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Journal ArticleDOI

Interactions in multispecies biofilms: do they actually matter?

01 Feb 2014-Trends in Microbiology (Trends Microbiol)-Vol. 22, Iss: 2, pp 84-91
TL;DR: The recent focus on complex bacterial communities has led to the recognition of interactions across species boundaries, particularly pronounced in multispecies biofilms, where synergistic interactions impact the bacterial distribution and overall biomass produced.
About: This article is published in Trends in Microbiology.The article was published on 2014-02-01. It has received 400 citations till now.
Citations
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Journal ArticleDOI
TL;DR: The fundamental role of the biofilm matrix is considered, 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.
Abstract: 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.

3,277 citations

Journal ArticleDOI
TL;DR: Recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed and questions are posed for targeted investigation of surface-specific community-level microbial features to advance understanding ofsurface-associated microbial community ecology and the biogeochemical functions of these communities.
Abstract: SUMMARY Biotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.

696 citations


Cites background from "Interactions in multispecies biofil..."

  • ...and element cycling (23, 52, 53, 55), contaminant (such as heavy metal) concentration and transfer in food webs (23), induction of benthic invertebrate larval settlement (10, 13, 56), and xenobiotic compound biodegradation (21, 30, 32, 57)....

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  • ...Interactions of microorganisms in close spatial juxtaposition within the biofilm matrix facilitate metabolic cooperation (1, 3, 19, 21, 22, 26, 30) and genetic exchanges due to both the physical structure of the biofilm and community-level communication among organisms (21, 22, 30, 31)....

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Journal ArticleDOI
TL;DR: The present review focuses on the principal mechanisms involved in the formation of biofilms of food-borne pathogens, where biofilm behaviour is driven by its three-dimensional heterogeneity and by species interactions within these biostructures, and the authors look at some emergent control strategies.

362 citations

Journal ArticleDOI
TL;DR: The fundamental roles of biofilm in protecting microbial exposure to extreme environmental stresses and the regulatory factors involved in biofilm formation are described.
Abstract: Microbial biofilms are communities of aggregated microbial cells embedded in a self-produced matrix of extracellular polymeric substances (EPS). Biofilms are recalcitrant to extreme environments, and can protect microorganisms from ultraviolet (UV) radiation, extreme temperature, extreme pH, high salinity, high pressure, poor nutrients, antibiotics, etc., by acting as “protective clothing”. In recent years, research works on biofilms have been mainly focused on biofilm-associated infections and strategies for combating microbial biofilms. In this review, we focus instead on the contemporary perspectives of biofilm formation in extreme environments, and describe the fundamental roles of biofilm in protecting microbial exposure to extreme environmental stresses and the regulatory factors involved in biofilm formation. Understanding the mechanisms of biofilm formation in extreme environments is essential for the employment of beneficial microorganisms and prevention of harmful microorganisms.

361 citations

Journal ArticleDOI
TL;DR: In this review, up-to-date data on both the intra- and inter-species interactions encountered in biofilms of these pathogens are presented and could lead to novel intervention strategies for controlling pathogenic biofilm formation in food processing environments and thus improve food safety.
Abstract: A community-based sessile life style is the normal mode of growth and survival for many bacterial species. Under such conditions, cell-to-cell interactions are inevitable and ultimately lead to the establishment of dense, complex and highly structured biofilm populations encapsulated in a self-produced extracellular matrix and capable of coordinated and collective behavior. Remarkably, in food processing environments, a variety of different bacteria may attach to surfaces, survive, grow, and form biofilms. Salmonella enterica, Listeria monocytogenes, Escherichia coli, and Staphylococcus aureus are important bacterial pathogens commonly implicated in outbreaks of foodborne diseases, while all are known to be able to create biofilms on both abiotic and biotic surfaces. Particularly challenging is the attempt to understand the complexity of inter-bacterial interactions that can be encountered in such unwanted consortia, such as competitive and cooperative ones, together with their impact on the final outcome of these communities (e.g., maturation, physiology, antimicrobial resistance, virulence, dispersal). In this review, up-to-date data on both the intra- and inter-species interactions encountered in biofilms of these pathogens are presented. A better understanding of these interactions, both at molecular and biophysical levels, could lead to novel intervention strategies for controlling pathogenic biofilm formation in food processing environments and thus improve food safety.

