Today, humans spend ~90% of their lives roaming the ‘great indoors’, which is very different from the outdoor environments where we co-evolved with our commensal microbiota (Kelley and Gilbert, 2013). We are just beginning to understand how the design of built environments (BEs) influences our microbiome, and how these interactions, in turn, might affect human health. An improved understanding of the BE-microbe-host feedback loop is important for protecting public health in an increasingly urbanized world.
Restrooms are a shared public space with clear disease transmission potential. Pioneering work by Flores et al. (2011) demonstrated how microbial communities, sourced predominantly from the human microbiome, are geographically distributed in a public restroom, showing gender- and surface-specific signatures. Recent work from our group has corroborated these results, showing how BE surfaces are coated with mostly human-associated microbes (Lax et al., 2014). In addition, we found that individuals leave behind distinct microbial fingerprints on BE surfaces, which has implications for forensics and for disease transmission.
In our most recent BE paper, we expand upon the Flores et al. (2011) work with a series of longitudinal studies (Gibbons et al., 2014). We characterize the reproducibility of microbial succession on public restroom surfaces and demonstrate the viability of host-associated microbes deposited on these surfaces. Specifically, we show that thorough decontamination of restroom surfaces with bleach results in the transient dominance of fecal-associated microbes, but that these fecal taxa are rapidly displaced by skin-associated microbes after ~5 hours. This skin-dominated community persists stably for months, even in the presence of normal soap-and-water cleaning regimes.
To our surprise, several Staphylococcus species represented a majority of the culturable floor community, even after many hours of human-exclusion. Staphylococcus aureus is responsible for a large fraction of hospital-related infections, and is a relatively common constituent of the human skin microbiome. Our results show that these potential pathogens remain viable on BE surfaces for long periods of time in the absence of their hosts. Methicillin resistant S. aureus (MRSA) is increasingly common outside the hospital environment, and represents a significant public health risk. We found evidence for methicillin resistance genes in the shotgun metagenomes from the late-successional communities, but we did not find any MRSA-related genes within assembled Staphylococcus sp. pan-genomes from our culture work.
In addition to bacteria, we were able to look at the viral community. We found a strong positive correlation between bacterial and viral abundances, and a dominance of the viral community by enterrophages (viruses that prey upon gut bacteria). We also found a large number of Human Papilloma and Herpes viruses on restroom surfaces. The unexpectedly low virus-to-bacterial ratio suggests that viral activity is minimal in this system. This fact, combined with low bacterial biomass on BE surfaces, reflects the ecological mismatch between the BE and host environments. Most host-associated taxa are coming from a warm, moist, and sometimes anaerobic ecosystem, with plenty of substrate for growth. Restroom surfaces are relatively dry, cold, aerobic and barren (inert), when compared to the host system. Thus, most bacteria are probably dormant, dying, or dead in these microbial deserts.
In summary, we found that the restroom microbiota show reproducible ecological succession from fecal-associated organisms toward a stable community state dominated by skin-associated taxa. This transition was rapid, occurring within a few hours. This was likely due to the dispersal of fecal taxa due to aerosolization from toilet flushing, followed by the enhanced ability of skin taxa to persist on dry, aerobic surfaces. Many human-associated organisms, including known pathogens, remained viable on BE surfaces for hours in the absence of humans. Overall, microbial communities residing on restroom surfaces are a reflection of the humans that inhabit the space; they are the slowly decaying remnants of the vibrant ecosystems found across the human body. As such, the health state of BEs may simply be a reflection of the health state of the humans that reside in them.
References:
- Flores GE, et al. (2011) Microbial Biogeography of Public Restroom Surfaces. PLoS ONE 6(11): e28132. doi:10.1371/journal.pone.0028132
- Gibbons SM, et al. Ecological succession and viability of human-associated microbiota on restroom surfaces Appl. Environ. Microbiol. AEM.03117-14; published ahead of print 14 November 2014, doi:10.1128/AEM.03117-14
This comment is from Maria Nunez.
“… low bacterial biomass on Building Environment surfaces, reflects the ecological mismatch between the BE and host environments. Most host-associated taxa are coming from a warm, moist, and sometimes anaerobic ecosystem, with plenty of substrate for growth. Restroom surfaces are relatively dry, cold, aerobic and barren (inert), when compared to the host system. Thus, most bacteria are probably dormant, dying, or dead in these microbial deserts.”
AT LAST! Somebody that understands that what we find on dry building surfaces is mainly remains of the human/pet/plant/soil microbiome, not the building microbiome itself! Building surfaces and air are designed to be dry because humans like it dry. Most microbes, including pathogens (beware of resistant structures of moulds and some bacteria that can remain dormant!), on building surfaces are dead within few hours, either because the building environment is too dry, the temperature is too low, or oxigen kills them. STILL WE CAN DETECT THEIR DNA.
Buildings CAN develop a building microbiome when excessive moisture enters the building, and microbes from different sources (not all of them) start growing. This happens often in hidden structures. Mapping microbial DNA on dry building surfaces seldom reveals the real building microbiome… But it is often there, and it is growing and interacting with us, making many of us sick.
Great comment! However, just because these organisms are probably dormant/dying doesn’t mean that they are all dead. Check out our culturing work – we show that many organisms remain viable on BE surfaces for quite a while after human-exclusion.
Yes, agree. But only the ones being able to grow on moist building surfaces, either clean or soiled, or the dormant ones, mostly spore-forming microorganisms. I also agree with you that culturing is necessary in order to characterize the ecology of building microorganisms. Too many people have disregarded culturing as an old-fashioned technique. The Ebola issue, as well as your paper, show that culturing is essential in understanding building microbial ecology. The good news is that you do not need time-consuming culturing in order to document the ability of many microorganisms to grow on moist building surfaces, especially moulds, if you observe them at the right magnification, that is the optical microscope (they are microscopic, right?). DNA is definitely not the panacea. Thanks for a very interesting publication that reduces microphobia markedly.
Thanks! Yep, agreed. We used microscopy to quantify overall microbial abundance, but then used 16S amplicon sequencing to look at the enrichment of particular taxa that grew up in liquid culture (2 days at 25C or 37C, under anaerobic or aerobic conditions).
Walsh and Camilli on Strep desiccation and rehydration http://mbio.asm.org/content/2/3/e00092-11.full . That would be a human-associated (almost exclusively) species, shed into the BE, and then reinfecting hosts (potentially).
I’d be careful with generalizations about human-associated species not populating the BE, fomites within the BE can easily serve as reservoirs for reinfection, even if not the ‘natural’ host. Also, strain differences as well as regulation within a species may allow for survival and propagation.
Very cool work! Re. Maria Paz Nunez Garcia’s comment on microphobia — while it does quell fear regarding surfaces that are regularly cleaned and haven’t been reinoculated for a while, it makes me a little queazy to think of the aerosols that are generated with every flush! But also leaves room for a great invention: the non-aerosol-generating flusher! ;) Thanks for the great research!!