Eukaryotic-type protein kinases in Streptomyces coelicolor: variations on a common theme

Petříčková, Kateřina; Petřı́ček, Miroslav

doi:10.1099/mic.0.26275-0

Cited by 78 publications

(50 citation statements)

References 53 publications

(41 reference statements)

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“…AfsK has an N-terminal STK domain and a C-terminal putative sensory portion carrying PQQ domain repeats. These PQQ domain repeats are predicted to form a β-propeller structure similar to WD40 domains and may interact with a ligand, although the general function of PQQ domains is not known (25). Further, AfsK does not have a predicted transmembrane segment, and is reported to be cytoplasmic but loosely associated with the membrane (28).…”

Section: Discussionmentioning

confidence: 99%

“…The S. coelicolor genome carries at least 34 genes predicted to encode STKs (25). Accordingly, we began systematically disrupting these genes, introducing the divIVA allele encoding the Nterminally FLAG-tagged version of the protein into the resulting mutants, and examining the pattern of DivIVA phosphorylation in FLAG-DivIVA/DivIVA mixtures immunoprecipitated from each strain.…”

Section: Diviva Phosphorylation Increases Dramatically When Cell Wallmentioning

confidence: 99%

“…The Actinobacteria are an ancient and deeply branching bacterial phylum in which STKs are particularly widespread and abundant. For example, Streptomyces coelicolor encodes at least 34 and Mycobacterium tuberculosis encodes 11 STKs (20,(24)(25)(26). In S. coelicolor, a recent phosphoproteomic survey detected at least 40 phosphoproteins (27), but the number of substrates is anticipated to be much larger, underlining the fundamental importance of actinobacterial STKs and the need for improved understanding of their substrates and biological functions.…”

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confidence: 99%

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

Hempel

Cantlay

Molle

et al. 2012

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

108

155

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In cells that exhibit apical growth, mechanisms that regulate cell polarity are crucial for determination of cellular shape and for the adaptation of growth to intrinsic and extrinsic cues. Broadly conserved pathways control cell polarity in eukaryotes, but less is known about polarly growing prokaryotes. An evolutionarily ancient form of apical growth is found in the filamentous bacteria Streptomyces, and is directed by a polarisome-like complex involving the essential protein DivIVA. We report here that this bacterial polarization machinery is regulated by a eukaryotic-type Ser/Thr protein kinase, AfsK, which localizes to hyphal tips and phosphorylates DivIVA. During normal growth, AfsK regulates hyphal branching by modulating branch-site selection and some aspect of the underlying polarisome-splitting mechanism that controls branching of Streptomyces hyphae. Further, AfsK is activated by signals generated by the arrest of cell wall synthesis and directly communicates this to the polarisome by hyperphosphorylating DivIVA. Induction of high levels of DivIVA phosphorylation by using a constitutively active mutant AfsK causes disassembly of apical polarisomes, followed by establishment of multiple hyphal branches elsewhere in the cell, revealing a profound impact of this kinase on growth polarity. The function of AfsK is reminiscent of the phoshorylation of polarity proteins and polarisome components by Ser/Thr protein kinases in eukaryotes.hyphal growth | protein phosphorylation | peptidoglycan | cytoskeleton | tip extension

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Section: Discussionmentioning

confidence: 99%

Section: Diviva Phosphorylation Increases Dramatically When Cell Wallmentioning

confidence: 99%

mentioning

confidence: 99%

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

Hempel

Cantlay

Molle

et al. 2012

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

108

155

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“…strain PCC 7120 (52; ref. 23), and the Gram-positive soil bacterium Streptomyces coelicolor 24 (34), also produce a large variety of natural products and have complex developmental cycles. These data support the emerging view that ELKs may play an equally important role to histidine protein kinases in modulating prokaryotic behaviors 22 .…”

