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A colloquium was convened in Longboat Key, Florida, in October 2002, by the American Academy of Microbiology to discuss the role of genomic techniques in microbiology research. Research professionals from both academia and industry met to discuss the current state of knowledge in microbial genomics. Unanswered questions that should drive future studies, technical challenges for applying genomics in microbial systems, and infrastructure and educational needs were discussed. Particular attention was focused on the great potential of genomic approaches to advance our understanding of microbial communities and ecosystems. Recommendations for activities that might promote and accelerate microbial genome science were identified and discussed.
Microbiology has always advanced in tandem with new technologies. Beginning with the first observations of microscopic organisms with early microscopes in the 17th century, the tools and methods for studying microbes have continually evolved. Slowly at first, and now with startling speed, scientists have developed increasingly complex and informative tools for analyzing the functions, interactions, and diversity of microorganisms. Today, genomic technologies are revolutionizing microbiology. Genomics employs all or part of the genome to answer questions about an organism and represents a generic tool that can be used to dissect any or all living cells. In this report, the term “genomics” includes structural genomic methods that focus on the determination of genomic sequence and higher order structural features, as well as functional genomic methods, which focus on the activities and products encoded by the genome.
To date, microbial genomics has largely been applied to individual, isolated microbial strains, with the results extrapolated to the wider world of microbial diversity. We are now presented with an opportune moment to move beyond studies of single isolates and to apply genome sciences directly to the study of microbial communities. It is now possible to adapt genomic tools and approaches to more realistic models of genome evolution and ecology involving natural microbial communities. Microbial communities are formed by organized groups of microbial species, each having different, often complementary functions or activities. In aggregate, the microbial community has emergent properties greater than the sum of its individual members. Outside the laboratory, virtually all microorganisms exist in complex assemblages, in which they exchange genetic material, nutrients, and biochemical signals with one another. While analysis of individual strains has been a highly profitable enterprise, greater strides can now be made by focusing attention on microbial communities. These are the entities that encompass the bulk of microbial interactions, evolutionary processes, and biogeochemical activities, with resulting immense impacts on human health and the entire planetary biosphere.
The natural microbial world can be viewed as a landscape of genes and genome ecology, in which organisms exchange genetic information and co-evolve with one another, shaping themselves and the biosphere over time. Microbial genomic evolution is crafted in microbial communities through the dynamic interplay of mutation, genetic drift, gene transfer, and natural selection. As it is currently envisioned, the application of genomic approaches to the study of microbial communities, i.e. “community genomics” or “metagenomics,” entails large-scale sequencing of pooled, community genomic material, with either random or targeted approaches, assembly of sequences into unique genomes or genome clusters, determination of variation in community gene and genome content or expression over space and time, and inference of global community activities, function, differentiation, and evolution from community genomic data.
With the aid of genomic techniques, scientists are poised to answer fundamental questions about the nature of microbial communities and the processes that shape and sustain them. Although there are few limits as to the phenomena that can be explored using these tools, certain areas of research deserve particular attention, due to their fundamental importance for understanding microbial life and due to their relative accessibility, given the current state-of-the-art. Outstanding questions about diversity and its generation and maintenance, ecosystem and community stability, and the relative significance of gene transfer in microbial communities need to be addressed.
Genomic techniques are a powerful set of methods, but there are certain technical hurdles to overcome before these techniques can be universally applied. Among these hurdles are the challenges of coordinating productive research programs centered around significant and tractable biological questions and applying appropriate and cost-effective technologies to answer them. One of the biggest challenges is the difficulty of coping with the tremendous complexity of microbial communities and their habitats and the difficulties in measuring all relevant biotic and environmental variables. Certain technical problems, such as identifying minority populations, deciphering diverse chromosome structures, and de-convoluting complex genome assembly problems, all need to be tackled to accelerate progress in microbial community genomics. In light of these technical challenges, establishing the proper biological and environmental contexts for genomic studies and developing new technology platforms and strategies are high priorities.
Microbial genome science can best be advanced by adopting multiple strategies and by addressing multiple levels of complexity in study systems. Investigations that focus on more simplistic model microbial communities will facilitate methods development. Less complex model systems will also allow multiple research groups to coordinate their work. Several recommendations are made with respect to the optimal attributes of model systems, and a few examples of such systems are explored. At the same time, genomic technologies are mature enough now to decipher the genomic characteristics of more complex microbial communities. Genomic investigations of microbial communities of global ecological, medical, or industrial importance should also begin immediately. Since genomic approaches generate vast amounts of data, improvements in information technology, database architecture, and data management strategies will significantly accelerate scientific progress. Outstanding unanswered questions include the amount and nature of within-population genetic diversity, the dynamics of genome evolutionary processes, and the levels of gene transfer in microbial communities.
A number of well recognized educational needs exist with respect to microbial genome science and are particularly critical for community genomics. These include cross-disciplinary training at the graduate and post-graduate levels, in fields that meld biology and computer science or mathematics.
Microbial genomics holds great promise for improving our world. By enabling a predictive understanding of the effects of perturbation on the microbial communities that impact human health and the environment, genomics could hold the key to treating diseases and managing the precious natural resources and processes that sustain life on this planet.