Indoor Air 2014; 24: 113–115 wileyonlinelibrary.com/journal/ina Printed in Singapore. All rights reserved
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd INDOOR AIR doi:10.1111/ina.12090
Editorial Can bioinformed design promote healthy indoor ecosystems? Twenty years ago, as an environmental engineering student at UC Berkeley, I had the opportunity to learn about air quality from William Nazaroff. Back then, class conversation centered on physics and chemistry: modeling the source, fate, and transport of pollutants like ozone, radon, and volatile organic compounds. The limited discussion of biology was focused on ‘microbial agents’ or bioaerosols, and their potential role in the spread of infectious disease and asthma. We were taught that microorganisms – viruses, bacteria, and fungi – were pollutants that should be reduced or eliminated indoors. The conversation is changing. We now understand that microorganisms are not all pollutants; in fact, many are critical to the health and well-being of humans and other organisms. In the not too distant future, students in engineering, design, and science may be presented a fundamentally different model. Rather than asking ‘how can we keep microbes out of the indoor environment?’, students and teachers might ask ‘how can we design the indoor environment to promote beneficial microbes and inhibit harmful ones?’ I call this latter model ‘bioinformed design’. There are three reasons I believe we will embrace bioinformed design. First, there has been an explosion of research and public interest focused on host– microbe interactions and in particular the human microbiome – the trillions of microorganisms living in and on our bodies. This trend will continue in the foreseeable future; as a result, knowledge about the types of microbial communities that we may want to cultivate indoors can only improve. Consider the skin microbiome, which is intimately in contact with indoor air and surfaces. Scientists have shown that microbes commonly found on the skin of healthy individuals, like the bacterium Staphylococcus epidermis, can help protect against skin infections and regulate the immune system of their hosts (Schommer and Gallo, 2013). The oral microbiome receives a collection of indoor bioaerosols with every breath (and, albeit less frequently, also from indoor surfaces, particularly with children). Strains of the oral bacteria Streptococcus salivarius have been shown to ward off ear and throat infections (Di Pierro et al., 2012). The gut, which is indirectly connected to the indoor environment, is home to microbes that help to regulate our weight, our immune system, and perhaps even our
brain function and behavior (Foster and McVey Neufeld, 2013). As human microbiome science continues to evolve, this growing body of knowledge can be dynamically integrated into an evolving bioinformed design framework. The second reason I believe we will embrace bioinformed design is due to the rich history of examples where an ecosystem has been managed to achieve some desired result. Entire fields and schools of thought are dedicated, at least in part, to the concept: adaptive ecosystem management, ecological engineering, ecosystem restoration, integrated pest management, agroecology, permaculture, and intervention ecology, to name a few. While the perceived breadth and rigor of these fields varies, below I briefly highlight a few success stories – from farmlands to parks to people – to illustrate the potential. The first example is from agroecology: the agrienvironmental schemes (AES) introduced in Europe in the 1990s. AES provide payments to farmers who subscribe, on a voluntary basis, to practices aimed at enhancing farmland biodiversity. Common practices include sowing wildflower strips along field edges, organic farming, and extensive (versus intensive) grassland management (e.g., restricted herbicide, pesticide, and machinery use). These approaches can have significant positive effects on the diversity and abundance of agroecosystems, particularly for the insects that provide vital pollination services to crops [e.g., bees, butterflies, and moths (Scheper et al., 2013)]. The next example is from wildlife management: the restoration of gray wolves into Yellowstone National Park. Wolves were well established when the park was designated in 1872, but considered pests and decimated by humans. People ultimately realized how crucial this top predator was to ecosystem health; without wolves, elk populations exploded, which in turn led to the overgrazing of deciduous trees like aspen. Restoration of the wolf after a 70-year absence resulted in decreased elk populations, increased tree canopy cover, and an overall increase in the biodiversity of the region (Ripple and Beschta, 2012). The final example is from medicine: fecal microbiota transplantation. In this procedure, microbiota from the stool of a healthy individual is administered (e.g., via pill or enema) to patients who have persistent severe diarrhea caused by an overgrowth of a bacterium called Clostridium difficile. C. difficile infections 113