Section: Phylogenomic Analysis Of S Cellulosum So Ce56mentioning

confidence: 99%

Complete genome sequence of the myxobacterium Sorangium cellulosum

et al. 2007

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The genus Sorangium synthesizes approximately half of the secondary metabolites isolated from myxobacteria, including the anti-cancer metabolite epothilone. We report the complete genome sequence of the model Sorangium strain S. cellulosum So ce56, which produces several natural products and has morphological and physiological properties typical of the genus. The circular genome, comprising 13,033,779 base pairs, is the largest bacterial genome sequenced to date. No global synteny with the genome of Myxococcus xanthus is apparent, revealing an unanticipated level of divergence between these myxobacteria. A large percentage of the genome is devoted to regulation, particularly post-translational phosphorylation, which probably supports the strain's complex, social lifestyle. This regulatory network includes the highest number of eukaryotic protein kinase-like kinases discovered in any organism. Seventeen secondary metabolite loci are encoded in the genome, as well as many enzymes with potential utility in industry.Natural products and their derivatives provide the basis for medicines targeting a wide range of human diseases. The Gram-negative myxobacteria, members of the d-subgroup of proteobacteria, are an important source of novel classes of secondary metabolites 1 . Of these, the genus Sorangium is particularly valuable, as 46% of metabolites isolated from myxobacteria 1 , including the potent antitumor compound epothilone 2 , derive from this group. The majority of myxobacterial metabolites are polyketides, nonribosomal polypeptides or hybrids of the two structures, many of which are synthesized on gigantic molecular assembly lines composed of polyketide synthase (PKS) and nonribosomal polypeptide synthetase (NRPS) multienzymes 3 . Sorangium strains exhibit additional characteristic features, including 'social behavior' , cell movement by gliding, biofilm formation and morphological differentiation culminating in complex multicellular structures called fruiting bodies 4 . Three myxobacterial suborders are known 5 and the availability of the genome sequence of Myxococcus xanthus (Cystobacterineae) 6 enables comparative analysis with the Sorangium cellulosum (Sorangiineae) genome to illuminate the basis for several important behavioral and metabolic differences. These include the ability of Sorangium strains to degrade complex plant materials (Fig. 1). S. cellulosum So ce56, an obligate aerobe, was established previously as a model Sorangium strain 7 by virtue of its favorable growth characteristics and ability to differentiate reproducibly under laboratory conditions. It synthesizes the cytotoxic chivosazoles 7 and the catecholate-type siderophores myxochelins 8 . Comparison of the complete genome sequence of strain S. cellulosum

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“…Two component systems, consisting of a histidine kinase with a cognate response regulator, are the most abundant signaling systems (5). Recent studies have shown that eukaryotic-type Ser/Thr protein kinases (STKs) also are present in a wide range of prokaryotic genomes and regulate complex and diverse cellular processes (6)(7)(8)(9)(10)(11)(12)(13).…”

mentioning

confidence: 99%

Control of cell division in Streptococcus pneumoniae by the conserved Ser/Thr protein kinase StkP

Beilharz

Novaková

Fadda

et al. 2012

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

160

276

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How the human pathogen Streptococcus pneumoniae coordinates cell-wall synthesis during growth and division to achieve its characteristic oval shape is poorly understood. The conserved eukaryotic-type Ser/Thr kinase of S. pneumoniae , StkP, previously was reported to phosphorylate the cell-division protein DivIVA. Consistent with a role in cell division, GFP-StkP and its cognate phosphatase, GFP-PhpP, both localize to the division site. StkP localization depends on its penicillin-binding protein and Ser/Thr-associated domains that likely sense uncross-linked peptidoglycan, because StkP and PhpP delocalize in the presence of antibiotics that target the latest stages of cell-wall biosynthesis and in cells that have stopped dividing. Time-lapse microscopy shows that StkP displays an intermediate timing of recruitment to midcell: StkP arrives shortly after FtsA but before DivIVA. Furthermore, StkP remains at midcell longer than FtsA, until division is complete. Cells mutated for stkP are perturbed in cell-wall synthesis and display elongated morphologies with multiple, often unconstricted, FtsA and DivIVA rings. The data show that StkP plays an important role in regulating cell-wall synthesis and controls correct septum progression and closure. Overall, our results indicate that StkP signals information about the cell-wall status to key cell-division proteins and in this way acts as a regulator of cell division.

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Eukaryotic-type protein kinases in Streptomyces coelicolor: variations on a common theme

Cited by 78 publications

References 53 publications

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

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

Complete genome sequence of the myxobacterium Sorangium cellulosum

Control of cell division in Streptococcus pneumoniae by the conserved Ser/Thr protein kinase StkP

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