Microbial landscapes : new paths to biofilm research Tom

| It is the best of times for biofilm research. Systems biology approaches are providing new insights into the genetic regulation of microbial functions, and sophisticated modelling techniques are enabling the prediction of microbial community structures. Yet it is also clear that there is a need for ecological theory to contribute to our understanding of biofilms. Here, we suggest a concept for biofilm research that is spatially explicit and solidly rooted in ecological theory, which might serve as a universal approach to the study of the numerous facets of biofilms. The importance of microorganisms in human health and disease, and the massive impact of the pure-culture approach devised by Robert Koch and others, has understandably led to a philosophy in microbiological research that emphasizes the study of microorganisms in pure liquid culture. This approach has so prominently pervaded microbiology that biofilm research was long neglected until microbiologists ‘re-discovered’ these fascinating communities almost 40 years ago1–3. Growing appreciation of the importance of biofilms has now led to the perception that these communities constitute the dominant mode of microbial life in most aquatic ecosystems1–3. Wherever free-swimming microbial cells encounter surfaces, they can switch from a planktonic lifestyle to form sessile communities that are enclosed by a slimy matrix. These communities often form striking architectures. A growing body of excellent reviews3–8 has plotted the highlights of biofilm research carried out over the last decade. Biofilms are now recognized as complex and dynamic communities in which substantial phenotypic diversification allows microorganisms to adapt to different environments. For instance, the hydrodynamic conditions and the availability of substrate and nutrients can shape biofilm architecture, whereas certain genes are essential for regulating the production of extracellular polymeric substances. Cell–cell communication can control biofilm development and architecture and, along with programmed cell death, seems to drive coordinated differentiation in mature biofilms and the release of dispersal cells. Microbiologists have discovered an unexpectedly high degree of coordinated multicellular behaviour that has led to the perception of biofilms as cities of microorganisms5. The intense research on singleor multispecies biofilms grown in flow cells1–3 and the continuing attempts to understand the role of biofilms in situ9–11 have both progressed our understanding of biofilm communities. Flow-cell work under standardized and optimized laboratory conditions echoes formal community theory that focuses on a single scale (in which scale is the temporal measure of a pattern or a process, or the level or degree of spatial resolution) and assumes that local communities are closed and isolated12. These laboratory experiments have unravelled many microbial interactions, including competition and cooperation, which are largely deterministic in nature and relate to theories of coexistence by niche differentiation. In the wild, however, biofilms are open and highly dynamic communities and exist as part of a larger microbial network. In this network, local communities are linked by dispersal and multiple interacting species to form a metacommunity. This introduces an explicitly spatial dimension to biofilm research, and, at the same time, calls for biofilm research that is solidly rooted in ecological concepts and unifying principles. Yet a sober examination of the latest research reveals that microbiologists lack such a framework13. Undoubtedly this is largely due to the diversity of the biofilm inhabitants and the habitats they occupy. The absence of a theoretical framework severely restricts the extension of biofilm research across multiple scales and limits our understanding of biofilms and their community interactions at the systems level. We have all walked through woods and seen seeds that are dispersed by the wind and carried away — and intuitively we accept the relationships between seed transport, vegetation patterns and the landscape. So why not import the tenets of landscape ecology and related fields into biofilm research? In this article, we propose that biofilms are microbial landscapes, to emphasize their spatially explicit dimension, and to lay the foundation for a unifying theoretical basis that supports and guides the relationships between biodiversity, ecosystem function and the effects of scales (composition, structure or function) in biofilm research. Biofilms are landscapes When we view a landscape, we look at the composition and expanse of elevations, valleys, rivers, vegetation and animals. Landscape ecology essentially studies the interactions between the spatial patterns of these landscape elements and the ecological processes operating within and between them14. Landscapes themselves can be defined as the configuration of patterns at any scale relative to the ecological processes or organisms under investigation, and the concept of landscape can therefore be applied to any scale or system14. The spatial patterns of organisms primarily result from abiotic factors, such as climate and landform, but organisms can also physically alter their environment and create spatial heterogeneity14. Resulting patches of resources and organisms are delineated by boundaries that control processes within the patches and regulate the flow of organisms and information through the landscape14–16. For instance, animals often move from one location to another because of the patchy distribution of resources and, at the same time, the heterogeneity of landscape elements (for example valleys and mountains) can enhance or inhibit their movement. This has logical implications for dispersal and the colonization of new niches or the invasion of existing communities. Patches and their boundaries also affect the transmission of communication signals, as canopy foliage, for instance, can absorb, attenuate and filter the song of birds. Yet boundaries in a patchy landscape also control material and energy fluxes and thereby ecosystem functioning. Landscape ecology therefore integrates various fields, such as neutral ecology, dispersal ecology, invasion ecology and ecosystem ecology, and is at the forefront of ecological science16. We advocate that biofilms should be viewed as microbial landscapes (FIG. 1a) and, at the same time, that they are interconnected parts of the larger landscape that they colonize. For instance, a biofilm in a stream is a system, but this system also interacts P E R S P E C T I V E S 76 | JANUARY 2007 | VOLUME 5 www.nature. com/reviews/micro © 2007 Nature Publishing Group