Editorial are often sparked by taking antibiotics, which can kill the gut’s ‘good’ bacteria. While the exact mechanisms responsible for the success of fecal transplants remain unknown, the process clearly helps transform the gut ecosystem from an unhealthy to a healthy state (Brandt and Aroniadis, 2013). This brings me to the third reason I believe we will embrace indoor bioinformed design. We’re designing indoor microbial ecosystems right now, but we’re doing it unintentionally. We unintentionally shape indoor microbial ecosystems through choices about ventilation. ‘Ventilate well’ is a key principle for achieving good indoor air quality (Nazaroff, 2013). This means, in part, providing ventilation air with low contaminant levels to occupants. Given that microbes have historically been considered contaminants, ‘ventilate well’ has translated to the flat goal of reducing airborne microorganism concentrations (Carslaw et al., 2013). But even at similar concentrations, different ventilation strategies can result in radically different airborne microbial communities. Kembel et al. (2012) demonstrated that in a healthcare facility, mechanical vs. window ventilation led to significantly different airborne bacterial communities in patient rooms, even though the airborne cell densities were similar in each case. Mechanically ventilated rooms had lower bacterial diversity (similar to a ‘monoculture’) and more human-associated bacteria (like those commonly found in the skin and mouth) compared to windowventilated rooms. Ventilation experiments conducted in a university classroom facility have further corroborated the idea that ventilation strategies directly impact the composition of indoor air microbiota (Meadow et al., 2014). We unintentionally shape indoor microbial ecosystems through choices about indoor surfaces. Basic ecology principles suggest that for any given indoor surface, microbial community composition will vary due to a combination of environmental conditions (e.g., material type, temperature, and humidity), dispersal conditions (e.g., the relative magnitude of human, pet, plant, and bioaerosol sources), and biological interactions (e.g., interactions within and among members of colonizing and resident communities). Regardless of the mechanisms at play, numerous studies have shown that microbial communities vary among indoor surfaces (Kelley and Gilbert, 2013). Recent examples include reports of distinct fungal (Adams et al., 2013) and bacterial (Dunn et al., 2013) communities across a wide array of residential surfaces ranging from drains and windowsills to counters, pillowcases, and TV screens. These studies and others suggest that the type, spatial extent, and location of indoor surfaces will impact microbial diversity not only
114
on surfaces themselves, but also in indoor air due to particle resuspension from surfaces. We unintentionally shape indoor microbial ecosystems through choices about human occupancy. Research has shown that human occupancy – through direct shedding and resuspension from the floor – increases the concentration of microbiota in indoor air (Hospodsky et al., 2012). But this and more recent work (Meadow et al., 2014) suggests that human occupancy influences not just the concentration, but also the composition of indoor air microbial communities. A recent study on the bacterial composition of settled dust throughout a building – which represents a more integrative record of indoor air over time – further supports the hypothesis that human occupancy patterns drive the distribution and diversity of indoor microbial ecosystems (Kembel et al., 2014). To be sure, there is a great deal to learn before we can responsibly practice bioinformed design (Corsi et al., 2012). We currently have an incomplete understanding how microbes and microbial communities (and their associated genes, proteins, transcripts, and metabolites) are linked to human health