James F. Meadow

Identifying personal microbiomes using metagenomic codes

Significance Recent surveys of the microbial communities living on and in the human body—the human microbiome—have revealed strong variation in community membership between individuals. Some of this variation is stable over time, leading to speculation that individuals might possess unique microbial “fingerprints” that distinguish them from the population. We rigorously evaluated this idea by combining concepts from microbial ecology and computer science. Our results demonstrated that individuals could be uniquely identified among populations of 100s based on their microbiomes alone. In the case of the gut microbiome, >80% of individuals could still be uniquely identified up to a year later—a result that raises potential privacy concerns for subjects enrolled in human microbiome research projects. Community composition within the human microbiome varies across individuals, but it remains unknown if this variation is sufficient to uniquely identify individuals within large populations or stable enough to identify them over time. We investigated this by developing a hitting set-based coding algorithm and applying it to the Human Microbiome Project population. Our approach defined body site-specific metagenomic codes: sets of microbial taxa or genes prioritized to uniquely and stably identify individuals. Codes capturing strain variation in clade-specific marker genes were able to distinguish among 100s of individuals at an initial sampling time point. In comparisons with follow-up samples collected 30–300 d later, ∼30% of individuals could still be uniquely pinpointed using metagenomic codes from a typical body site; coincidental (false positive) matches were rare. Codes based on the gut microbiome were exceptionally stable and pinpointed >80% of individuals. The failure of a code to match its owner at a later time point was largely explained by the loss of specific microbial strains (at current limits of detection) and was only weakly associated with the length of the sampling interval. In addition to highlighting patterns of temporal variation in the ecology of the human microbiome, this work demonstrates the feasibility of microbiome-based identifiability—a result with important ethical implications for microbiome study design. The datasets and code used in this work are available for download from huttenhower.sph.harvard.edu/idability.

Indoor airborne bacterial communities are influenced by ventilation, occupancy, and outdoor air source

Architects and engineers are beginning to consider a new dimension of indoor air: the structure and composition of airborne microbial communities. A first step in this emerging field is to understand the forces that shape the diversity of bioaerosols across space and time within the built environment. In an effort to elucidate the relative influences of three likely drivers of indoor bioaerosol diversity – variation in outdoor bioaerosols, ventilation strategy, and occupancy load – we conducted an intensive temporal study of indoor airborne bacterial communities in a high-traffic university building with a hybrid HVAC (mechanically and naturally ventilated) system. Indoor air communities closely tracked outdoor air communities, but human-associated bacterial genera were more than twice as abundant in indoor air compared with outdoor air. Ventilation had a demonstrated effect on indoor airborne bacterial community composition; changes in outdoor air communities were detected inside following a time lag associated with differing ventilation strategies relevant to modern building design. Our results indicate that both occupancy patterns and ventilation strategies are important for understanding airborne microbial community dynamics in the built environment.

Architectural design drives the biogeography of indoor bacterial communities.

Background Architectural design has the potential to influence the microbiology of the built environment, with implications for human health and well-being, but the impact of design on the microbial biogeography of buildings remains poorly understood. In this study we combined microbiological data with information on the function, form, and organization of spaces from a classroom and office building to understand how design choices influence the biogeography of the built environment microbiome. Results Sequencing of the bacterial 16S gene from dust samples revealed that indoor bacterial communities were extremely diverse, containing more than 32,750 OTUs (operational taxonomic units, 97% sequence similarity cutoff), but most communities were dominated by Proteobacteria, Firmicutes, and Deinococci. Architectural design characteristics related to space type, building arrangement, human use and movement, and ventilation source had a large influence on the structure of bacterial communities. Restrooms contained bacterial communities that were highly distinct from all other rooms, and spaces with high human occupant diversity and a high degree of connectedness to other spaces via ventilation or human movement contained a distinct set of bacterial taxa when compared to spaces with low occupant diversity and low connectedness. Within offices, the source of ventilation air had the greatest effect on bacterial community structure. Conclusions Our study indicates that humans have a guiding impact on the microbial biodiversity in buildings, both indirectly through the effects of architectural design on microbial community structure, and more directly through the effects of human occupancy and use patterns on the microbes found in different spaces and space types. The impact of design decisions in structuring the indoor microbiome offers the possibility to use ecological knowledge to shape our buildings in a way that will select for an indoor microbiome that promotes our health and well-being.

