Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism.

Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.

Erratum: Author Correction: Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism.

[This corrects the article DOI: 10.1038/s42003-018-0120-9.].

Urban greenness influences airborne bacterial community composition.

Urban green space provides health benefits for city dwellers, and new evidence suggests that microorganisms associated with soil and vegetation could play a role. While airborne microorganisms are ubiquitous in urban areas, the influence of nearby vegetation on airborne microbial communities remains poorly understood. We examined airborne microbial communities in parks and parking lots in Eugene, Oregon, using high-throughput sequencing of the bacterial 16S rRNA gene on the Illumina MiSeq platform to identify bacterial taxa, and GIS to measure vegetation cover in buffer zones of different diameters. Our goal was to explore variation among highly vegetated (parks) versus non-vegetated (parking lots) urban environments. A secondary objective was to evaluate passive versus active collection methods for outdoor airborne microbial sampling. Airborne bacterial communities from five parks were different from those of five parking lots (p=0.023), although alpha diversity was similar. Direct gradient analysis showed that the proportion of vegetated area within a 50m radius of the sampling station explained 15% of the variation in bacterial community composition. A number of key taxa, including several Acidobacteriaceae were substantially more abundant in parks, while parking lots had higher relative abundance of Acetobacteraceae. Parks had greater beta diversity than parking lots, i.e. individual parks were characterized by unique bacterial signatures, whereas parking lot communities tended to be similar to each other. Although parks and parking lots were selected to form pairs of nearby sites, spatial proximity did not appear to affect compositional similarity. Our results also showed that passive and active collection methods gave comparable results, indicating the "settling dish" method is effective for outdoor airborne sampling. This work sets a foundation for understanding how urban vegetation may impact microbial communities, with potential implications for designing neighborhoods and open space systems that foster better human health.

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

BACKGROUND: Local 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. RESULTS: The 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. CONCLUSIONS: This 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.

MycoDB, a global database of plant response to mycorrhizal fungi.

Plants form belowground associations with mycorrhizal fungi in one of the most common symbioses on Earth. However, few large-scale generalizations exist for the structure and function of mycorrhizal symbioses, as the nature of this relationship varies from mutualistic to parasitic and is largely context-dependent. We announce the public release of MycoDB, a database of 4,010 studies (from 438 unique publications) to aid in multi-factor meta-analyses elucidating the ecological and evolutionary context in which mycorrhizal fungi alter plant productivity. Over 10 years with nearly 80 collaborators, we compiled data on the response of plant biomass to mycorrhizal fungal inoculation, including meta-analysis metrics and 24 additional explanatory variables that describe the biotic and abiotic context of each study. We also include phylogenetic trees for all plants and fungi in the database. To our knowledge, MycoDB is the largest ecological meta-analysis database. We aim to share these data to highlight significant gaps in mycorrhizal research and encourage synthesis to explore the ecological and evolutionary generalities that govern mycorrhizal functioning in ecosystems.

Microbiota of the indoor environment: a meta-analysis.

BACKGROUND: As 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). RESULTS: Combined 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. CONCLUSIONS: We 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.

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 10(6) 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.

Identifying personal microbiomes using metagenomic codes.

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.

Evolution of the indoor biome.

Few biologists have studied the evolutionary processes at work in indoor environments. Yet indoor environments comprise approximately 0.5% of ice-free land area--an area as large as the subtropical coniferous forest biome. Here we review the emerging subfield of 'indoor biome' studies. After defining the indoor biome and tracing its deep history, we discuss some of its evolutionary dimensions. We restrict our examples to the species found in human houses--a subset of the environments constituting the indoor biome--and offer preliminary hypotheses to advance the study of indoor evolution. Studies of the indoor biome are situated at the intersection of evolutionary ecology, anthropology, architecture, and human ecology and are well suited for citizen science projects, public outreach, and large-scale international collaborations.

Local domestication of lactic acid bacteria via cassava beer fermentation.