and disease. We understand little about the degree to which the built environment microbiome colonizes the human microbiome (and vice versa). It is reasonable to assume that humans are continuously acquiring microbes from their homes, offices, cars, gyms, and more; but the magnitude, nature, and importance of this exchange relative to other sources (e.g., diet or person-to-person contact) has yet to be rigorously quantified. Finally, even though we spend up to 90% of our lives indoors, we still remain in the nascent stages of understanding indoor ecology – which in broad terms includes understanding the interactions among all indoor organisms (microbes, plants, and animals) and the indoor environment. While a handful of studies have demonstrated that we are shaping indoor ecology through design, it remains unknown whether there exist generalizable patterns to help guide the design process. In sum, bioinformed design will necessarily build upon our ever-expanding knowledge about human–microbial ecosystems, indoor ecosystems, and the interface between the two. Twenty years ago, I knew my future was in ecology. I never imagined that today, I would be reconnecting with engineers to study the microbial ecology of the indoor environment. I am optimistic that well before 2034 we will be collectively designing and managing buildings with intention, to promote healthy indoor ecosystems. Jessica L. Green University of Oregon
Editorial References Adams, R.I., Miletto, M., Taylor, J.W. and Bruns, T.D. (2013) The diversity and distribution of fungi on residential surfaces, PLoS One, 8, e78866. Brandt, L.J. and Aroniadis, O.C. (2013) An overview of fecal microbiota transplantation: techniques, indications, and outcomes, Gastrointest. Endosc., 78, 240–249. Carslaw, N., Hathway, A., Fletcher, L., Hamilton, J., Ingham, T. and Noakes, C. (2013) Chemical versus biological contamination indoors: trade-offs versus win–win opportunities for improving indoor air quality, Indoor Air, 23, 173–174. Corsi, R.L., Kinney, K.A. and Levin, H. (2012) Microbiomes of built environments: 2011 symposium highlights and workgroup recommendations, Indoor Air, 22, 171–172. Di Pierro, F., Donato, G., Fomia, F., Adami, T., Careddu, D., Cassandro, C. and Albera, R. (2012) Preliminary pediatric clinical evaluation of the oral probiotic Streptococcus salivarius K12 in preventing recurrent pharyngitis and/or tonsillitis caused by Streptococcus pyogenes and recurrent acute otitis media, Int. J. Gen. Med., 5, 991–997.
Dunn, R.R., Fierer, N., Henley, J.B., Leff, J.W. and Menninger, H.L. (2013) Home life: factors structuring the bacterial diversity found within and between homes, PLoS One, 8, e64133. Foster, J.A. and McVey Neufeld, K.-A. (2013) Gut–brain axis: how the microbiome influences anxiety and depression, Trends Neurosci., 36, 305–312. Hospodsky, D., Qian, J., Nazaroff, W.W., Yamamoto, N., Bibby, K., RismaniYazdi, H. and Peccia, J. (2012) Human occupancy as a source of indoor airborne bacteria, PLoS One, 7, e34867. Kelley, S.T. and Gilbert, J.A. (2013) Studying the microbiology of the indoor environment, Genome Biol., 14, 1–9. Kembel, S.W., Jones, E., Kline, J., Northcutt, D., Stenson, J., Womack, A.M., Bohannan, B.J.M., Brown, G.Z. and Green, J.L. (2012) Architectural design influences the diversity and structure of the built environment microbiome, ISME J., 6, 1469–1479. Kembel, S.W., Meadow, J.F., O’Connor, T., Mhuireach, G., Northcutt, D., Kline, J., Moriyama, M., Brown, G.Z., Bohannan, B.J.M. and Green, J.L. (2014) Architectural design drives the biogeography of
indoor bacterial communities, PLoS One, 9, e87093. Meadow, J.F., Altrichter, A.E., Kembel, S.W., Kline, J., Mhuireach, G., Moriyama, M., Northcutt, D., O’Connor, T.K., Womack, A.M., Brown, G.Z., Green, J.L. and Bohannan, B.J.M. (2014) Indoor airborne bacterial communities are influenced by ventilation, occupancy, and outdoor air source, Indoor Air, 24, 41–48. Nazaroff, W.W. (2013) Four principles for achieving good indoor air quality, Indoor Air, 23, 353–356. Ripple, W.J. and Beschta, R.L. (2012) Trophic cascades in Yellowstone: the first 15 years after wolf reintroduction, Biol. Conserv., 145, 205–213. Scheper, J., Holzschuh, A., Kuussaari, M., Potts, S.G., Rundl€ of, M., Smith, H.G. and Kleijn, D. (2013) Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss – a meta-analysis, Ecol. Lett., 16, 912–920. Schommer, N.N. and Gallo, R.L. (2013) Structure and function of the human skin microbiome, Trends Microbiol., 21, 660–668.
