PERSPECTIVES the relationships between seed transport, OPINION vegetation patterns and the landscape. So why not import the tenets of landscape ecology and Microbial landscapes: new paths to related fields into biofilm research? In this article, we propose that biofilms are micro- bial landscapes, to emphasize their spatially biofilm research explicit dimension, and to lay the foundation for a unifying theoretical basis that supports Tom J. Battin, William T. Sloan, Staffan Kjelleberg, Holger Daims, Ian M. Head, and guides the relationships between biodi- Tom P. Curtis and Leo Eberl versity, ecosystem function and the effects of scales (composition, structure or function) Abstract | It is the best of times for biofilm research. Systems biology approaches are in biofilm research. providing new insights into the genetic regulation of microbial functions, and sophisticated modelling techniques are enabling the prediction of microbial Biofilms are landscapes community structures. Yet it is also clear that there is a need for ecological theory to When we view a landscape, we look at the contribute to our understanding of biofilms. Here, we suggest a concept for biofilm composition and expanse of elevations, valleys, rivers, vegetation and animals. research that is spatially explicit and solidly rooted in ecological theory, which might Landscape ecology essentially studies the serve as a universal approach to the study of the numerous facets of biofilms. interactions between the spatial patterns of these landscape elements and the ecological The importance of microorganisms in behaviour that has led to the perception of processes operating within and between human health and disease, and the massive biofilms as cities of microorganisms5. them14. Landscapes themselves can be impact of the pure-culture approach devised The intense research on single- or multi- defined as the configuration of patterns at by Robert Koch and others, has understand- species biofilms grown in flow cells1–3 and the any scale relative to the ecological processes ably led to a philosophy in microbiologi- continuing attempts to understand the role or organisms under investigation, and the cal research that emphasizes the study of of biofilms in situ9–11 have both progressed concept of landscape can therefore be applied microorganisms in pure liquid culture. This our understanding of biofilm communities. to any scale or system14. The spatial patterns approach has so prominently pervaded Flow-cell work under standardized and opti- of organisms primarily result from abiotic microbiology that biofilm research was long mized laboratory conditions echoes formal factors, such as climate and landform, but neglected until microbiologists ‘re-discovered’ community theory that focuses on a single organisms can also physically alter their envi- these fascinating communities almost 40 scale (in which scale is the temporal measure ronment and create spatial heterogeneity14. years ago1–3. Growing appreciation of the of a pattern or a process, or the level or Resulting patches of resources and organisms importance of biofilms has now led to the degree of spatial resolution) and assumes that are delineated by boundaries that control perception that these communities consti- local communities are closed and isolated12. processes within the patches and regulate the tute the dominant mode of microbial life These laboratory experiments have unrav- flow of organisms and information through in most aquatic ecosystems1–3. Wherever elled many microbial interactions, including the landscape14–16. For instance, animals often free-swimming microbial cells encounter competition and cooperation, which are move from one location to another because surfaces, they can switch from a planktonic largely deterministic in nature and relate to of the patchy distribution of resources lifestyle to form sessile communities that are theories of coexistence by niche differentiation. and, at the same time, the heterogeneity of enclosed by a slimy matrix. These commu- In the wild, however, biofilms are open and landscape elements (for example valleys and nities often form striking architectures. highly dynamic communities and exist as part mountains) can enhance or inhibit their A growing body of excellent reviews3–8 of a larger microbial network. In this network, movement. This has logical implications for has plotted the highlights of biofilm local communities are linked by dispersal dispersal and the colonization of new niches research carried out over the last decade. and multiple interacting species to form a or the invasion of existing communities. Biofilms are now recognized as complex metacommunity. This introduces an explicitly Patches and their boundaries also affect the and dynamic