The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria
            <i>Streptomyces</i>

Hempel, Antje M.; Cantlay, Stuart; Molle, Virginie; Wang, Sheng Bing; Naldrett, Mike J.; Parker, Jennifer; Richards, David P.; Jung, Yong Gyun; Buttner, Mark J.; Flärdh, Klas

doi:10.1073/pnas.1207409109

Cited by 108 publications

(174 citation statements)

References 50 publications

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“…Although the amount of DivIVA coeluted with His-Scy was low, it was significantly higher compared with that in the control cell extracts, where very little, if any, His-Scy was present. Interestingly, in one of the preload samples, we detected multiple bands of DivIVA presumably corresponding to its different phosphorylated forms (24). The single DivIVA band that coeluted with His-Scy could indicate that Scy might interact only with a specific form of DivIVA.…”

Section: Protein-protein Interactions Confirm a Polar Assembly Of Coimentioning

confidence: 93%

Coiled-coil protein Scy is a key component of a multiprotein assembly controlling polarized growth inStreptomyces

Holmes¹,

Walshaw

Leggett³

et al. 2013

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

146

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Polarized growth in eukaryotes requires polar multiprotein complexes. Here, we establish that selection and maintenance of cell polarity for growth also requires a dedicated multiprotein assembly in the filamentous bacterium, Streptomyces coelicolor. We present evidence for a tip organizing center and confirm two of its main components: Scy (Streptomyces cytoskeletal element), a unique bacterial coiled-coil protein with an unusual repeat periodicity, and the known polarity determinant DivIVA. We also establish a link between the tip organizing center and the filamentforming protein FilP. Interestingly, both deletion and overproduction of Scy generated multiple polarity centers, suggesting a mechanism wherein Scy can both promote and limit the number of emerging polarity centers via the organization of the Scy-DivIVA assemblies. We propose that Scy is a molecular "assembler," which, by sequestering DivIVA, promotes the establishment of new polarity centers for de novo tip formation during branching, as well as supporting polarized growth at existing hyphal tips.bacterial polarized growth | polar multiprotein assembly | cell division | modified hendecad coiled coil H ow organisms, cells, or tissues establish polarity is one of the fundamental questions in developmental biology. In eukaryotes, from unicellular organisms to multicellular plants and animals, some of the core mechanisms for generating polarity are conserved (1). Sites for polarization must be selected using positional markers, followed by the recruitment of a complex assembly, which, in turn, orients cytoskeletal filaments that deliver vesicles to the particular sites. A specific example of polarity is polarized growth, during which cells select a single polarization site and generate elongated, cylindrical shapes, such as neuronal dendrites in animals, root hairs and pollen tubes in plants, hyphal growth of filamentous fungi, elongation of Schizosaccharomyces pombe, or the short period of polarized growth during budding in Saccharomyces cerevisiae. However, the presumed earliest examples of polarized growth can be found in bacteria. These include the actinomycete Streptomyces coelicolor, which is used as a model organism for studying morphological differentiation and filamentous growth.The complex life cycle of S. coelicolor begins with an ovoid spore that contains a single chromosome. During germination, long, multigenomic filaments (germ tubes) are formed, which branch regularly to generate a network of hyphal filaments. Branching is a necessity for exponential growth because the rate of tip elongation cannot exceed a certain maximum; hence, there is an exponential increase in the number of new tips. New tips develop on the lateral wall well behind the existing tip, a phenomenon also observed and described as apical dominance in eukaryotic filamentous fungi. When grown on semisolid agar medium, these hyphal filaments first grow across and into the solid medium, generating the vegetative mycelium, followed by the formation of an aerial mycelium by h...

