The Biofilm Mode of Life: Mechanisms and Adaptations Chapter Abstracts

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Chapter 2
The Biofilm Mode of Life
Staffan Kjelleberg and Michael Givskov

Recent advances in studies of biofilm systems have generated a wealth of novel information on multicellular prokaryotic biology and have established models for the formation of biofilms and the biology of their lifecycles. As a prelude to the subsequent chapters in this volume, this introductory article is aimed at identifying the contextual scientific and experimental framework for contemporary biofilm research programs, and addresses the strengths and weaknesses of some of the current key biofilm models. We will discuss whether or not a unique biofilm specific gene expression underpins our observations on biofilm structure and biology. Further, we will highlight the limitations inherent to current genetic and physiological analyses of bacterial biofilms, including the strengths and weaknesses of the molecular toolbox and the biofilm assays commonly employed. Moreover, the extent by which multiple parallel pathways of biofilm formation exist will be addressed, with reference also to applications for novel control strategies based on contemporary advances in studies of bacterial biofilms. The chapter will conclude by discussing the relevance of a consensus view of bacterial biofilm formation and biology.

Chapter 3
Do Not Fear Commitment: The Initial Transition to a Surface Lifestyle by Pseudomonads
D. P. MacEachran and G.A. O'Toole

This chapter aims to describe the early stages of biofilm formation, particularly on abiotic surfaces, by focusing on Pseudomonas aeruginosa. Specifically, we will dissect the early steps in the establishment of a multicellular community: i) translocation to the surface from a free-swimming planktonic lifestyle, ii) initial or reversible attachment, and finally iii) irreversible attachment. We will also compare the mechanisms used by P. aeruginosa to its related fluorescent pseudomonad cousins, Pseudomonas fluorescens and Pseudomonas putida. We argue that, for pseudomonads, irreversible attachment is the first committed step in the transition to a biofilm lifestyle.

Chapter 4
The Biofilm Matrix: A Sticky Framework
Sünje Johanna Pamp, Morten Gjermansen and Tim Tolker-Nielsen

The extracellular matrix of structured microbial communities constitutes the framework that holds the component cells together. Although the presence of cell-to-cell interconnecting matrices appears to be a common feature of structured microbial communities, there is a remarkable diversity in the composition of these matrices. Compounds such as polysaccharides, fimbriae, mating pili, and extracellular DNA can all function as extracellular matrix components. In the present chapter we provide examples of the diversity of biofilm matrices.

Chapter 5
Cyclic di-GMP As An Intracellular Signal Regulating Bacterial Biofilm Formation
J. M. Dow, Y. Fouhy, J. Lucey and R. P. Ryan

Cyclic di-GMP is a novel second messenger in bacteria that was first described as an allosteric activator of cellulose synthase in Gluconacetobacter xylinus. It is now established that this nucleotide regulates a range of functions including developmental transitions, aggregative behaviour, adhesion, biofilm formation and virulence in diverse bacteria. The level of cyclic di-GMP in bacterial cells is influenced by both synthesis and degradation. The GGDEF protein domain synthesises cyclic di-GMP, whereas EAL and HD-GYP domains are involved in cyclic di-GMP hydrolysis. Bacterial genomes encode a number of proteins with GGDEF, EAL and HD-GYP domains. The majority of these proteins contain additional signal input domains, suggesting that their activities are responsive to environmental cues. An emerging theme is that high cellular levels of cyclic di-GMP promote biofilm formation and aggregative behaviour whereas low cellular levels promote motility. The mechanism(s) by which cyclic di-GMP exerts its effects on these cellular functions is however poorly understood.

Chapter 6
N-Acylhomoserine Lactones, Quorum Sensing and Biofilm Development in Gram-negative Bacteria
Steve Atkinson, Miguel Camara and Paul Williams

Many different Gram negative bacteria employ N-acylhomoserine lactones (AHLs) as diffusible signal molecules which enable bacterial populations to co-ordinate gene expression as a function of cell population density. Such co-ordinated community behaviour, termed "quorum sensing" (QS) regulates diverse physiological processes including secondary metabolite production, motility, DNA transfer and pathogenicity. AHLs are produced during the biofilm mode of growth and AHL-dependent QS influences the development, integrity and architecture of biofilm communities as well as orchestrating the optimal timing and production of secondary metabolites to combat predators and host defence mechanisms. In most cases the identity of the QS-regulated target structural genes which contribute to biofilm development have not yet been identified. However, the increased susceptibility of biofilms formed by Pseudomonas aeruginosa QS mutants to conventional antibacterial agents and host defences highlights the utility of AHL-dependent QS as a novel antimicrobial target.

Chapter 7
Signaling in Escherichia coli Biofilms
Thomas K. Wood and William E. Bentley

Cell signaling in Escherichia coli biofilms is more important than originally known, in that autoinducer two (AI-2), AI-1 (N-acylhomoserine lactones), indole, hydroxylated indoles, norepinephrine, and epinephrine are all functional signals in this organism. This gives the bacterium the ability to monitor not only the presence of cells of its own species (through AI-2 and indole) but also the activity of the human host (through norepinephrine and epinephrine) as well as that of the other commensal bacteria (through hydroxylated indoles). We have also found that E. coli monitors the presence of bacteria that produce acylhomoserine lactones as these signals influence formation of its biofilms through the LuxR homolog SdiA. Hence, E. coli monitors its surroundings through signals it synthesizes as well as those synthesized by both prokaryotes and eukaryotes. In this chapter, we present recent findings on the role of these different signals as well as provide a detailed account of the complex features of uptake and regulation of the AI-2 signal in E. coli.