115
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd INDOOR AIR doi:10.1111/ina.12090
Editorial Can bioinformed design promote healthy indoor ecosystems? Twenty years ago, as an environmental engineering student at UC Berkeley, I had the opportunity to learn about air quality from William Nazaroff. Back then, class conversation centered on physics and chemistry: modeling the source, fate, and transport of pollutants like ozone, radon, and volatile organic compounds. The limited discussion of biology was focused on ‘microbial agents’ or bioaerosols, and their potential role in the spread of infectious disease and asthma. We were taught that microorganisms – viruses, bacteria, and fungi – were pollutants that should be reduced or eliminated indoors. The conversation is changing. We now understand that microorganisms are not all pollutants; in fact, many are critical to the health and well-being of humans and other organisms. In the not too distant future, students in engineering, design, and science may be presented a fundamentally different model. Rather than asking ‘how can we keep microbes out of the indoor environment?’, students and teachers might ask ‘how can we design the indoor environment to promote beneficial microbes and inhibit harmful ones?’ I call this latter model ‘bioinformed design’. There are three reasons I believe we will embrace bioinformed design. First, there has been an explosion of research and public interest focused on host– microbe interactions and in particular the human microbiome – the trillions of microorganisms living in and on our bodies. This trend will continue in the foreseeable future; as a result, knowledge about the types of microbial communities that we may want to cultivate indoors can only improve. Consider the skin microbiome, which is intimately in contact with indoor air and surfaces. Scientists have shown that microbes commonly found on the skin of healthy individuals, like the bacterium Staphylococcus epidermis, can help protect against skin infections and regulate the immune system of their hosts (Schommer and Gallo, 2013). The oral microbiome receives a collection of indoor bioaerosols with every breath (and, albeit less frequently, also from indoor surfaces, particularly with children). Strains of the oral bacteria Streptococcus salivarius have been shown to ward off ear and throat infections (Di Pierro et al., 2012). The gut, which is indirectly connected to the indoor environment, is home to microbes that help to regulate our weight, our immune system, and perhaps even our
brain function and behavior (Foster and McVey Neufeld, 2013). As human microbiome science continues to evolve, this growing body of knowledge can be dynamically integrated into an evolving bioinformed design framework. The second reason I believe we will embrace bioinformed design is due to the rich history of examples where an ecosystem has been managed to achieve some desired result. Entire fields and schools of thought are dedicated, at least in part, to the concept: adaptive ecosystem management, ecological engineering, ecosystem restoration, integrated pest management, agroecology, permaculture, and intervention ecology, to name a few. While the perceived breadth and rigor of these fields varies, below I briefly highlight a few success stories – from farmlands to parks to people – to illustrate the potential. The first example is from agroecology: the agrienvironmental schemes (AES) introduced in Europe in the 1990s. AES provide payments to farmers who subscribe, on a voluntary basis, to practices aimed at enhancing farmland biodiversity. Common practices include sowing wildflower strips along field edges, organic farming, and extensive (versus intensive) grassland management (e.g., restricted herbicide, pesticide, and machinery use). These approaches can have significant positive effects on the diversity and abundance of agroecosystems, particularly for the insects that provide vital pollination services to crops [e.g., bees, butterflies, and moths (Scheper et al., 2013)]. The next example is from wildlife management: the restoration of gray wolves into Yellowstone National Park. Wolves were well established when the park was designated in 1872, but considered pests and decimated by humans. People ultimately realized how crucial this top predator was to ecosystem health; without wolves, elk populations exploded, which in turn led to the overgrazing of deciduous trees like aspen. Restoration of the wolf after a 70-year absence resulted in decreased elk populations, increased tree canopy cover, and an overall increase in the biodiversity of the region (Ripple and Beschta, 2012). The final example is from medicine: fecal microbiota transplantation. In this procedure, microbiota from the stool of a healthy individual is administered (e.g., via pill or enema) to patients who have persistent severe diarrhea caused by an overgrowth of a bacterium called Clostridium difficile. C. difficile infections 113