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Section: Protein-protein Interactions Confirm a Polar Assembly Of Coimentioning

confidence: 93%

Coiled-coil protein Scy is a key component of a multiprotein assembly controlling polarized growth inStreptomyces

Holmes¹,

Walshaw

Leggett³

et al. 2013

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

146

View full text Add to dashboard Cite

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“…It is therefore possible that AfsR integrates signals from more than one STK-dependent signal transduction system. Remarkably, S. coelicolor AfsK is also implicated in the phosphorylation of a key determinant of mycelial polar growth, DivIVA (129). It was found that AfsK is almost entirely located at hyphal tips, where DivIVA is concentrated, as part of a "polarisome" that controls tip extension (Fig.…”

Section: The Afsk/afsr/afss System and A Possible Interface With Hyphmentioning

confidence: 99%

Molecular Regulation of Antibiotic Biosynthesis in Streptomyces

Liu

Chater

Chandra

et al. 2013

Microbiol Mol Biol Rev

608

536

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SUMMARY Streptomycetes are the most abundant source of antibiotics. Typically, each species produces several antibiotics, with the profile being species specific. Streptomyces coelicolor , the model species, produces at least five different antibiotics. We review the regulation of antibiotic biosynthesis in S. coelicolor and other, nonmodel streptomycetes in the light of recent studies. The biosynthesis of each antibiotic is specified by a large gene cluster, usually including regulatory genes (cluster-situated regulators [CSRs]). These are the main point of connection with a plethora of generally conserved regulatory systems that monitor the organism's physiology, developmental state, population density, and environment to determine the onset and level of production of each antibiotic. Some CSRs may also be sensitive to the levels of different kinds of ligands, including products of the pathway itself, products of other antibiotic pathways in the same organism, and specialized regulatory small molecules such as gamma-butyrolactones. These interactions can result in self-reinforcing feed-forward circuitry and complex cross talk between pathways. The physiological signals and regulatory mechanisms may be of practical importance for the activation of the many cryptic secondary metabolic gene cluster pathways revealed by recent sequencing of numerous Streptomyces genomes.

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“…Recent studies suggest that this strategy can be exploited by bacteria. For example, in S. coelicolor, the increased phosphorylation of DivIVA by the eukaryotic-like Ser/Thr protein kinase AfsK, which can be activated artificially or upon arrest of cell wall synthesis, leads to the disassembly of DivIVA foci at the hyphal tips with dramatic effects on apical growth and hyphal branching (Hempel et al, 2012). Hence, phosphorylation of DivIVA could modify its oligomerization state.…”

Section: Intrinsic Temporal and Spatial Patterning Through Cell Divisionmentioning

confidence: 99%

How do bacteria localize proteins to the cell pole?

Laloux

Jacobs‐Wagner

2014

Journal of Cell Science

162

158

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It is now well appreciated that bacterial cells are highly organized, which is far from the initial concept that they are merely bags of randomly distributed macromolecules and chemicals. Central to their spatial organization is the precise positioning of certain proteins in subcellular domains of the cell. In particular, the cell poles -the ends of rod-shaped cells -constitute important platforms for cellular regulation that underlie processes as essential as cell cycle progression, cellular differentiation, virulence, chemotaxis and growth of appendages. Thus, understanding how the polar localization of specific proteins is achieved and regulated is a crucial question in bacterial cell biology. Often, polarly localized proteins are recruited to the poles through their interaction with other proteins or protein complexes that were already located there, in a so-called diffusion-and-capture mechanism. Bacteria are also starting to reveal their secrets on how the initial pole 'recognition' can occur and how this event can be regulated to generate dynamic, reproducible patterns in time (for example, during the cell cycle) and space (for example, at a specific cell pole). Here, we review the major mechanisms that have been described in the literature, with an emphasis on the self-organizing principles. We also present regulation strategies adopted by bacterial cells to obtain complex spatiotemporal patterns of protein localization.

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The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces

Cited by 108 publications

References 50 publications

Coiled-coil protein Scy is a key component of a multiprotein assembly controlling polarized growth inStreptomyces

Coiled-coil protein Scy is a key component of a multiprotein assembly controlling polarized growth inStreptomyces

Molecular Regulation of Antibiotic Biosynthesis in Streptomyces

How do bacteria localize proteins to the cell pole?

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