243 citations


Cites background from "Interactions in multispecies biofil..."

  • ...However, biofilms in nature mostly comprisemultiple species, where inter-species interactions can shape the development, structure and function of these communities (Yang et al., 2011b; Elias and Banin, 2012; Rendueles and Ghigo, 2012; Burmølle et al., 2014)....

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  • ...Undoubtedly, biofilms should be envisioned as continuously evolving dynamic entities that cannot merely be seen as the sum of all components therein (Yang et al., 2011b; Burmølle et al., 2014)....

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References
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Journal ArticleDOI
21 May 1999-Science
TL;DR: Improvements in understanding of the genetic and molecular basis of bacterial community behavior point to therapeutic targets that may provide a means for the control of biofilm infections.
Abstract: Bacteria that attach to surfaces aggregate in a hydrated polymeric matrix of their own synthesis to form biofilms. Formation of these sessile communities and their inherent resistance to antimicrobial agents are at the root of many persistent and chronic bacterial infections. Studies of biofilms have revealed differentiated, structured groups of cells with community properties. Recent advances in our understanding of the genetic and molecular basis of bacterial community behavior point to therapeutic targets that may provide a means for the control of biofilm infections.

11,162 citations

Journal ArticleDOI
TL;DR: The functions, properties and constituents of the EPS matrix that make biofilms the most successful forms of life on earth are described.
Abstract: The microorganisms in biofilms live in a self-produced matrix of hydrated extracellular polymeric substances (EPS) that form their immediate environment. EPS are mainly polysaccharides, proteins, nucleic acids and lipids; they provide the mechanical stability of biofilms, mediate their adhesion to surfaces and form a cohesive, three-dimensional polymer network that interconnects and transiently immobilizes biofilm cells. In addition, the biofilm matrix acts as an external digestive system by keeping extracellular enzymes close to the cells, enabling them to metabolize dissolved, colloidal and solid biopolymers. Here we describe the functions, properties and constituents of the EPS matrix that make biofilms the most successful forms of life on earth.

7,041 citations

Journal ArticleDOI
TL;DR: It is evident that biofilm formation is an ancient and integral component of the prokaryotic life cycle, and is a key factor for survival in diverse environments.
Abstract: Biofilms--matrix-enclosed microbial accretions that adhere to biological or non-biological surfaces--represent a significant and incompletely understood mode of growth for bacteria. Biofilm formation appears early in the fossil record (approximately 3.25 billion years ago) and is common throughout a diverse range of organisms in both the Archaea and Bacteria lineages, including the 'living fossils' in the most deeply dividing branches of the phylogenetic tree. It is evident that biofilm formation is an ancient and integral component of the prokaryotic life cycle, and is a key factor for survival in diverse environments. Recent advances show that biofilms are structurally complex, dynamic systems with attributes of both primordial multicellular organisms and multifaceted ecosystems. Biofilm formation represents a protected mode of growth that allows cells to survive in hostile environments and also disperse to colonize new niches. The implications of these survival and propagative mechanisms in the context of both the natural environment and infectious diseases are discussed in this review.

6,170 citations

Journal ArticleDOI
TL;DR: Owing to the heterogeneous nature of the biofilm, it is likely that there are multiple resistance mechanisms at work within a single community.

3,578 citations

Journal ArticleDOI
TL;DR: Current concepts of biofilm tolerance are reviewed with special emphasis on the role of the biofilm matrix and the physiology ofBiofilm-embedded cells, and the heterogeneity in metabolic and reproductive activity within a biofilm correlates with a non-uniform susceptibility of enclosed bacteria.

1,730 citations