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.

Biofilms: an emergent form of bacterial life.

Most natural environments harbour a stunningly diverse collection of microbial species. In these communities, bacteria compete with their neighbours for space and resources. Laboratory experiments with pure and mixed cultures have revealed many active mechanisms by which bacteria can impair or kill other microorganisms. In addition, a growing body of theoretical and experimental population studies indicates that the interactions within and between bacterial species can have a profound impact on the outcome of competition in nature. The next challenge is to integrate the findings of these laboratory and theoretical studies and to evaluate the predictions that they generate in more natural settings.

Bacterial competition: surviving and thriving in the microbial jungle

Our knowledge of the microbiology of the phyllosphere, or the aerial parts of plants, has historically lagged behind our knowledge of the microbiology of the rhizosphere, or the below-ground habitat of plants, particularly with respect to fundamental questions such as which microorganisms are present and what they do there. In recent years, however, this has begun to change. Cultivation-independent studies have revealed that a few bacterial phyla predominate in the phyllosphere of different plants and that plant factors are involved in shaping these phyllosphere communities, which feature specific adaptations and exhibit multipartite relationships both with host plants and among community members. Insights into the underlying structural principles of indigenous microbial phyllosphere populations will help us to develop a deeper understanding of the phyllosphere microbiota and will have applications in the promotion of plant growth and plant protection.

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Microbial life in the phyllosphere

The rhizodeposition of plants dramatically influence the surrounding soil and its microflora. Root exudates have pronounced selective and promoting effects on specific microbial populations which are able to respond with chemotaxis and fast growth responses, such that only a rather small subset of the whole soil microbial diversity is finally colonizing roots successfully. The exudates carbon compounds provide readily available nutrient and energy sources for heterotrophic organisms but also contribute e.g. complexing agents, such as carboxylates, phenols or siderophores for the mobilization and acquisition of rather insoluble minerals. Root exudation can also quite dramatically alter the pH- and redox-milieu in the rhizosphere. In addition, not only specific stimulatory compounds, but also antimicrobials have considerable discriminatory effect on the rhizosphere microflora. In the “biased rhizosphere” concept, specific root associated microbial populations are favored based on modification of the root exudation profile. Rhizosphere microbes may exert specific plant growth promoting or biocontrol effects, which could be of great advantage for the plant host. Since most of the plant roots have symbiotic fungi, either arbuscular or ectomycorrhizal fungi, the impact of plants towards the rhizosphere extends also to the mycorrhizosphere. The selective effect of the roots towards the selection of microbes also extends towards the root associated and symbiotic fungi. While microbes are known to colonize plant roots endophytically, also mycorrhiza are now known to harbor closely associated bacterial populations even within their hyphae. The general part of the manuscript is followed by the more detailed presentation of specific examples for the selection and interaction of roots and microbes, such as in the rhizosphere of strawberry, potato and oilseed rape, where the soil-borne plant pathogen Verticillium dahliae can cause high yield losses; the potential of biocontrol by specific constituents of the rhizosphere microbial community is demonstrated. Furthermore, plant cultivar specificity of microbial communities is described in different potato lines including the case of transgenic lines. Finally, also the specific selective effect of different Medicago species on the selection of several arbuscular mycorrhizal taxa is presented.

Plant-driven selection of microbes

Pseudomonas aeruginosa causes severe and persistent infections in immune compromised individuals and cystic fibrosis sufferers. The infection is hard to eradicate as P. aeruginosa has developed strong resistance to most conventional antibiotics. The problem is further compounded by the ability of the pathogen to form biofilm matrix, which provides bacterial cells a protected environment withstanding various stresses including antibiotics. Quorum sensing (QS), a cell density-based intercellular communication system, which plays a key role in regulation of the bacterial virulence and biofilm formation, could be a promising target for developing new strategies against P. aeruginosa infection. The QS network of P. aeruginosa is organized in a multi-layered hierarchy consisting of at least four interconnected signaling mechanisms. Evidence is accumulating that the QS regulatory network not only responds to bacterial population changes but also could react to environmental stress cues. This plasticity should be taken into consideration during exploration and development of anti-QS therapeutics.

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The hierarchy quorum sensing network in Pseudomonas aeruginosa.

