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18.5 N&V Feature Greenbe#822F58 18.5 N&V Feature Greenbe#822F58 12/5/06 6:34 PM Page 300 Vol 441|18 May 2006 NEWS & VIEWS FEATURE MICROBIAL SCIENCES The superficial life of microbes Roberto Kolter and E. Peter Greenberg The social activities and organization of bacteria are crucial to their ecological success. But it is only in recent years that we have begun to study these secret societies. Most surfaces on this planet teem with micro- and establish a sedentary yet remarkably liquid cultures, which produce homogeneous bial life, creating ecosystems of diverse organ- diverse community (Fig. 1a). These are com- populations of genetically identical cells, isms that flourish in slimy beds of their own munities in the sense that we humans organize growth in biofilms generates a large amount of making. The plaque encrusting our teeth, the ourselves into communities with division of genetic diversity 2. How can a single cell, with a slippery coating on river stones, the gunge labour — as the surface-associated population single genetic complement, give rise to a clogging up water pipes or infected wounds: grows, the biofilm becomes increasingly biofilm population in which the individual cells these are just a few examples of the microbial sophisticated in its activities, with individual are genetically different from one another? The ‘biofilms’ that form anywhere there is a surface cells taking on specific tasks. As a result, simplest explanation may be that in any biofilm, with a little moisture and some nutrients. biofilms can develop intricate architectures; individual cells are stuck in the same place, Although microbes by and large live in such striking mushroom-like structures can bloom attached to their neighbours and the slime that biofilm communities, most of our understand- on submerged surfaces, and aerial projections surrounds them, so their access to nutrients will ing of their physiology stems from experiments sprout from surfaces exposed to the air vary as gradients form within the biofilms using liquid cultures of dispersed, free-swim- (Fig. 1b,c). The diversity of biofilm architec- through metabolic activity. As a consequence, ming ‘planktonic’ cells. In the past decade, how- tures is akin to a miniature coral reef, with many microniches are likely to arise, as are ran- ever, the number of studies performed on their structures differing enormously depend- dom spontaneous mutants that can exploit surface-associated microbes has increased dra- ing on the species present and the environ- those microniches. As various mutants grow in matically. Today, we recognize that most, if not mental conditions. their location, the result will be a biofilm con- all, microbial species can form biofilms. The Natural biofilms nearly always harbour a taining a multitude of genotypes. This genetic physiological differences between free-living multitude of microbial species — the region diversity within a strain may provide a sort of individuals and communal biofilm-associated around a single tooth, for example, is often insurance, as the population can adapt better cells are becoming apparent, as are the regula- sheathed in a community of several hundred to sudden environmental changes than can a tory mechanisms that underlie the switch species1. Within such microbial ecosystems, genetically homogeneous population. between these two lifestyles. species richness may ensure stability of the To understand these minute ecosystems, it ecosystem in the face of changing environ- is necessary to be able to grow, observe and The diverse universe of biofilms mental conditions, very much as species rich- manipulate biofilms in the laboratory. This When individual bacterial cells encounter a ness is thought to aid the stability of macro- is accomplished using transparent flow cells, surface under conditions propitious for growth, scale ecosystems such as a tropical rainforest. where bacteria attach to a glass surface and they almost invariably undergo dramatic Even in the context of artificial, single- are continuously fed fresh nutrients3. The ensu- lifestyle changes. The nomadic single cells species biofilms, strain diversification seems to ing biofilm growth can be followed using settle down on the surface, where they divide be the rule. Unlike the growth of bacteria in confocal laser microscopy. In such flow cells, ab c Figure 1 | Biofilm formation and architecture. a, Individual bacteria b, These mushroom-like structures are characteristic of many submerged undergo a reversible lifestyle switch between a nomadic and a sedentary biofilms. In this Pseudomonas aeruginosa biofilm, which was grown existence. In the process, they lose motility and become enclosed in a gooey in a flow cell, they are about 150 Ȗm high. c, A biofilm of P. aeruginosa extracellular matrix. As the community grows, different cell types appear grown on a semi-solid agar surface (about 10 mm in diameter). The as the original strain diversifies to allow cells to take on different tasks colony displays aerial projections or wrinkling characteristic of an or to exist in different ‘microniches’, shown by differently coloured cells. air-exposed biofilm. 