Jessica L. Green

The role of ecological theory in microbial ecology

Microbial ecology is currently undergoing a revolution, with repercussions spreading throughout microbiology, ecology and ecosystem science. The rapid accumulation of molecular data is uncovering vast diversity, abundant uncultivated microbial groups and novel microbial functions. This accumulation of data requires the application of theory to provide organization, structure, mechanistic insight and, ultimately, predictive power that is of practical value, but the application of theory in microbial ecology is currently very limited. Here we argue that the full potential of the ongoing revolution will not be realized if research is not directed and driven by theory, and that the generality of established ecological theory must be tested using microbial systems.

Microbes on mountainsides: Contrasting elevational patterns of bacterial and plant diversity

The study of elevational diversity gradients dates back to the foundation of biogeography. Although elevational patterns of plant and animal diversity have been studied for centuries, such patterns have not been reported for microorganisms and remain poorly understood. Here, in an effort to assess the generality of elevational diversity patterns, we examined soil bacterial and plant diversity along an elevation gradient. To gain insight into the forces that structure these patterns, we adopted a multifaceted approach to incorporate information about the structure, diversity, and spatial turnover of montane communities in a phylogenetic context. We found that observed patterns of plant and bacterial diversity were fundamentally different. While bacterial taxon richness and phylogenetic diversity decreased monotonically from the lowest to highest elevations, plants followed a unimodal pattern, with a peak in richness and phylogenetic diversity at mid-elevations. At all elevations bacterial communities had a tendency to be phylogenetically clustered, containing closely related taxa. In contrast, plant communities did not exhibit a uniform phylogenetic structure across the gradient: they became more overdispersed with increasing elevation, containing distantly related taxa. Finally, a metric of phylogenetic beta-diversity showed that bacterial lineages were not randomly distributed, but rather exhibited significant spatial structure across the gradient, whereas plant lineages did not exhibit a significant phylogenetic signal. Quantifying the influence of sample scale in intertaxonomic comparisons remains a challenge. Nevertheless, our findings suggest that the forces structuring microorganism and macroorganism communities along elevational gradients differ.

Spatial scaling of microbial eukaryote diversity

Patterns in the spatial distribution of organisms provide important information about mechanisms that regulate the diversity of life and the complexity of ecosystems. Although microorganisms may comprise much of the Earths biodiversity and have critical roles in biogeochemistry and ecosystem functioning, little is known about their spatial diversification. Here we present quantitative estimates of microbial community turnover at local and regional scales using the largest spatially explicit microbial diversity data set available (> 106 sample pairs). Turnover rates were small across large geographical distances, of similar magnitude when measured within distinct habitats, and did not increase going from one vegetation type to another. The taxa–area relationship of these terrestrial microbial eukaryotes was relatively flat (slope z = 0.074) and consistent with those reported in aquatic habitats. This suggests that despite high local diversity, microorganisms may have only moderate regional diversity. We show how turnover patterns can be used to project taxa–area relationships up to whole continents. Taxa dissimilarities across continents and between them would strengthen these projections. Such data do not yet exist, but would be feasible to collect.

A latitudinal diversity gradient in planktonic marine bacteria

For two centuries, biologists have documented a gradient of animal and plant biodiversity from the tropics to the poles but have been unable to agree whether it is controlled primarily by productivity, temperature, or historical factors. Recent reports that find latitudinal diversity gradients to be reduced or absent in some unicellular organisms and attribute this to their high abundance and dispersal capabilities would suggest that bacteria, the smallest and most abundant organisms, should exhibit no latitudinal pattern of diversity. We used amplified ribosomal intergenic spacer analysis (ARISA) whole-assemblage genetic fingerprinting to quantify species richness in 103 near-surface samples of marine bacterial plankton, taken from tropical to polar in both hemispheres. We found a significant latitudinal gradient in richness. The data can help to evaluate hypotheses about the cause of the gradient. The correlations of richness with latitude and temperature were similarly strong, whereas correlations with parameters relating to productivity (chlorophyll, annual primary productivity, bacterial abundance) and other variables (salinity and distance to shore) were much weaker. Despite the high abundance and potentially high dispersal of bacteria, they exhibit geographic patterns of species diversity that are similar to those seen in other organisms. The latitudinal gradient in marine bacteria supports the hypothesis that the kinetics of metabolism, setting the pace for life, has strong influence on diversity.

Microbial Biogeography: From Taxonomy to Traits

The biogeographic variation of life has predominantly been studied using taxonomy, but this focus is changing. There is a resurging interest in understanding patterns in the distribution not only of taxa but also of the traits those taxa possess. Patterns of trait variation shed light on fundamental questions in biology, including why organisms live where they do and how they will respond to environmental change. Technological advances such as environmental genomics place microbial ecology in a unique position to move trait-based biogeography forward. We anticipate that as trait-based biogeography continues to evolve, micro- and macroorganisms will be studied in concert, establishing a science that is informed by and relevant to all domains of life.