Chapter 8
Peptide Signaling
Jeremy M. Yarwood

The study of peptide signaling is yielding both fascinating and valuable information regarding bacterial biofilm development and helping to elucidate the disease processes caused by several human pathogens. Peptide signaling potentially impacts all stages of the biofilm "life-cycle" for many bacterial species, from attachment to maturation and detachment. While the particular roles of the signaling systems in biofilm formation varies among species, the implications of several phenomena, from natural transformation of streptococci to quorum sensing variant generation in staphylococci, may only be fully appreciated in the context of biofilms and cell-to-cell signaling. Understanding the mechanisms by which the peptide signaling systems exert their effects on biofilms may yield therapeutic strategies with limited, but important, uses.

Chapter 9
Differentiation and Dispersal in Biofilms
Jeremy S. Webb

Biofilm formation is now commonly associated with concepts of development, differentiation, and dispersal of microorganisms, and often more broadly with multicellular biological systems. This underlying theme of multicellularity among sessile microorganisms has undoubtably attracted significant fundamental research interest to the field. This chapter will summarize and discuss aspects of cellular differentiation in biofilms, including microcolony-based dispersal, autolysis of subpopulations of biofilm cells, and the recent finding that nitric oxide - a ubiquitous signal for cellular differentiation - can induce dispersal in Pseudomonas aeruginosa biofilms.

Chapter 10
Human Oral Multi-Species Biofilms: Bacterial Communities in Health and Disease
Paul E. Kolenbrander, Nicholas S. Jakubovics, Natalia I. Chalmers and Robert J. Palmer, Jr.

Possibly the first biofilm samples ever examined from a microbiological perspective were obtained from the oral cavity: Antonie van Leeuwenhoek's tooth scrapings. Since that time, oral microbiologists have made major contributions to microbial taxonomy, physiology, and ecology. The oral cavity distinguishes itself from other environments by having over 700 phylotypes (taxonomic units), nearly half of which have culturable representatives. Aerobic, facultatively anaerobic, and obligately anaerobic physiologies are present. Members of the microbial kingdoms Archaea, Bacteria and Fungi are present. What generates and maintains this diversity? Why are these communities attractive targets for study? How does community analysis using modern molecular methods differ from that using classical bacteriological approaches? We strive to answer these questions in the following contribution and, as far as possible, we rely on knowledge obtained from studies of plaque in situ.

Chapter 11
Biofilms as Refuge against Predation
Carsten Matz

Bacterial growth and survival in the environment as well as in association with human hosts are constrained by the action of phagocytic eukaryotic cells. Phagocytic predation on bacteria by host immune cells shares a number of cellular mechanisms with free-living protozoa. In and outside the human host, bacteria growing in biofilms appear to be less vulnerable to phagocytic predators than planktonic cells. Widespread resistance against predators is mediated by the interplay of biofilm-specific traits such as substratum adherence, exopolymer production, cellular cooperation, inhibitor secretion, and phenotypic variation. Selective predation is suggested to promote bacterial life in the biofilm niche and to govern structure-function relationships. There is increasing evidence that some of the pathogenicity traits may have their origin specifically in successful antipredator adaptations. Parallel selective pressures in and outside the human host may result in cross-adaptations of bacterial pathogens.

Chapter 12
Biofilms on Plant Surfaces
Leo Eberl, Susanne B. von Bodman and Clay Fuqua

Land plants modify the terrestrial environment extensively by nutrient acquisition, water utilization, physical disruption and cohesion of the soil, and the release of complex exudate materials. Decaying plant matter is also a major source of organic material in soils. Large numbers of microorganisms associate with and flourish on, within, and around plants, colonizing virtually all exposed tissues. While some of these microbes may incite disease on certain plants, a large number are harmless or beneficial symbionts. Microbial populations multiply in response to the plant environment and often form multicellular complexes that range from small aggregates to expansive, highly structured biofilms. Plant-associated biofilms have important consequences for plant health and disease, as the microorganisms within these populations may provide benefits or, conversely, damage the host. The structure, activity and microbial diversity harbored within biofilms influence the plant interaction to varying degrees, dependent on plant type, growth stage and environmental conditions. Likewise, plants influence the bacterial population density, fostering communities that interact with each other and the plant through metabolic activity and cell-cell communication mechanisms that allow the microbes to coordinate their activities and optimize their competitive success.

Chapter 13
Bacterial Biofilms on Fungal Surfaces
Deborah A. Hogan, Matthew J. Wargo and Nancy Beck

Bacterial biofilm formation on fungi participates in the synergistic degradation of substrates, antagonism of fungal growth, bacterial utilization of fungi as nutrient sources, and the formation of more complex synergistic associations for the purposes of nutrient acquisition. While bacterial biofilm formation has been described in many systems, the molecular mechanisms that govern these interactions are not yet well understood. Analysis of physical interactions between Pseudomonas aeruginosa and the dimorphic opportunistic fungal pathogen Candida albicans has provided insights into factors involved in attachment and matrix production, and has demonstrated a role for the bacterial quorum sensing molecule, 3-oxo-C12-homoserine lactone, within bacterial-fungal biofilms. Subsequent to P. aeruginosa biofilm formation on the fungus, extracellular bacterial products contribute to the death of the fungal hyphae. Studies focused on the interactions between bacteria and fungi in the rhizosphere have illustrated additional processes that contribute to bacterial biofilm formation on fungi including bacterial chemotaxis towards fungal cells, the cross feeding of nutrients between interacting species, and the expression of specific genes upon contact with fungal cells. By understanding bacterial biofilm formation on fungi, we will gain insight into economically important interactions, such as those involved in the bacterial biocontrol of fungal plant pathogens. Furthermore, using tractable bacterial-fungal biofilm model systems, we may uncover important elements of bacterial biofilms on other living surfaces such as plant and animal tissues.

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