Editorial are often sparked by taking antibiotics, which can kill the gut’s ‘good’ bacteria. While the exact mechanisms responsible for the success of fecal transplants remain unknown, the process clearly helps transform the gut ecosystem from an unhealthy to a healthy state (Brandt and Aroniadis, 2013). This brings me to the third reason I believe we will embrace indoor bioinformed design. We’re designing indoor microbial ecosystems right now, but we’re doing it unintentionally. We unintentionally shape indoor microbial ecosystems through choices about ventilation. ‘Ventilate well’ is a key principle for achieving good indoor air quality (Nazaroff, 2013). This means, in part, providing ventilation air with low contaminant levels to occupants. Given that microbes have historically been considered contaminants, ‘ventilate well’ has translated to the flat goal of reducing airborne microorganism concentrations (Carslaw et al., 2013). But even at similar concentrations, different ventilation strategies can result in radically different airborne microbial communities. Kembel et al. (2012) demonstrated that in a healthcare facility, mechanical vs. window ventilation led to significantly different airborne bacterial communities in patient rooms, even though the airborne cell densities were similar in each case. Mechanically ventilated rooms had lower bacterial diversity (similar to a ‘monoculture’) and more human-associated bacteria (like those commonly found in the skin and mouth) compared to windowventilated rooms. Ventilation experiments conducted in a university classroom facility have further corroborated the idea that ventilation strategies directly impact the composition of indoor air microbiota (Meadow et al., 2014). We unintentionally shape indoor microbial ecosystems through choices about indoor surfaces. Basic ecology principles suggest that for any given indoor surface, microbial community composition will vary due to a combination of environmental conditions (e.g., material type, temperature, and humidity), dispersal conditions (e.g., the relative magnitude of human, pet, plant, and bioaerosol sources), and biological interactions (e.g., interactions within and among members of colonizing and resident communities). Regardless of the mechanisms at play, numerous studies have shown that microbial communities vary among indoor surfaces (Kelley and Gilbert, 2013). Recent examples include reports of distinct fungal (Adams et al., 2013) and bacterial (Dunn et al., 2013) communities across a wide array of residential surfaces ranging from drains and windowsills to counters, pillowcases, and TV screens. These studies and others suggest that the type, spatial extent, and location of indoor surfaces will impact microbial diversity not only
114
on surfaces themselves, but also in indoor air due to particle resuspension from surfaces. We unintentionally shape indoor microbial ecosystems through choices about human occupancy. Research has shown that human occupancy – through direct shedding and resuspension from the floor – increases the concentration of microbiota in indoor air (Hospodsky et al., 2012). But this and more recent work (Meadow et al., 2014) suggests that human occupancy influences not just the concentration, but also the composition of indoor air microbial communities. A recent study on the bacterial composition of settled dust throughout a building – which represents a more integrative record of indoor air over time – further supports the hypothesis that human occupancy patterns drive the distribution and diversity of indoor microbial ecosystems (Kembel et al., 2014). To be sure, there is a great deal to learn before we can responsibly practice bioinformed design (Corsi et al., 2012). We currently have an incomplete understanding how microbes and microbial communities (and their associated genes, proteins, transcripts, and metabolites) are linked to human health and disease. We understand little