Download PDF Microbiomes of the Built Environment September 15, 2022 Volume 52 Issue 3 The covid-19 pandemic suddenly directed awareness to potential health impacts of the built environment of everyday living – schools, dwellings, offices, public buildings, and other spaces. This issue explores the “microbiome” of the built environment in the postpandemic reality in terms of ventilation performance, filtration, understanding and quantification of transmission risk, protection of “benign” microbes, and the important role of equity, among others. The Future of Microbiomes in the Built Environment Tuesday, September 13, 2022 Author: Robert R. Dunn and Megan S. Thoemmes People need to know how to manage the microbiomes of daily life to favor beneficial species, ignore benign species, and target problem species. The story of microbes in the built environment—including houses and apartments, office buildings, schools, barns, production facilities, and other structures—is a story of people’s conscious and unconscious knowledge of the world. Conscious awareness of microbes as entities is recent, dating from the work of Antonie van Leeuwenhoek (1677). Humans’ unconscious awareness of the surrounding microbial world is far more ancient: it begins with the origin of the vertebrate immune system, hundreds of millions of years ago (Kasahara et al. 2004). Background When immune systems were first discovered and studied, they were viewed as defensive. Consequently, efforts to understand the natural history and evolution of immune systems focused on their responses to pathogens. Over the last few decades, however, it has become clear that immune systems are more nuanced. They recognize microorganisms and respond to them as friend or foe depending not only on the identity of the organisms but also on their behaviors (e.g., which metabolite compounds they happen to produce at any given time in response to various internal and/or external stimuli; Levy et al. 2016). Efforts to fully comprehend the extraordinary sophistication with which immune systems recognize and respond to friends or foes are still in their early stages. However, three things have become clear. First, immune systems can and do recognize a subset of commensal microbes or their products as beneficial (e.g., Peters et al. 2019). Second, in doing so, they not only avoid attacking those organisms but also often provide them food, whether as glycogen in vaginal communities (Miller et al. 2016), mucin or nitrogen in the gut (Reese et al. 2018), or amino acids and lipids on the skin (from the apocrine glands; Barzantny et al. 2012). Third, the responses of human immune systems to microorganisms have evolved over the last 300,000 years in response to changes in the composition of beneficial and dangerous microorganisms in human environments (Brinkworth and Valizadegan 2021; Varki 2009). This microhistory of the subconscious responses of human bodies to the microbes around them is relevant to an understanding of the microbiomes of the built environment because it is exceptionally distinct from conscious responses to microbes. Humans’ Conscious Responses to Microbes Conscious responses to microbes began with the development of germ theory by Louis Pasteur and contemporaries (Gaynes 2011). Germ theory ushered in extraordinarily functional and beneficial social responses such as the control of drinking water systems to reduce the probability of fecal-oral transmission of pathogens, hand washing and other general hygiene practices, and, eventually, vaccinations and the development and use of antibiotics (Dunn 2018). Collectively, these interventions have saved hundreds of millions of lives. However, compared to the responses of the human immune system to the microbial world, they remain unsophisticated. Rather than being tailored to favor some microbes and disfavor others, most of these interventions, with the exception of vaccines, focus on killing microbes in general. Medicine’s very successful but largely unsophisticated efforts to control pathogens eventually became part of a broader cultural response to microbes. Efforts to kill microbes were generalized in ways that affected not just drinking water or human bodies but also the built environments in which humans now spend most of their lives (Dunn 2018). This transition built on efforts to take disease control efforts from sanatoriums and apply them in houses (it has been argued that Modernist architecture emerges from sanatorium architecture; Colomina 2019). In addition, efforts to control all microbes in houses were heightened by the advertisement campaigns of companies selling “cleaning” products. Then the marketing of cleaning products for houses and those for bodies were entangled and interwoven. In much the same way that antiperspirant, which works by closing the apocrine glands that evolved to feed skin microbes (Kong 2011; McGrath 2009), is now sold to large populations who have apocrine glands that do not produce such food, cleaning products are sold for houses to kill dangerous microbes, whether or not such microbes are likely to be present. Differentiating between Harmful and Beneficial Microbes Scientists have finally begun—like the human immune system—to recognize which bodily and environmental microbes are beneficial for human health. For example, it is now known that the microbes associated with some fermented foods enrich beneficial bacteria in the gut and promote healthy digestive functions (Marco et al. 2017). Conversely, studies have reported the negative effects for health and well-being of losing certain microbial taxa (Haahtela et al. 2015; von Mutius and Vercelli 2010). Compared to the responses of the human immune system to the microbial world, conscious interventions are unsophisticated. Understanding is also emerging about the extent to which the