Humans differ in their personal microbial cloud

Dispersal of microbes between humans and the built environment can occur through direct contact with surfaces or through airborne release; the latter mechanism remains poorly understood. Humans emit upwards of 106 biological particles per hour, and have long been known to transmit pathogens to other individuals and to indoor surfaces. However it has not previously been demonstrated that humans emit a detectible microbial cloud into surrounding indoor air, nor whether such clouds are sufficiently differentiated to allow the identification of individual occupants. We used high-throughput sequencing of 16S rRNA genes to characterize the airborne bacterial contribution of a single person sitting in a sanitized custom experimental climate chamber. We compared that to air sampled in an adjacent, identical, unoccupied chamber, as well as to supply and exhaust air sources. Additionally, we assessed microbial communities in settled particles surrounding each occupant, to investigate the potential long-term fate of airborne microbial emissions. Most occupants could be clearly detected by their airborne bacterial emissions, as well as their contribution to settled particles, within 1.5–4 h. Bacterial clouds from the occupants were statistically distinct, allowing the identification of some individual occupants. Our results confirm that an occupied space is microbially distinct from an unoccupied one, and demonstrate for the first time that individuals release their own personalized microbial cloud.

Bacterial communities on classroom surfaces vary with human contact

BackgroundHumans can spend the majority of their time indoors, but little is known about the interactions between the human and built-environment microbiomes or the forces that drive microbial community assembly in the built environment. We sampled 16S rRNA genes from four different surface types throughout a university classroom to determine whether bacterial assemblages on each surface were best predicted by routine human interactions or by proximity to other surfaces within the classroom. We then analyzed our data with publicly-available datasets representing potential source environments.ResultsBacterial assemblages from the four surface types, as well as individual taxa, were indicative of different source pools related to the type of human contact each surface routinely encounters. Spatial proximity to other surfaces in the classroom did not predict community composition.ConclusionsOur results indicate that human-associated microbial communities can be transferred to indoor surfaces following contact, and that such transmission is possible even when contact is indirect, but that proximity to other surfaces in the classroom does not influence community composition.

Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park

The relative importance of dispersal and niche restrictions remains a controversial topic in community ecology, especially for microorganisms that are often assumed to be ubiquitous. We investigated the impact of these factors for the community assembly of the root-symbiont arbuscular mycorrhizal fungi (AMF) by sampling roots from geothermal and nonthermal grasslands in Yellowstone National Park (YNP), followed by sequencing and RFLP of AMF ribosomal DNA. With the exception of an apparent generalist RFLP type closely related to Glomus intraradices, a distance-based redundancy analysis indicated that the AMF community composition correlated with soil pH or pH-driven changes in soil chemistry. This was unexpected, given the large differences in soil temperature and plant community composition between the geothermal and nonthermal grasslands. RFLP types were found in either the acidic geothermal grasslands or in the neutral to alkaline grasslands, one of which was geothermal. The direct effect of the soil chemical environment on the distribution of two AMF morphospecies isolated from acidic geothermal grasslands was supported in a controlled greenhouse experiment. Paraglomus occultum and Scutellospora pellucida were more beneficial to plants and formed significantly more spores when grown in acidic than in alkaline soil. Distance among grasslands, used as an estimate of dispersal limitations, was not a significant predictor of AMF community similarity within YNP, and most fungal taxa may be part of a metacommunity. The isolation of several viable AMF taxa from bison feces indicates that wide-ranging bison could be a vector for at least some RFLP types among grasslands within YNP. In support of classical niche theory and the Baas-Becking hypothesis, our results suggest that AMF are not limited by dispersal at the scale of YNP, but that the soil environment appears to be the primary factor affecting community composition and distribution.

Microbiota of the indoor environment: a meta-analysis

BackgroundAs modern humans, we spend the majority of our time in indoor environments. Consequently, environmental exposure to microorganisms has important implications for human health, and a better understanding of the ecological drivers and processes that impact indoor microbial assemblages will be key for expanding our knowledge of the built environment. In the present investigation, we combined recent studies examining the microbiota of the built environment in order to identify unifying community patterns and the relative importance of indoor environmental factors. Ultimately, the present meta-analysis focused on studies of bacteria and archaea due to the limited number of high-throughput fungal studies from the indoor environment. We combined 16S ribosomal RNA (rRNA) gene datasets from 16 surveys of indoor environments conducted worldwide, additionally including 7 other studies representing putative environmental sources of microbial taxa (outdoor air, soil, and the human body).ResultsCombined analysis of subsets of studies that shared specific experimental protocols or indoor habitats revealed community patterns indicative of consistent source environments and environmental filtering. Additionally, we were able to identify several consistent sources for indoor microorganisms, particularly outdoor air and skin, mirroring what has been shown in individual studies. Technical variation across studies had a strong effect on comparisons of microbial community assemblages, with differences in experimental protocols limiting our ability to extensively explore the importance of, for example, sampling locality, building function and use, or environmental substrate in structuring indoor microbial communities.ConclusionsWe present a snapshot of an important scientific field in its early stages, where studies have tended to focus on heavy sampling in a few geographic areas. From the practical perspective, this endeavor reinforces the importance of negative “kit” controls in microbiome studies. From the perspective of understanding mechanistic processes in the built environment, this meta-analysis confirms that broad factors, such as geography and building type, structure indoor microbes. However, this exercise suggests that individual studies with common sampling techniques may be more appropriate to explore the relative importance of subtle indoor environmental factors on the indoor microbiome.

