Bacterial biofilms are formed by communities that are embedded in a self-produced matrix of extracellular polymeric substances (EPS). Importantly, bacteria in biofilms exhibit a set of 'emergent properties' that differ substantially from free-living bacterial cells. In this Review, we consider the fundamental role of the biofilm matrix in establishing the emergent properties of biofilms, describing how the characteristic features of biofilms - such as social cooperation, resource capture and enhanced survival of exposure to antimicrobials - all rely on the structural and functional properties of the matrix. Finally, we highlight the value of an ecological perspective in the study of the emergent properties of biofilms, which enables an appreciation of the ecological success of biofilms as habitat formers and, more generally, as a bacterial lifestyle.
Traditional treatment of infectious diseases is based on compounds that kill or inhibit growth of bacteria. A major concern with this approach is the frequent development of resistance to antibiotics. The discovery of communication systems (quorum sensing systems) regulating bacterial virulence has afforded a novel opportunity to control infectious bacteria without interfering with growth. Compounds that can override communication signals have been found in the marine environment. Using Pseudomonas aeruginosa PAO1 as an example of an opportunistic human pathogen, we show that a synthetic derivate of natural furanone compounds can act as a potent antagonist of bacterial quorum sensing. We employed GeneChip â microarray technology to identify furanone target genes and to map the quorum sensing regulon. The transcriptome analysis showed that the furanone drug speci®c-ally targeted quorum sensing systems and inhibited virulence factor expression. Application of the drug to P.aeruginosa bio®lms increased bacterial susceptibility to tobramycin and SDS. In a mouse pulmonary infection model, the drug inhibited quorum sensing of the infecting bacteria and promoted their clearance by the mouse immune response.
Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to 'barrens' when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.
The principles underlying the assembly and structure of complex microbial communities are an issue of long-standing concern to the field of microbial ecology. We previously analyzed the community membership of bacterial communities associated with the green macroalga Ulva australis, and proposed a competitive lottery model for colonization of the algal surface in an attempt to explain the surprising lack of similarity in species composition across different algal samples. Here we extend the previous study by investigating the link between community structure and function in these communities, using metagenomic sequence analysis. Despite the high phylogenetic variability in microbial species composition on different U. australis (only 15% similarity between samples), similarity in functional composition was high (70%), and a core of functional genes present across all algal-associated communities was identified that were consistent with the ecology of surface-and hostassociated bacteria. These functions were distributed widely across a variety of taxa or phylogenetic groups. This observation of similarity in habitat (niche) use with respect to functional genes, but not species, together with the relative ease with which bacteria share genetic material, suggests that the key level at which to address the assembly and structure of bacterial communities may not be "species" (by means of rRNA taxonomy), but rather the more functional level of genes.lateral gene transfer | biofilm | ecological model M etagenomic analysis of environmental microbial communities has revealed an enormous and previously unknown microbial diversity, and expanded our knowledge of their function in a variety of environments (1-5). Much still remains unknown, however, such as the principles underlying the assembly and structure of complex microbial communities, an issue of long-standing concern to the field of microbial ecology. To this aim, several recent studies have supported the "neutral hypothesis" (6-8), a largely stochastic model for community assembly, which assumes that species are ecologically equivalent and that community structure is determined by random processes (9, 10). However, there is also evidence that niche or deterministic processes play a role in community structure (11, 12); thus, both niche and neutral processes are likely to affect the assembly of complex microbial communities.Support for these models is based on species abundance distributions, and critical functional aspects, such as the assumption of ecological equivalence, have for the most part not been tested. In this study, we examine the encoded functions of an algalassociated bacterial community and link patterns of function to patterns of community assembly. Following the results of an earlier study (13), we investigate these communities in the context of the lottery hypothesis, a model for community "assembly" derived from studies of eukaryotic communities, such as coral reef fish (14). This hypothesis incorporates both neutral and functional aspects and arg...
In most environments, bacteria reside primarily in biofilms, which are social consortia of cells that are embedded in an extracellular matrix and undergo developmental programmes resulting in a predictable biofilm 'life cycle'. Recent research on many different bacterial species has now shown that the final stage in this life cycle includes the production and release of differentiated dispersal cells. The formation of these cells and their eventual dispersal is initiated through diverse and remarkably sophisticated mechanisms, suggesting that there are strong evolutionary pressures for dispersal from an otherwise largely sessile biofilm. The evolutionary aspect of biofilm dispersal is now being explored through the integration of molecular microbiology with eukaryotic ecological and evolutionary theory, which provides a broad conceptual framework for the diversity of specific mechanisms underlying biofilm dispersal. Here, we review recent progress in this emerging field and suggest that the merging of detailed molecular mechanisms with ecological theory will significantly advance our understanding of biofilm biology and ecology.