communities in which sub- spatial dimension to biofilm research, and, at transmission of communication signals, stantial phenotypic diversification allows the same time, calls for biofilm research that is as canopy foliage, for instance, can absorb, microorganisms to adapt to different envi- solidly rooted in ecological concepts and uni- attenuate and filter the song of birds. Yet ronments. For instance, the hydrodynamic fying principles. Yet a sober examination of boundaries in a patchy landscape also control conditions and the availability of substrate the latest research reveals that microbiologists material and energy fluxes and thereby and nutrients can shape biofilm architec- lack such a framework13. Undoubtedly this ecosystem functioning. Landscape ecology ture, whereas certain genes are essential for is largely due to the diversity of the biofilm therefore integrates various fields, such as regulating the production of extracellular inhabitants and the habitats they occupy. The neutral ecology, dispersal ecology, invasion polymeric substances. Cell–cell communica- absence of a theoretical framework severely ecology and ecosystem ecology, and is at the tion can control biofilm development and restricts the extension of biofilm research forefront of ecological science16. architecture and, along with programmed across multiple scales and limits our under- We advocate that biofilms should be cell death, seems to drive coordinated standing of biofilms and their community viewed as microbial landscapes (FIG. 1a) and, differentiation in mature biofilms and the interactions at the systems level. at the same time, that they are intercon- release of dispersal cells. Microbiologists We have all walked through woods and nected parts of the larger landscape that they have discovered an unexpectedly high seen seeds that are dispersed by the wind colonize. For instance, a biofilm in a stream degree of coordinated multicellular and carried away — and intuitively we accept is a system, but this system also interacts 76 | JANUARY 2007 | VOLUME 5 www.nature.com/reviews/micro © 2007 Nature Publishing Group PERSPECTIVES with the surrounding landscape that is biofilms and locally reduce biomass, which is Whether trees grow protected on the formed by the streambed and the catchment. comparable to the wind-fall of canopy trees valley bottom or are exposed to wind on a Similarly, biofilms that form in the lungs of and the resulting gaps in forests. Grazing by mountain, it is the basic landscape topog- individuals with cystic fibrosis3 are integrated protozoa can further contribute to the patchy raphy and the related aerodynamics that into the lung landscape, and are exposed to distribution of biomass17 (FIG. 1a.). More gen- shape their canopies. Similarly, the texture the spatial heterogeneity of hydration and erally, boundary conditions induced either of the colonized surface determines the respiratory mucous viscosity. by wind or water dynamics are analogous in primary structure of biofilm topography. What do forested and microbial land- diverse situations including: the canopy of Whether biofilms coat a flat or a rough scapes have in common? In both landscapes, forests18, mosses19, soil crusts20 and biofilms21. surface determines their exposure to shear multiple physical and biological factors shape Such boundaries not only determine gaseous stress and mass transfer — and these sources the spatial configuration of the biomass. For and dissolved mass transfer, but also influence of spatial variation are rarely encountered in instance, flow-induced disturbance can erode the transport of seeds and other propagules. flow cells. In addition to the resident biofilm a Figure 1 | Biofilms as microbial landscapes. a | Bacterial biofilms colonizing a lung epithe- lium (left) that could also represent a single- or multispecies biofilm grown in a flow cell, and a microbial biofilm colonizing a sedimen- tary environment in the ‘wild‘ (right). Biofilms coalesce and accumulate biomass in slow flow 2 (1), but predominantly develop filamentous streamers floating in the fast flow (2). Turbulent flow and eddies that are induced by 3 the landscape topography might be preferen- 4 tial trajectories for dispersal cells to land (3). Grazing by protozoa increases the spatial 1 heterogeneity of the microbial landscape (4). b | Neutral theory predicts that demographic stochasticity (death, reproduction) but also immigration from a source community (meta- b Source community community) shapes local community assembly. Biotic interactions and cell–cell signalling might function as filters (dashed line) that dif- c ferentially influence the invasion success of immigrating cells. c | Confocal micrograph of microcolonies of a Pseudomonas aeruginosa biofilm