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The Role of Ecological Theory in Microbial Ecology

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The Role of Ecological Theory in Microbial Ecology PERSPECTIVES many areas in which microorganisms are of ESSAY environmental and economic importance. For example, improved quantitative theory The role of ecological theory could increase the efficiency of wastewater treatment processes, through the predic- tion of optimal operating conditions and in microbial ecology conditions that are likely to result in system failure. Quantitative information on the James I. Prosser, Brendan J. M. Bohannan, Tom P. Curtis, Richard J. Ellis, links between microbial community structure, Mary K. Firestone, Rob P. Freckleton, Jessica L. Green, Laura E. Green, population dynamics and activities will also Ken Killham, Jack J. Lennon, A. Mark Osborn, Martin Solan, facilitate assessment and, potentially, mitiga- Christopher J. van der Gast and J. Peter W. Young tion of microbial contributions to climate change, and should lead to quantitative Abstract | Microbial ecology is currently undergoing a revolution, with predictions of the impact of climate change repercussions spreading throughout microbiology, ecology and ecosystem science. on microbial contributions to specific eco- The rapid accumulation of molecular data is uncovering vast diversity, abundant system processes. Given the high abundance, biomass, diversity and global activities of uncultivated microbial groups and novel microbial functions. This accumulation of microorganisms, the ecological theory that data requires the application of theory to provide organization, structure, has been developed for plants and animals mechanistic insight and, ultimately, predictive power that is of practical value, but is of limited value if it does not apply to the application of theory in microbial ecology is currently very limited. Here we microbial communities. Microorganisms argue that the full potential of the ongoing revolution will not be realized if arguably provide much better controlled and more manipulable experimental systems research is not directed and driven by theory, and that the generality of established for testing ecological theory than plants ecological theory must be tested using microbial systems. or animals, and such testing is essential to establish the generality of theory. The use of Bacteria and Archaea have an essential microbial processes (in, for example, better controlled microbial systems might role in earth system processes. They are wastewater treatment, industrial chemical also generate new theory that is relevant to ubiquitous, possess enormous metabolic and production, pharmaceutical production and plants and animals. physiological versatility and are essential to bioremediation), and the realization that Two factors limit the development of virtually all biogeochemical cycling proc- many nonspecific microbial processes such theory in microbial ecology. The first esses — microbial carbon and nitrogen are as biogeochemical cycling are essential for is a lack of data and associated insights. calculated to be, respectively, equivalent to ecosystem sustainability, understanding the This is due in large part to the difficulties and tenfold as great as the carbon and nitro- factors that control these processes is crucial. inherent in observing microorganisms in gen stored in plants1. Although small (~10–6 In our view, this can best be achieved by nature, which often have few distinguishing m), they are abundant (>1030 individuals generating theory that is based on existing morphological features and often cannot globally). Their phylogenetic and physiologi- observations and subsequent experimental be cultivated in the laboratory. The applica- cal diversity is considerably greater than that validation. tion of cultivation-independent molecular of animals and plants and their interactions techniques and their successors — genom- with other life forms are correspondingly The importance of theory ics, metagenomics, transcriptomics and more complex. Theory is used to classify, interpret and proteomics — has generated a plethora of Understanding the ecology of micro- predict the world around us. Without it, new and more comprehensive observations organisms is arguably one of the most microbial ecology is merely the accumula- of microorganisms in nature, but we still compelling intellectual challenges facing tion of situation-bound statements that lack the theoretical tools required to detect contemporary ecology. Although worthy for are of limited predictive ability, providing underlying principles and mechanisms. its intellectual merits alone, developing such microbiologists with few insights. Theory The second factor is cultural, in that the an understanding is essential to meet many has an essential role in developing an under- tools and disciplines of ecological theory of the major challenges facing human society standing of, and explaining the interactions are not part of the contemporary mindset today, such as the management of natural between, microorganisms and their physical, in microbiology. Ecological theory and ecosystems and the mitigation of climate chemical and biological environments. quantitative reasoning typically form only change. Despite this, the application of theory This understanding will be lacking if it is minor components of education in microbi- is severely lacking in microbial ecology solely qualitative, and a full understanding ology, and microbiologists have traditionally where, paradoxically, it is required most. Just therefore requires quantitative theory. used a detailed, reductionist approach that as ecological theory arose from natural his- Theory generates predictions that can be is based on understanding physiological tory to draw generalized conclusions from of practical value for policy makers, stake- mechanisms, with relatively little attention specific observations of organisms in their holders and society. A striking example is the paid to theory. Although the challenge environment, so microbiologists need theory use of epidemiological models to predict for the microbial ecologist might appear to interpret the plethora of observations the spread of human and plant pathogens to be the discovery (or recollection) of ever- that have been made since van Leeuwenhoek and the use of these predictions to inform and more fascinating details of a given system, first saw ‘animalcules’ more than 300 years implement control policies2. There is similar the theoretician aims to predict as much as ago. With the increasing reliance on specific potential value in applying theory in the possible about a system using as few of these 384 | MAY 2007 | VOLUME 5 www.nature.com/reviews/micro © 2007 Nature Publishing Group PERSPECTIVES details as possible; but the populations and systems and allow the much more effective might not lead to simple mapping between structures of microbial communities, by management of the natural world. molecular markers and an ecological niche. comparison with those of plants and ani- In the following sections we discuss More crucially, speciation, and ecological mals, remain inscrutable. The application of examples of areas of ecological theory that species definitions, must consider bacterial molecular techniques has demonstrated the might be particularly valuable in microbial gene-transfer processes, which are erratic need for discovery research, but in our view ecology. In doing this, we attempt to deter- and transfer only a small part of the genome. this can only be exploited if it is directed mine whether the particular characteristics They provide a potential mechanism for by insights gained from the application of of microorganisms present difficulties in maintaining biological species in Mayr’s theory. applying ecological theory that has been sense8, because an incoming gene can developed for plants and higher animals. replace the homologous copy in the genome, Current ecological theory We consider whether and where new theory maintaining the genetic cohesion of the An established body of theory exists for might be required for microorganisms to species. In addition, these processes can also plant and animal ecology but the differ- enhance or replace established ecological result in the horizontal transfer of genes with ences between microorganisms and ‘large’ theory. We also identify conceptual and no counterpart in the recipient that can be organisms, and the extent to which these dif- practical challenges faced by microbial maintained on a plasmid or integrated by ferences restrict the applicability of existing ecologists in applying quantitative ecological non-homologous recombination. However, theory to microbial ecology, often form an theory. the importance of homologous recombina- impasse that is tacitly accepted and seldom tion and horizontal transfer varies widely questioned. Commonly cited differences Ecological species concepts among well-studied bacterial species, and include the small size of microorganisms, Most ecological theory depends on a con- perhaps even more so among the uncultured high rates of population growth, high rates cept of species: population ecology counts masses in the environment. This hetero- and extent of dispersal, the vast abundance individuals within species whereas com- geneity is one reason why we are still far of microorganisms, and the unique aspects of munity ecology and macroecology count from a consensus on the nature of bacterial their biology (such as parasexuality or the number of species. Species are most species, as revealed at a recent Royal Society extremely hardy resting stages). However, commonly defined
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