300 © 2006 Nature Publishing Group 18.5 N&V Feature Greenbe#822F58 12/5/06 6:34 PM Page 301 NATURE|Vol 441|18 May 2006 NEWS & VIEWS FEATURE experimental reproducibility is best obtained are carried out respectively by proteins that using single-species systems. As a consequence, Sedentary have structural domains possessing diguany- (biofilm) many microbial species have been analysed late cyclase and phosphodiesterase enzymatic as monocultures. Yet, in natural settings, these activities (referred to as GGDEF and EAL microbes nearly always grow in the context of Sensor domains, respectively, because of the highly multi-species communities. To approximate the GGDEF conserved amino-acid sequences they con- natural setting more closely, investigators have 2 GTP tain). Genomic analyses of dozens of microbial begun to foray into systems containing two or 2 GMP c-di-GMP genomes show that most bacteria harbour a more microbial species. Some potentially inter- pGpG multitude of these proteins — Vibrio vulnifi- esting multi-species model systems are poised cus, an extreme example, has 66 GGDEF for molecular analyses. Among these are EAL proteins and 33 EAL proteins18. Often, the mixed-species biofilms of the opportunistic Sensor GGDEF or EAL segment is fused to one pathogens Pseudomonas aeruginosa (a bac- of several types of environment-sensing terium) and Candida albicans (a fungus)4; two domains, implying that the production and Nomadic bacterial species that colonize teeth, Strepto- (planktonic) breakdown of c-di-GMP are controlled by the coccus gordonii and Veillonella atypica 5; and two bacterium’s surroundings. species that occur in the soil environment Figure 2 | The lifestyle switch. The second- The GGDEF and EAL proteins, and by around plant roots, P. aeruginosa and Agro- messenger molecule c-di-GMP mediates the extension c-di-GMP, are involved in many 6 bacterium tumefaciens . switch between nomadic and sedentary lifestyles. diverse cellular activities, but the mechanism Many species of bacteria have a multitude of by which c-di-GMP acts remains largely Sticking together enzymes capable of making c-di-GMP from GTP unknown. It may act to integrate the many Given the diversity of species that form (GGDEF proteins), and of breaking it down by external inputs sensed by GGDEF and EAL biofilms, it is not surprising that the molecular hydrolysing it into GMP (EAL proteins). Overall, proteins, allowing this single messenger to mechanisms involved in biofilm development it seems that increased intracellular levels of instigate multiple indirect effects. Or perhaps reflect the remarkable variety of the microbial c-di-GMP favour a sedentary existence, whereas there are small cellular ‘compartments’ where reduced levels of the second messenger favour world. Different species build biofilms differ- a nomadic existence. local fluctuations in the concentration of ently, and many strains have multiple biofilm- c-di-GMP cause independent outcomes. formation pathways. For instance, some that production of flagella and of extracellular Initially, c-di-GMP was shown to function by mutants of the soil bacterium Pseudomonas matrix are mutually exclusive processes: bac- activating the enzyme that synthesizes extra- fluorescens that cannot make a biofilm when teria give up the ability to move in order to set- cellular cellulose in Gluconoacetobacter xyli- grown with glucose as the sole carbon source tle down. The regulatory circuitry involved in nus. This activity occurs at what is known as do form biofilms when the sole carbon source this lifestyle switch is beginning to be mapped the post-translational level, once the target is glutamate7. out. In Bacillus subtilis, for instance, the switch protein, in this case the enzyme, has been So, do any general principles emerge? One between flagellar synthesis and matrix pro- synthesized19. By extension, investigators feature that does seem to be common to all duction is controlled by the master gene regu- believed c-di-GMP acted exclusively at the biofilms is that the cells secrete a ‘matrix’ to lator SinR (refs 13–15). This protein directly post-translational level on enzymes in other hold themselves in place and to provide a represses genes encoding matrix components bacteria. But it now seems that c-di-GMP can buffer against the environment. The make-up and activates those encoding flagellar compo- affect many processes, not only
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