On estimating the exponent of power-law frequency distributions

Power-law frequency distributions characterize a wide array of natural phenomena. In ecology, biology, and many physical and social sciences, the exponents of these power laws are estimated to draw inference about the processes underlying the phenomenon, to test theoretical models, and to scale up from local observations to global patterns. Therefore, it is essential that these exponents be estimated accurately. Unfortunately, the binning-based methods traditionally used in ecology and other disciplines perform quite poorly. Here we discuss more sophisticated methods for fitting these exponents based on cumulative distribution functions and maximum likelihood estimation. We illustrate their superior performance at estimating known exponents and provide details on how and when ecologists should use them. Our results confirm that maximum likelihood estimation outperforms other methods in both accuracy and precision. Because of the use of biased statistical methods for estimating the exponent, the conclusions of several recently published papers should be revisited.

Architectural design influences the diversity and structure of the built environment microbiome

Buildings are complex ecosystems that house trillions of microorganisms interacting with each other, with humans and with their environment. Understanding the ecological and evolutionary processes that determine the diversity and composition of the built environment microbiome—the community of microorganisms that live indoors—is important for understanding the relationship between building design, biodiversity and human health. In this study, we used high-throughput sequencing of the bacterial 16S rRNA gene to quantify relationships between building attributes and airborne bacterial communities at a health-care facility. We quantified airborne bacterial community structure and environmental conditions in patient rooms exposed to mechanical or window ventilation and in outdoor air. The phylogenetic diversity of airborne bacterial communities was lower indoors than outdoors, and mechanically ventilated rooms contained less diverse microbial communities than did window-ventilated rooms. Bacterial communities in indoor environments contained many taxa that are absent or rare outdoors, including taxa closely related to potential human pathogens. Building attributes, specifically the source of ventilation air, airflow rates, relative humidity and temperature, were correlated with the diversity and composition of indoor bacterial communities. The relative abundance of bacteria closely related to human pathogens was higher indoors than outdoors, and higher in rooms with lower airflow rates and lower relative humidity. The observed relationship between building design and airborne bacterial diversity suggests that we can manage indoor environments, altering through building design and operation the community of microbial species that potentially colonize the human microbiome during our time indoors.

Incorporating 16S Gene Copy Number Information Improves Estimates of Microbial Diversity and Abundance

The abundance of different SSU rRNA (“16S”) gene sequences in environmental samples is widely used in studies of microbial ecology as a measure of microbial community structure and diversity. However, the genomic copy number of the 16S gene varies greatly – from one in many species to up to 15 in some bacteria and to hundreds in some microbial eukaryotes. As a result of this variation the relative abundance of 16S genes in environmental samples can be attributed both to variation in the relative abundance of different organisms, and to variation in genomic 16S copy number among those organisms. Despite this fact, many studies assume that the abundance of 16S gene sequences is a surrogate measure of the relative abundance of the organisms containing those sequences. Here we present a method that uses data on sequences and genomic copy number of 16S genes along with phylogenetic placement and ancestral state estimation to estimate organismal abundances from environmental DNA sequence data. We use theory and simulations to demonstrate that 16S genomic copy number can be accurately estimated from the short reads typically obtained from high-throughput environmental sequencing of the 16S gene, and that organismal abundances in microbial communities are more strongly correlated with estimated abundances obtained from our method than with gene abundances. We re-analyze several published empirical data sets and demonstrate that the use of gene abundance versus estimated organismal abundance can lead to different inferences about community diversity and structure and the identity of the dominant taxa in microbial communities. Our approach will allow microbial ecologists to make more accurate inferences about microbial diversity and abundance based on 16S sequence data.

A general framework for the distance–decay of similarity in ecological communities

Species spatial turnover, or β-diversity, induces a decay of community similarity with geographic distance known as the distance–decay relationship. Although this relationship is central to biodiversity and biogeography, its theoretical underpinnings remain poorly understood. Here, we develop a general framework to describe how the distance–decay relationship is influenced by population aggregation and the landscape-scale species-abundance distribution. We utilize this general framework and data from three tropical forests to show that rare species have a weak influence on distance–decay curves, and that overall similarity and rates of decay are primarily influenced by species abundances and population aggregation respectively. We illustrate the utility of the framework by deriving an exact analytical expression of the distance–decay relationship when population aggregation is characterized by the Poisson Cluster Process. Our study provides a foundation for understanding the distance–decay relationship, and for predicting and testing patterns of beta-diversity under competing theories in ecology. Ecology Letters (2008) 11: 904–917

Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa

Polymicrobial bronchopulmonary infections in cystic fibrosis (CF) cause progressive lung damage and death. Although the arrival of Pseudomonas aeruginosa often heralds a more rapid rate of pulmonary decline, there is significant inter-individual variation in the rate of decline, the causes of which remain poorly understood. By coupling culture-independent methods with ecological analyses, we discovered correlations between bacterial community profiles and clinical disease markers in respiratory tracts of 45 children with CF. Bacterial community complexity was inversely correlated with patient age, presence of P. aeruginosa and antibiotic exposure, and was related to CF genotype. Strikingly, bacterial communities lacking P. aeruginosa were much more similar to each other than were those containing P. aeruginosa, regardless of antibiotic exposure. This suggests that community composition might be a better predictor of disease progression than the presence of P. aeruginosa alone and deserves further study.