Structural Proteins Involved in Emergence of Microbial Aerial Hyphae

Wösten, Han A. B.; Richter, M.; Willey, Joanne M.

doi:10.1006/fgbi.1999.1130

Cited by 50 publications

(30 citation statements)

References 45 publications

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“…Surfactants can aid in the colonization of surfaces and acquisition of nutrients through their surface-wetting and detergent properties (20). More germane to the present study, surfactants have been shown to be required for the development of aerial structures in numerous microbes (36). Prior work had shown that the lanthionine-containing peptide SapB from S. coelicolor is required for raising aerial hyphae.…”

Section: Discussionmentioning

confidence: 65%

Interactions between Streptomyces coelicolor and Bacillus subtilis : Role of Surfactants in Raising Aerial Structures

2006

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Using mixed-species cultures, we have undertaken a study of interactions between two common sporeforming soil bacteria, Bacillus subtilis and Streptomyces coelicolor. Our experiments demonstrate that the development of aerial hyphae and spores by S. coelicolor is inhibited by surfactin, a lipopeptide surfactant produced by B. subtilis. Current models of aerial development by sporulating bacteria and fungi postulate a role for surfactants in reducing surface tension at air-liquid interfaces, thereby removing the major barrier to aerial growth. S. coelicolor produces SapB, an amphipathic peptide that is surface active and required for aerial growth on certain media. Loss of aerial hyphae in developmental mutants can be rescued by addition of purified SapB. While a surfactant from a fungus can substitute for SapB in a mutant that lacks aerial hyphae, not all surfactants have this effect. We show that surfactin is required for formation of aerial structures on the surface of B. subtilis colonies. However, in contrast to this positive role, our experiments reveal that surfactin acts antagonistically by arresting S. coelicolor aerial development and causing altered expression of developmental genes. Our observations support the idea that surfactants function specifically for a given organism regardless of their shared ability to reduce surface tension. Production of surfactants with antagonistic activity could provide a powerful competitive advantage during surface colonization and in competition for resources.Microbial populations in natural settings almost invariably consist of complex mixtures of species, yet most laboratory studies of bacterial physiology have focused on the artificial setting of single-species cultures. Relatively little is known, at the molecular level, about how bacteria of different species interact with each other when cocultivated. Nonetheless, what little we know about interspecies interactions makes it clear that individual cellular physiology and intercellular signaling can be greatly affected when two species are cocultured (12, 13, 31). As part of our ongoing interest in interspecies interactions, we have begun to analyze the effects of cocultivating two wellcharacterized soil bacteria that, in all likelihood, share habitats in the wild: Bacillus subtilis and Streptomyces coelicolor (1). Our rationale is that by studying cocultures of genetically tractable microorganisms that coexist in nature, we might be able to uncover some of the molecular mechanisms underlying their interactions.Our interest in studying possible interactions between B. subtilis and S. coelicolor is partly driven by the fact that both of these species enter elaborate developmental pathways as a consequence of nutrient limitation (3). These developmental pathways have been extensively studied and are characterized by the production of numerous secreted secondary metabolites and the formation of spores (4). Up to now, our knowledge of the molecular mechanisms governing secondary metabolite production and sporulation b...

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Section: Discussionmentioning

confidence: 65%

Interactions between Streptomyces coelicolor and Bacillus subtilis : Role of Surfactants in Raising Aerial Structures

2006

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“…Such a role for surface-active compounds in the structuring of microbial populations at interfaces is not unprecedented in the microbial world. Surfactants are known to play a role in the emergence of aerial hyphae in both fungi and the filamentous bacterium Streptomyces coelicolor (31,36) and in the formation of hydrophobic air channels in fruiting bodies of fungi (15). In addition, a recent study of fruiting body formation in the bacterium Bacillus subtilis showed that a mutant (sfp) deficient in surfactin production formed atypical surfaceassociated pellicle (biofilm) structures (2).…”

Section: Discussionmentioning

confidence: 99%

Rhamnolipid Surfactant Production Affects Biofilm Architecture in Pseudomonas aeruginosa PAO1

2003

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In response to certain environmental signals, bacteria will differentiate from an independent free-living mode of growth and take up an interdependent surface-attached existence. These surface-attached microbial communities are known as biofilms. In flowing systems where nutrients are available, biofilms can develop into elaborate three-dimensional structures. The development of biofilm architecture, particularly the spatial arrangement of colonies within the matrix and the open areas surrounding the colonies, is thought to be fundamental to the function of these complex communities. Here we report a new role for rhamnolipid surfactants produced by the opportunistic pathogen Pseudomonas aeruginosa in the maintenance of biofilm architecture. Biofilms produced by mutants deficient in rhamnolipid synthesis do not maintain the noncolonized channels surrounding macrocolonies. We provide evidence that surfactants may be able to maintain open channels by affecting cell-cell interactions and the attachment of bacterial cells to surfaces. The induced synthesis of rhamnolipids during the later stages of biofilm development (when cell density is high) implies an active mechanism whereby the bacteria exploit intercellular interaction and communication to actively maintain these channels. We propose that the maintenance of biofilm architecture represents a previously unrecognized step in the development of these microbial communities.Although bacteria are commonly viewed as solitary life forms, these organisms are more typically colonial creatures. In their natural settings, bacteria persist within microbial communities, where they exploit elaborate systems of intercellular interaction and communication to adjust to changing environmental parameters. Moreover, biofilm formation has also been linked to the emergence of a variety of opportunistic human pathogens (5). For example, organisms such as Staphylococcus epidermidis and Pseudomonas aeruginosa form biofilms on implants and dead or living tissue, thereby contributing to a variety of persistent infections.Thinking about bacterial populations as connected organisms capable of concerted multicellular activities has provided researchers with novel insights into microbial biology. The key to such multicellular behavior lies in the ability of each individual cell to sense and respond to information from nearby cells, and this behavior requires a certain population size or quorum of cells. The development of biofilms is a process that involves both a quorum of cells and multicellular behavior (6). Single-species biofilms are of particular interest due to their clinical importance and the monospecies biofilms formed by P. aeruginosa has become a prominent model for studying this aspect of microbial biology.The complex structure of microbial biofilms has only recently been determined. Detailed analysis by scanning confocal laser microscopy has shown that biofilms of P. aeruginosa formed on solid surfaces and exposed to a continuous flow of fresh nutrients are open, highly hydrate...