microbes encountered in modern homes differ from those our ancestors would have encountered. Studies of chimpanzee beds suggest that human ancestors are likely to have been predominantly exposed to leaf and soil-associated species for millions of years (Thoemmes et al. 2018). As humans began to gather in larger densities, those leaf and soil species began to be accompanied by larger numbers of pathogens. Globally, humans are now afflicted by problems stemming from more than 1400 pathogen species, compared to the tens of pathogen species that are currently known to afflict chimpanzees and almost certainly afflicted our common ancestors (Dunn et al. 2017). Clean drinking water, personal hygiene, antibiotics, and vaccinations have brought the vast majority of these pathogens under control in much of the world. At the same time, houses became tightly sealed and humans began to spend more of their daily lives indoors (95 percent of their lives, in many regions; Klepeis et al. 2001). The result is that the microbes people predominantly encounter in their daily lives are species associated with human bodies and pets (Dunn et al. 2013; Lax et al. 2014, 2017; Richardson et al. 2019), along with extremophiles associated with, for example, water heaters, refrigerators, freezers (Savage et al. 2016), and dishwashers (Raghupathi et al. 2018). The International Space Station is an extreme version of this reality, where the microbial environment is dominated by body microbes (Checinska et al. 2015). The loss of exposure to key microbes is associated with problems of gut health, skin health, and even mental health. With increased sanitation and restrictive measures to prevent microbial contamination from terrestrial sources, there is little to no opportunity for leaf or soil microbes to enter and colonize air and surface environments. Yet exposure to these same microbes is increasingly recognized as key to immune health (Haahtela et al. 2015). Impacts of the Covid-19 Pandemic By the time the covid-19 pandemic began, microbiologists around the world had already begun to study ways to reintroduce beneficial microbes into people’s daily lives. Researchers assessed the value of biodiverse plantings outdoors (Hanski et al. 2012), of probiotics and microbial foods (Marco et al. 2017), of opening windows (Richardson et al. 2019), and even of household probiotics (Caselli et al. 2018). These studies recognize that the loss of exposure to key microbes is associated with problems of gut health, skin health, and even mental health. Yet, a holistic understanding of which species should be reintroduced to create healthy buildings is still nascent. The subconscious human body may have fine-tuned “understandings” of which species to favor and disfavor, but the conscious minds of scientists have no such consensus. Prior to the onset of the covid-19 pandemic, the scientific community was making progress in understanding the impacts of daily human practices on the microbiomes that surround us, and the mainstream Western world seemed eager to embrace ways in which cultivating a particular microbial community in the home might be beneficial. At the same time an increasing number of studies had begun to detail the problems associated with the absence of key microbes, whether in human bodies or in dwellings. Then, as covid-19 spread around the world, the long tendency of Western humans to kill microbes in general, rather than just pathogens, accelerated (Chang et al. 2020). During the first 2 years (and continuing today) many individuals, perhaps most, moved toward behaviors in their homes that more closely resemble the ways in which one might clean a hospital room, a sanatorium, or a space station—even as products aimed at favoring microbes have become more popular, whether as skin creams, oral probiotics, or microbial foods. Concluding Thoughts We perceive that this is a time of general cognitive dissonance, when many individuals are trying to kill all the microscopic life around them and, at the same time, paying for products that favor some species. It is clear that in the long term people need to understand how to manage the microbiomes of daily life in more sophisticated ways to favor beneficial species, ignore benign species, and strategically target problem species. We expect that this challenge will remain twofold. First, unlike the human immune system, is it not yet feasible for humans to see microbial life in the environs in real time in ways that make obvious and conscious the difference between beneficial and harmful. Second, understanding of what is beneficial and harmful is nascent. At this point it is almost certainly true that, so long as you washed your hands with soap and water and had a source of drinking water that was free of pathogens, sleeping in a bed built like a chimpanzee nest would be healthier than any modern home thus far designed. References Barzantny H, Brune I, Tauch A. 2012. Molecular basis of human body odour formation: Insights deduced from corynebacterial genome sequences. International Journal of Cosmetic Science 34(1):2–11. Brinkworth JF, Valizadegan N. 2021. Sepsis and the evolution of human increased sensitivity to lipopolysaccharide. Evolutionary Anthropology 30(2):141–57. 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Glycoconjugate Journal 26(3):231–45. von Mutius E, Vercelli D. 2010. Farm living: Effects on childhood asthma and allergy. Nature Reviews Immunology 10(12):861–68.  Editorial: Microbiology by numbers. Nature Reviews -Microbiology 9:628 (2011). About the Author:Robert Dunn is the William Neal Reynolds Distinguished Professor, Department of Applied Ecology, North Carolina State University. Megan Thoemmes is a postdoctoral scholar, Department of Pediatrics and Scripps Institution of Oceanography, University of California San Diego School of Medicine.