Significant changes in the skin microbiome mediated by the sport of roller derby

Diverse bacterial communities live on and in human skin. These complex communities vary by skin location on the body, over time, between individuals, and between geographic regions. Culture-based studies have shown that human to human and human to surface contact mediates the dispersal of pathogens, yet little is currently known about the drivers of bacterial community assembly patterns on human skin. We hypothesized that participation in a sport involving skin to skin contact would result in detectable shifts in skin bacterial community composition. We conducted a study during a flat track roller derby tournament, and found that teammates shared distinct skin microbial communities before and after playing against another team, but that opposing teams’ bacterial communities converged during the course of a roller derby bout. Our results are consistent with the hypothesis that the human skin microbiome shifts in composition during activities involving human to human contact, and that contact sports provide an ideal setting in which to evaluate dispersal of microorganisms between people.

Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis

BackgroundLocal adaptation, the differential success of genotypes in their native versus foreign environment, arises from various evolutionary processes, but the importance of concurrent abiotic and biotic factors as drivers of local adaptation has only recently been investigated. Local adaptation to biotic interactions may be particularly important for plants, as they associate with microbial symbionts that can significantly affect their fitness and may enable rapid evolution. The arbuscular mycorrhizal (AM) symbiosis is ideal for investigations of local adaptation because it is globally widespread among most plant taxa and can significantly affect plant growth and fitness. Using meta-analysis on 1170 studies (from 139 papers), we investigated the potential for local adaptation to shape plant growth responses to arbuscular mycorrhizal inoculation.ResultsThe magnitude and direction for mean effect size of mycorrhizal inoculation on host biomass depended on the geographic origin of the soil and symbiotic partners. Sympatric combinations of plants, AM fungi, and soil yielded large increases in host biomass compared to when all three components were allopatric. The origin of either the fungi or the plant relative to the soil was important for explaining the effect of AM inoculation on plant biomass. If plant and soil were sympatric but allopatric to the fungus, the positive effect of AM inoculation was much greater than when all three components were allopatric, suggesting potential local adaptation of the plant to the soil; however, if fungus and soil were sympatric (but allopatric to the plant) the effect of AM inoculation was indistinct from that of any allopatric combinations, indicating maladaptation of the fungus to the soil.ConclusionsThis study underscores the potential to detect local adaptation for mycorrhizal relationships across a broad swath of the literature. Geographic origin of plants relative to the origin of AM fungal communities and soil is important for describing the effect of mycorrhizal inoculation on plant biomass, suggesting that local adaptation represents a powerful factor for the establishment of novel combinations of fungi, plants, and soils. These results highlight the need for subsequent investigations of local adaptation in the mycorrhizal symbiosis and emphasize the importance of routinely considering the origin of plant, soil, and fungal components.

Mobile phones carry the personal microbiome of their owners

Most people on the planet own mobile phones, and these devices are increasingly being utilized to gather data relevant to our personal health, behavior, and environment. During an educational workshop, we investigated the utility of mobile phones to gather data about the personal microbiome — the collection of microorganisms associated with the personal effects of an individual. We characterized microbial communities on smartphone touchscreens to determine whether there was significant overlap with the skin microbiome sampled directly from their owners. We found that about 22% of the bacterial taxa on participants’ fingers were also present on their own phones, as compared to 17% they shared on average with other people’s phones. When considered as a group, bacterial communities on men’s phones were significantly different from those on their fingers, while women’s were not. Yet when considered on an individual level, men and women both shared significantly more of their bacterial communities with their own phones than with anyone else’s. In fact, 82% of the OTUs were shared between a person’s index and phone when considering the dominant taxa (OTUs with more than 0.1% of the sequences in an individual’s dataset). Our results suggest that mobile phones hold untapped potential as personal microbiome sensors.