Brendan J. M. Bohannan

Counting the Uncountable: Statistical Approaches to Estimating Microbial Diversity

All biologists who sample natural communities are plagued with the problem of how well a sample reflects a communitys “true” diversity. New genetic techniques have revealed extensive microbial diversity that was previously undetected with culture-dependent methods and morphological

Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors

One of the central aims of ecology is to identify mechanisms that maintain biodiversity. Numerous theoretical models have shown that competing species can coexist if ecological processes such as dispersal, movement, and interaction occur over small spatial scales. In particular, this may be the case for non-transitive communities, that is, those without strict competitive hierarchies. The classic non-transitive system involves a community of three competing species satisfying a relationship similar to the childrens game rock–paper–scissors, where rock crushes scissors, scissors cuts paper, and paper covers rock. Such relationships have been demonstrated in several natural systems. Some models predict that local interaction and dispersal are sufficient to ensure coexistence of all three species in such a community, whereas diversity is lost when ecological processes occur over larger scales. Here, we test these predictions empirically using a non-transitive model community containing three populations of Escherichia coli. We find that diversity is rapidly lost in our experimental community when dispersal and interaction occur over relatively large spatial scales, whereas all populations coexist when ecological processes are localized.

The Application of Ecological Theory Toward an Understanding of the Human Microbiome

The human-microbial ecosystem plays a variety of important roles in human health and disease. Each person can be viewed as an island-like “patch” of habitat occupied by microbial assemblages formed by the fundamental processes of community ecology: dispersal, local diversification, environmental selection, and ecological drift. Community assembly theory, and metacommunity theory in particular, provides a framework for understanding the ecological dynamics of the human microbiome, such as compositional variability within and between hosts. We explore three core scenarios of human microbiome assembly: development in infants, representing assembly in previously unoccupied habitats; recovery from antibiotics, representing assembly after disturbance; and invasion by pathogens, representing assembly in the context of invasive species. Judicious application of ecological theory may lead to improved strategies for restoring and maintaining the microbiota and the crucial health-associated ecosystem services that it provides.

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.

A taxa-area relationship for bacteria.

A positive power-law relationship between the number of species in an area and the size of that area has been observed repeatedly in plant and animal communities. This species–area relationship, thought to be one of the few laws in ecology, is fundamental to our understanding of the distribution of global biodiversity. However, such a relationship has not been reported for bacteria, and little is known regarding the spatial distribution of bacteria, relative to what is known of plants and animals. Here we describe a taxa–area relationship for bacteria over a scale of centimetres to hundreds of metres in salt marsh sediments. We found that bacterial communities located close together were more similar in composition than communities located farther apart, and we used the decay of community similarity with distance to show that bacteria can exhibit a taxa–area relationship. This relationship was driven primarily by environmental heterogeneity rather than geographic distance or plant composition.

The Competitive Cost of Antibiotic Resistance in Mycobacterium tuberculosis

Mathematical models predict that the future of the multidrug-resistant tuberculosis epidemic will depend on the fitness cost of drug resistance. We show that in laboratory-derived mutants of Mycobacterium tuberculosis, rifampin resistance is universally associated with a competitive fitness cost and that this cost is determined by the specific resistance mutation and strain genetic background. In contrast, we demonstrate that prolonged patient treatment can result in multidrug-resistant strains with no fitness defect and that strains with low- or no-cost resistance mutations are also the most frequent among clinical isolates.

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.

An ecological perspective on bacterial biodiversity

Bacteria may be one of the most abundant and species–rich groups of organisms, and they mediate many critical ecosystem processes. Despite the ecological importance of bacteria, past practical and theoretical constraints have limited our ability to document patterns of bacterial diversity and to understand the processes that determine these patterns. However, recent advances in molecular techniques that allow more thorough detection of bacteria in nature have made it possible to examine such patterns and processes. Here, we review recent studies of the distribution of free–living bacterial diversity and compare our current understanding with what is known about patterns in plant and animal diversity. From these recent studies a preliminary picture is emerging: bacterial diversity may exhibit regular patterns, and in some cases these patterns may be qualitatively similar to those observed for plants and animals.

PHYLOGENETIC CLUSTERING AND OVERDISPERSION IN BACTERIAL COMMUNITIES

Very little is known about the structure of microbial communities, despite their abundance and importance to ecosystem processes. Recent work suggests that bacterial biodiversity might exhibit patterns similar to those of plants and animals. However, relative to our knowledge about the diversity of macro-organisms, we know little about patterns of relatedness in free-living bacterial communities, and relatively few studies have quantitatively examined community structure in a phylogenetic framework. Here we apply phylogenetic tools to bacterial diversity data to determine whether bacterial communities are phylogenetically structured. We find that bacterial communities tend to contain lower taxonomic diversity and are more likely to be phylogenetically clustered than expected by chance. Such phylogenetic clustering may indicate the importance of habitat filtering (where a group of closely related species shares a trait, or suite of traits, that allow them to persist in a given habitat) in the assembly of bacterial communities. Microbial communities are especially accessible for phylogenetic analysis and thus have the potential to figure prominently in the integration of evolutionary biology and community ecology.

From Structure to Function: the Ecology of Host-Associated Microbial Communities

SUMMARY In the past several years, we have witnessed an increased interest in understanding the structure and function of the indigenous microbiota that inhabits the human body. It is hoped that this will yield novel insight into the role of these complex microbial communities in human health and disease. What is less appreciated is that this recent activity owes a great deal to the pioneering efforts of microbial ecologists who have been studying communities in non-host-associated environments. Interactions between environmental microbiologists and human microbiota researchers have already contributed to advances in our understanding of the human microbiome. We review the work that has led to these recent advances and illustrate some of the possible future directions for continued collaboration between these groups of researchers. We discuss how the application of ecological theory to the human-associated microbiota can lead us past descriptions of community structure and toward an understanding of the functions of the human microbiota. Such an approach may lead to a shift in the prevention and treatment of human diseases that involves conservation or restoration of the normal community structure and function of the host-associated microbiota.