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“…These hydrophobins are small proteins that are secreted as monomers and self-assemble into rodlets that pack to form amphipathic monolayers at hydrophilic: hydrophobic boundaries, such as the surface of the growth medium (4). These proteins are extremely surface active and lower the surface tension of the aqueous growth medium, allowing hyphae to break through the surface and to produce aerial structures (5,6). Many of these aerial structures subsequently become coated with amyloid rodlets, creating a hydrophobic layer that serves multiple purposes, including conferring water resistance to spores for easier dispersal in air (7), preventing wetting or collapse of gas transfer channels (8), enhancing adherence to waxy surfaces such as leaves during infection of rice plants by Magnaporthe grisea (9), and mediating evasion of the immune system as is observed in Aspergillus fumigatus infections (10).…”

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confidence: 99%

Self-assembly of functional, amphipathic amyloid monolayers by the fungal hydrophobin EAS

Macindoe

Kwan

Ren

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

121

111

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The hydrophobin EAS from the fungus Neurospora crassa forms functional amyloid fibrils called rodlets that facilitate spore formation and dispersal. Self-assembly of EAS into fibrillar rodlets occurs spontaneously at hydrophobic:hydrophilic interfaces and the rodlets further associate laterally to form amphipathic monolayers. We have used site-directed mutagenesis and peptide experiments to identify the region of EAS that drives intermolecular association and formation of the cross-β rodlet structure. Transplanting this region into a nonamyloidogenic hydrophobin enables it to form rodlets. We have also determined the structure and dynamics of an EAS variant with reduced rodlet-forming ability. Taken together, these data allow us to pinpoint the conformational changes that take place when hydrophobins self-assemble at an interface and to propose a model for the amphipathic EAS rodlet structure.A myloid fibrils were first identified in association with human diseases, but recent discoveries show that the amyloid ultrastructure also contributes to important functions in normal biology (1, 2). In bacteria, fungi, insects, fish, and mammals, amyloid structures perform a wide variety of roles (3). Functional amyloids in the form of fibrillar rodlets composed of class I hydrophobin proteins are found in filamentous fungi. These hydrophobins are small proteins that are secreted as monomers and self-assemble into rodlets that pack to form amphipathic monolayers at hydrophilic: hydrophobic boundaries, such as the surface of the growth medium (4). These proteins are extremely surface active and lower the surface tension of the aqueous growth medium, allowing hyphae to break through the surface and to produce aerial structures (5, 6). Many of these aerial structures subsequently become coated with amyloid rodlets, creating a hydrophobic layer that serves multiple purposes, including conferring water resistance to spores for easier dispersal in air (7), preventing wetting or collapse of gas transfer channels (8), enhancing adherence to waxy surfaces such as leaves during infection of rice plants by Magnaporthe grisea (9), and mediating evasion of the immune system as is observed in Aspergillus fumigatus infections (10).Hydrophobins are characterized by the presence of eight cysteine residues that form four disulphide bonds, but the hydrophobin family can be further divided into two classes based on the spacing of the conserved cysteine residues and the nature of the amphipathic monolayers that they form (11). Class I, but not class II, hydrophobins form amyloid-like rodlets that are extremely robust and require treatment with strong acid to induce depolymerization. The amphipathic monolayers formed by class II hydrophobins are not fibrillar and can be dissociated by treatment with detergent and alcohol solutions. The soluble, monomeric forms of hydrophobins share a unique β-barrel topology, and all have a relatively large exposed hydrophobic area on the protein monomer surface (4). The diversity in sequence and chain length ...

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Structural Proteins Involved in Emergence of Microbial Aerial Hyphae

Cited by 50 publications

References 45 publications

Interactions between Streptomyces coelicolor and Bacillus subtilis : Role of Surfactants in Raising Aerial Structures

Interactions between Streptomyces coelicolor and Bacillus subtilis : Role of Surfactants in Raising Aerial Structures

Rhamnolipid Surfactant Production Affects Biofilm Architecture in Pseudomonas aeruginosa PAO1

Self-assembly of functional, amphipathic amyloid monolayers by the fungal hydrophobin EAS

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