Cassava beer, or chicha, is typically consumed daily by the indigenous Shuar people of the Ecuadorian Amazon. This traditional beverage made from cassava tuber (Manihot esculenta) is thought to improve nutritional quality and flavor while extending shelf life in a tropical climate. Bacteria responsible for chicha fermentation could be a source of microbes for the human microbiome, but little is known regarding the microbiology of chicha. We investigated bacterial community composition of chicha batches using Illumina high-throughput sequencing. Fermented chicha samples were collected from seven Shuar households in two neighboring villages in the Morona-Santiago region of Ecuador, and the composition of the bacterial communities within each chicha sample was determined by sequencing a region of the 16S ribosomal gene. Members of the genus Lactobacillus dominated all samples. Significantly greater phylogenetic similarity was observed among chicha samples taken within a village than those from different villages. Community composition varied among chicha samples, even those separated by short geographic distances, suggesting that ecological and/or evolutionary processes, including human-mediated factors, may be responsible for creating locally distinct ferments. Our results add to evidence from other fermentation systems suggesting that traditional fermentation may be a form of domestication, providing endemic beneficial inocula for consumers, but additional research is needed to identify the mechanisms and extent of microbial dispersal.

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.

Bacterial communities on classroom surfaces vary with human contact.

BACKGROUND: Humans 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. RESULTS: Bacterial 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. CONCLUSIONS: Our 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.

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.

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.

Prokaryotic communities differ along a geothermal soil photic gradient.

Geothermal influenced soils exert unique physical and chemical limitations on resident microbial communities but have received little attention in microbial ecology research. These environments offer a model system in which to investigate microbial community heterogeneity and a range of soil ecological concepts. We conducted a 16S bar-coded pyrosequencing survey of the prokaryotic communities in a diatomaceous geothermal soil system and compared communities across soil types and along a conspicuous photic depth gradient. We found significant differences between the communities of the two different soils and also predictable differences between samples taken at different depths. Additionally, we targeted three ecologically relevant bacterial phyla, Cyanobacteria, Planctomycetes, and Verrucomicrobia, for clade-wise comparisons with these variables and found strong differences in their abundances, consistent with the autecology of these groups.

Spatial heterogeneity of eukaryotic microbial communities in an unstudied geothermal diatomaceous biological soil crust: Yellowstone National Park, WY, USA.

Knowledge of microbial communities and their inherent heterogeneity has dramatically increased with the widespread use of high-throughput sequencing technologies, and we are learning more about the ecological processes that structure microbial communities across a wide range of environments, as well as the relative scales of importance for describing bacterial communities in natural systems. Little work has been carried out to assess fine-scale eukaryotic microbial heterogeneity in soils. Here, we present findings from a bar-coded 18S rRNA survey of the eukaryotic microbial communities in a previously unstudied geothermal diatomaceous biological soil crust in Yellowstone National Park, WY, USA, in which we explicitly compare microbial community heterogeneity at the particle scale within soil cores. Multivariate analysis of community composition showed that while subsamples from within the same soil core clustered together, community dissimilarity between particles in the same core was high. This study describes a novel soil microbial environment and also adds to our growing understanding of microbial heterogeneity and the scales relevant to the study of soil microbial communities.

Linking symbiont community structures in a model arbuscular mycorrhizal system.

• The influence of plant communities on symbiotic arbuscular mycorrhizal fungal (AMF) communities is difficult to study in situ as both symbionts are strongly influenced by some of the same soil and environmental conditions, and thus we have a poor understanding of the potential links in community composition and structure between host and fungal communities. • AMF were characterized in colonized roots of thermal soil Mimulus guttatus in both isolated plants supporting AMF for only a few months of the growing season and plants growing in mixed plant communities composed of annual and perennial hosts. Cluster and discriminant analysis were used to compare competing models based on either communities or soil conditions. • Mimulus guttatus in adjacent contrasting plant community situations harbored distinct AMF communities with few fungal taxa occurring in both community types. Isolated plants harbored communities of fewer fungal taxa with lower diversity than plants in mixed communities. Host community type was more indicative than pH of AMF community structure. • Our results support an inherent relationship between host plant and AMF community structures, although pH-based models were also statistically supported.

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.