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.
- 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