Quorum sensing faces evolutionary problems from non-producing or over-producing cheaters Such problems are circumvented in diffusion sensing, an alternative explanation for quorum sensing However, both explanations face the problems of signalling in complex environments such as the rhizosphere where, for example, the spatial distribution of cells can be more important for sensing than cell density, which we show by mathematical modelling We argue that these conflicting concepts can be unified by a new hypothesis, efficiency sensing, and that some of the problems associated with signalling in complex environments, as well as the problem of maintaining honesty in signalling, can be avoided when the signalling cells grow in microcolonies

Does efficiency sensing unify diffusion and quorum sensing

Higher organisms evolved in theomnipresence of microbes, which couldbe of pathogenic or symbiotic nature.A framework of response patterns evolvedwhich is known as innate immunity.A major part of this response is the recog-nition of microbial-associated molecularpatterns (MAMP) such as chitin orlipochitooligosaccharides, peptidogly-can, lipopolysaccharides or ﬂagellumstructures, and the initiation of efﬁ-cient plant defence reactions (Janewayand Medzhitov, 2002; Jones and Dangl,2006). However, there are many plant-associated endophytic bacteria known,which are living within plants withouttriggering persistent and apparent defenceresponses or visibly do not harm theplant. In some cases, even a stimulationof plant growth due to the presence ofspeciﬁc players within the plant micro-biome was reported (Turner et al., 2013).It is now generally accepted, that plantperformance and activities can only becharacterized and understood completely,if the “holobiont,” the plant plus theintimately associated microbiota, is con-sidered (Zilber-Rosenberg and Rosenberg,2008). The evolutionary advantage of anintegrated holobiontic system is char-acterized by a much better adaptabilityand ﬂexibility towards rapidly changingadverseenvironmentalconditions.Itisstillmostly unknown, which particular plantgeneticlociarecontrollingtheinteractionswith the plant microbiome and whichsignals are steering this cooperativity.Mutualistic microbes are able to overcomeor short-circuit plant defence responsesto enable successful colonization of thehost (Zamioudis and Pieterse, 2012;Alqueres et al., 2013). Beneﬁcial associa-tions with microbes other than mycorhizaor

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Bacterial quorum sensing compounds are important modulators of microbe-plant interactions

Biofilms are microbial communities encased in a layer of extracellular polymeric substances (EPS). The EPS matrix provides several functional purposes for the biofilm, such as protecting bacteria from environmental stresses, and providing mechanical stability. Quorum sensing is a cell-cell communication mechanism used by several bacterial taxa to coordinate gene expression and behaviour in groups, based on population densities. We mathematically model quorum sensing and EPS production in a growing biofilm under various environmental conditions, to study how a developing biofilm impacts quorum sensing, and conversely, how a biofilm is affected by quorum sensing-regulated EPS production. We investigate circumstances when using quorum-sensing regulated EPS production is a beneficial strategy for biofilm cells. We find that biofilms that use quorum sensing to induce increased EPS production do not obtain the high cell populations of low-EPS producers, but can rapidly increase their volume to parallel high-EPS producers. Quorum sensing-induced EPS production allows a biofilm to switch behaviours, from a colonization mode (with an optimized growth rate), to a protection mode. A biofilm will benefit from using quorum sensing-induced EPS production if bacteria cells have the objective of acquiring a thick, protective layer of EPS, or if they wish to clog their environment with biomass as a means of securing nutrient supply and outcompeting other colonies in the channel, of their own or a different species.

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A mathematical model of quorum sensing regulated EPS production in biofilm communities

Dynamic regulation of N-acyl-homoserine lactone production and degradation in Pseudomonas putida IsoF.

Background
Cell dispersal (or detachment) is part of the developmental cycle of microbial biofilms. It can be externally or internally induced, and manifests itself in discrete sloughing events, whereby many cells disperse in an instance, or in continuous slower dispersal of single cells. One suggested trigger of cell dispersal is quorum sensing, a cell-cell communication mechanism used to coordinate gene expression and behavior in groups based on population densities.

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Burkhard A. Hense

Papers

Does efficiency sensing unify diffusion and quorum sensing

Bacterial quorum sensing compounds are important modulators of microbe-plant interactions

A mathematical model of quorum sensing regulated EPS production in biofilm communities

Dynamic regulation of N-acyl-homoserine lactone production and degradation in Pseudomonas putida IsoF.

A Mathematical Model of Quorum Sensing Induced Biofilm Detachment.