about the degree to which the built environment microbiome colonizes the human microbiome (and vice versa). It is reasonable to assume that humans are continuously acquiring microbes from their homes, offices, cars, gyms, and more; but the magnitude, nature, and importance of this exchange relative to other sources (e.g., diet or person-to-person contact) has yet to be rigorously quantified. Finally, even though we spend up to 90% of our lives indoors, we still remain in the nascent stages of understanding indoor ecology – which in broad terms includes understanding the interactions among all indoor organisms (microbes, plants, and animals) and the indoor environment. While a handful of studies have demonstrated that we are shaping indoor ecology through design, it remains unknown whether there exist generalizable patterns to help guide the design process. In sum, bioinformed design will necessarily build upon our ever-expanding knowledge about human–microbial ecosystems, indoor ecosystems, and the interface between the two. Twenty years ago, I knew my future was in ecology. I never imagined that today, I would be reconnecting with engineers to study the microbial ecology of the indoor environment. I am optimistic that well before 2034 we will be collectively designing and managing buildings with intention, to promote healthy indoor ecosystems. Jessica L. Green University of Oregon
Editorial References Adams, R.I., Miletto, M., Taylor, J.W. and Bruns, T.D. (2013) The diversity and distribution of fungi on residential surfaces, PLoS One, 8, e78866. Brandt, L.J. and Aroniadis, O.C. (2013) An overview of fecal microbiota transplantation: techniques, indications, and outcomes, Gastrointest. Endosc., 78, 240–249. Carslaw, N., Hathway, A., Fletcher, L., Hamilton, J., Ingham, T. and Noakes, C. (2013) Chemical versus biological contamination indoors: trade-offs versus win–win opportunities for improving indoor air quality, Indoor Air, 23, 173–174. Corsi, R.L., Kinney, K.A. and Levin, H. (2012) Microbiomes of built environments: 2011 symposium highlights and workgroup recommendations, Indoor Air, 22, 171–172. Di Pierro, F., Donato, G., Fomia, F., Adami, T., Careddu, D., Cassandro, C. and Albera, R. (2012) Preliminary pediatric clinical evaluation of the oral probiotic Streptococcus salivarius K12 in preventing recurrent pharyngitis and/or tonsillitis caused by Streptococcus pyogenes and recurrent acute otitis media, Int. J. Gen. Med., 5, 991–997.
Dunn, R.R., Fierer, N., Henley, J.B., Leff, J.W. and Menninger, H.L. (2013) Home life: factors structuring the bacterial diversity found within and between homes, PLoS One, 8, e64133. Foster, J.A. and McVey Neufeld, K.-A. (2013) Gut–brain axis: how the microbiome influences anxiety and depression, Trends Neurosci., 36, 305–312. Hospodsky, D., Qian, J., Nazaroff, W.W., Yamamoto, N., Bibby, K., RismaniYazdi, H. and Peccia, J. (2012) Human occupancy as a source of indoor airborne bacteria, PLoS One, 7, e34867. Kelley, S.T. and Gilbert, J.A. (2013) Studying the microbiology of the indoor environment, Genome Biol., 14, 1–9. Kembel, S.W., Jones, E., Kline, J., Northcutt, D., Stenson, J., Womack, A.M., Bohannan, B.J.M., Brown, G.Z. and Green, J.L. (2012) Architectural design influences the diversity and structure of the built environment microbiome, ISME J., 6, 1469–1479. Kembel, S.W., Meadow, J.F., O’Connor, T., Mhuireach, G., Northcutt, D., Kline, J., Moriyama, M., Brown, G.Z., Bohannan, B.J.M. and Green, J.L. (2014) Architectural design drives the biogeography of
indoor bacterial communities, PLoS One, 9, e87093. Meadow, J.F., Altrichter, A.E., Kembel, S.W., Kline, J., Mhuireach, G., Moriyama, M., Northcutt, D., O’Connor, T.K., Womack, A.M., Brown, G.Z., Green, J.L. and Bohannan, B.J.M. (2014) Indoor airborne bacterial communities are influenced by ventilation, occupancy, and outdoor air source, Indoor Air, 24, 41–48. Nazaroff, W.W. (2013) Four principles for achieving good indoor air quality, Indoor Air, 23, 353–356. Ripple, W.J. and Beschta, R.L. (2012) Trophic cascades in Yellowstone: the first 15 years after wolf reintroduction, Biol. Conserv., 145, 205–213. Scheper, J., Holzschuh, A., Kuussaari, M., Potts, S.G., Rundl€ of, M., Smith, H.G. and Kleijn, D. (2013) Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss – a meta-analysis, Ecol. Lett., 16, 912–920. Schommer, N.N. and Gallo, R.L. (2013) Structure and function of the human skin microbiome, Trends Microbiol., 21, 660–668.
115