Acylated homoserine lactones (AHLs) play a widespread role in intercellular communication among bacteria. The Australian macroalga Delisea pulchra produces secondary metabolites which have structural similarities to AHL molecules. We report here that these metabolites inhibited AHL-controlled processes in prokaryotes. Our results suggest that the interaction between higher organisms and their surface-associated bacteria may be mediated by interference with bacterial regulatory systems.Acylated homoserine lactones (AHLs) serve as signals in bacterial communication. AHLs and their derivatives regulate bioluminescence, Ti plasmid transfer, production of virulence factors and antibiotics (for reviews, see references 15 and 24), and swarming motility (14). These bacterial processes are fundamental to the interaction of bacteria with each other, their environment, and, particularly, higher organisms. It might therefore be expected that plants or animals would have evolved strategies to interfere with bacterial AHL-mediated processes. The seaweed Delisea pulchra (Rhodophyta) produces a number of halogenated furanones (9), which are structurally similar to the bacterial AHLs ( Fig. 1) and have strong biological activity (7), including antifouling and antimicrobial properties (8,23). We hypothesized that these metabolites could interfere with bacterial processes which involve AHLdriven quorum-sensing systems. This hypothesis was tested in terms of responses known to be regulated by AHLs; swarming motility in Serratia liquefaciens (14) and bioluminescence produced by the marine bacterial strains Vibrio fischeri and Vibrio harveyi (15).Bacterial swarming is a multicellular, density-dependent behavior that is induced in response to recognition of surfaces with a certain viscosity. Cells differentiate into a multinucleated, elongated, and hyperflagellated form, orient themselves lengthwise in close contact with each other, and then move rapidly in a coordinated fashion over the surface of the growth substratum. Swarming has been described for a variety of bacteria, including members of the genera Serratia, Proteus, Vibrio, Bacillus, Escherichia, and Salmonella (1,2,17). For Proteus mirabilis and Vibrio parahaemolyticus, the ability to differentiate into the swarmer cell state plays an important role in bacterial virulence, surface adsorption, and colonization (3-5).S. liquefaciens is a suitable model organism, because members of the genus can colonize a wide variety of surfaces in water, soil, plants, insects, fish, and humans (16). The formation of a swarming colony of S. liquefaciens was recently shown to involve two genetic switches, the first of which encodes a quorum-sensing control mechanism employing at least two extracellular signal molecules, N-butanoyl-L-homoserine lactone (BHL) and N-hexanoyl-L-homoserine lactone ( Fig. 1 and reference 14). The second involves the flhDC master operon, which regulates expression of the flagellar regulon and governs control over swim and swarm cell differentiation (13).Development ...
Seaweeds (macroalgae) form a diverse and ubiquitous group of photosynthetic organisms that play an essential role in aquatic ecosystems. These ecosystem engineers contribute significantly to global primary production and are the major habitat formers on rocky shores in temperate waters, providing food and shelter for aquatic life. Like other eukaryotic organisms, macroalgae harbor a rich diversity of associated microorganisms with functions related to host health and defense. In particular, epiphytic bacterial communities have been reported as essential for normal morphological development of the algal host, and bacteria with antifouling properties are thought to protect chemically undefended macroalgae from detrimental, secondary colonization by other microscopic and macroscopic epibiota. This tight relationship suggests that macroalgae and epiphytic bacteria interact as a unified functional entity or holobiont, analogous to the previously suggested relationship in corals. Moreover, given that the impact of diseases in marine ecosystems is apparently increasing, understanding the role of bacteria as saprophytes and pathogens in seaweed communities may have important implications for marine management strategies. This review reports on the recent advances in the understanding of macroalgal-bacterial interactions with reference to the diversity and functional role of epiphytic bacteria in maintaining algal health, highlighting the holobiont concept.
Halogenated furanones produced by the macroalga Delisea pulchra inhibit AHL-dependent gene expression. This study assayed for an in vivo interaction between a tritiated halogenated furanone and the LuxR protein of Vibrio fischeri overproduced in Escherichia coli. Whilst a stable interaction between the algal metabolite and the bacterial protein was not found, it was noted by Western analysis that the half-life of the protein is reduced up to 100-fold in the presence of halogenated furanones. This suggests that halogenated furanones modulate LuxR activity but act to destabilize, rather than protect, the AHL-dependent transcriptional activator. The furanone-dependent reduction in the cellular concentration of the LuxR protein was associated with a reduction in expression of a plasmid encoded P luxI -gfp(ASV) fusion suggesting that the reduction in LuxR concentration is the mechanism by which furanones control expression of AHL-dependent phenotypes. The mode of action by which halogenated furanones reduce cellular concentrations of the LuxR protein remains to be characterized.
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