.
In 2012, our areas of interest overlapped in the Hospital Microbiome Project, funded by the Alfred P. Sloan Foundation, in which our teams combined to collect microbial samples and capture detailed building operational data in a newly constructed hospital in Chicago over the course of a year, both for a couple of months before the hospital opened and for almost a year after it was opened and occupied with doctors, patients, and staff members. We found that the bacteria in patient rooms, particularly on bedrails, consistently resembled the skin microbiota of the patient occupying the room and that the bacterial communities on patients and room surfaces became increasingly similar over the course of a patient’s stay. Patients initially acquired room-associated taxa that predated their stay but then their own microbial signatures began to influence the room community structure over time. There were minimal correlations observed with the detailed built environment data, as human occupancy dominated these complex interactions between surfaces, humans, and indoor air.
We’ve worked together on several projects since then, and our collective interest aligned again to conduct this Review on the Microbiology of the Built Environment. There is a surprisingly long history of research in this field that dates back hundreds of years. Researchers started with visual observations, microscopy, and culture-based techniques, but have recently transitioned to a variety of culture-independent techniques that have addressed new fundamental evolutionary and ecological questions.
In uncovering some of this history, we found records of humanity’s understanding that ‘unclean’ indoor environments can adversely affect human health dating back to ancient times. Even the bible presents the prevailing knowledge that sterilization of building materials – albeit using some rather unconventional methods, including cleansing the walls of a house infected with a ‘plague’ with the blood of a sacrificial bird! – is sometimes warranted to stop the spread of ‘leprous disease’ in a contaminated home (Leviticus Ch. 14, 33-58). This doctrine of sterilization has dominated human efforts to mitigate microbial contamination in buildings for centuries. By the early 1900s, research began to demonstrate how overcrowding, poor ventilation, and contamination of buildings by microorganisms and ‘organic matter’ can lead to infection and disease.
I am always drawn back to a landmark study from 1887, which James Scott at the University of Toronto first turned me on to: “The carbonic acid, organic matter, and micro-organisms air, more especially of dwellings and schools,” by Thomas Carnelley and colleagues. It’s a simple and elegant study that investigated the relationship between over-crowding, occupant activity, ventilation, and airborne concentrations of microorganisms, carbonic acid (a surrogate for CO2), and organic matter (a surrogate for organic particulate matter). They collected microorganisms by pulling air through a glass tube layered with a nutrient solution of ‘meat juice,’ peptone, salt, gelatin, and water (mmm yummy…), incubating what was collected on the jelly, and conducting visual counts of the colonies that grew (see below). We are still studying similar outcomes and relationships today.
We found dozens of other similarly elegant and informative papers throughout our Review. We document how researchers learned to separately count bacteria and fungi via microscopy from samples collected on culture media, then to identify specific bacterial or fungal species from a sample using selective culture media, then used those techniques to investigate the sources, survival and, eventually, means of controlling microorganisms in the built environment. Culture-based investigations dominated studies of bacteria and fungi in the built environment throughout the 2000s (and continues to dominate industrial hygiene sampling), until ribosomal RNA sequencing was discovered, which enabled the identification of previously unculturable microorganisms and cleared the way for a deeper understanding of the complexity of the microbial evolution and ecology of environmental samples.
Jack found that the first sequence-based bacterial community-wide survey of an indoor environment was performed in 2004, in which Scott Kelley at San Diego State University and colleagues conducted a 16S rRNA amplicon survey of the bacterial biofilms associated with the soap-scum film on shower curtains – turns out they belonged to world-renowned human microbiome expert, Professor Ruth Ley. The complex communities that were identified included many alphaproteobacterial genera, such as Sphingomonas and Methylobacterium, which the authors interpreted as potentially contributing to the pink coloration of many of the biofilms. They also highlighted the potential pathogenicity of those bacteria, as closely related strains have been shown to be opportunistic pathogens.
Dozens of studies over the following decade continued to characterize patterns, associations, and drivers of microbial community structures in various built environments, elucidating the most abundant taxa and investigating the similarities and differences of the microbial communities between spaces. We document and describe many of them in our Review. Some highlights include the first metagenomic studies conducted on indoor air samples, the first studies to conduct 16S rDNA amplicon sequencing of reverse transcribed RNA to characterize which microbial organisms are actively transcribing in the built environment, and advances in a number of techniques to visualize microorganisms in situ, to determine their viability and activity, and to apply computational models of microbial metabolism of microbes in the built environment.
Finally, we also consider the implications of this research, specifically, how it is changing the types of materials we use in buildings, how we clean and manage our spaces, and how we understand human health in relation to our built environments. Although many studies have contributed to cataloguing microbial species that can be found in built environments, there has been a recent shift towards investigating the translational potential, as well as creating more fundamental knowledge on how microorganisms biochemically adapt to the resources available in human-made spaces and the impact on their evolution.