Alignment of multiple chromosomes along helical ParA scaffolding in sporulating <i>Streptomyces</i> hyphae

Jakimowicz, Dagmara; Żydek, Paulina; Kois, Agnieszka; Zakrzewska‐Czerwińska, Jolanta; Chater, Keith F.

doi:10.1111/j.1365-2958.2007.05815.x

Cited by 71 publications

(114 citation statements)

References 59 publications

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“…It is therefore unclear how streptomycetes avoid DNA damage in the multinucleoid hyphae. Elegant work on DNA partitioning revealed the important role of the ParAB proteins in DNA segregation during growth and development (299)(300)(301). FtsK helps to avoid "guillotining" of the DNA by pumping chromosomes into the spore compartments prior to septum closure, and ftsK mutants frequently generate spores with incomplete chromosomes (302)(303)(304).…”

Section: From Aerial Hyphae To Spores: Sporulation-specific Cell Divimentioning

confidence: 99%

Taxonomy, Physiology, and Natural Products of Actinobacteria

Barka

Vatsa

Sanchez

et al. 2016

Microbiol Mol Biol Rev

1,600

1,048

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SUMMARYActinobacteriaare Gram-positive bacteria with high G+C DNA content that constitute one of the largest bacterial phyla, and they are ubiquitously distributed in both aquatic and terrestrial ecosystems. ManyActinobacteriahave a mycelial lifestyle and undergo complex morphological differentiation. They also have an extensive secondary metabolism and produce about two-thirds of all naturally derived antibiotics in current clinical use, as well as many anticancer, anthelmintic, and antifungal compounds. Consequently, these bacteria are of major importance for biotechnology, medicine, and agriculture.Actinobacteriaplay diverse roles in their associations with various higher organisms, since their members have adopted different lifestyles, and the phylum includes pathogens (notably, species ofCorynebacterium,Mycobacterium,Nocardia,Propionibacterium, andTropheryma), soil inhabitants (e.g.,MicromonosporaandStreptomycesspecies), plant commensals (e.g.,Frankiaspp.), and gastrointestinal commensals (Bifidobacteriumspp.).Actinobacteriaalso play an important role as symbionts and as pathogens in plant-associated microbial communities. This review presents an update on the biology of this important bacterial phylum.

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Section: From Aerial Hyphae To Spores: Sporulation-specific Cell Divimentioning

confidence: 99%

Taxonomy, Physiology, and Natural Products of Actinobacteria

Barka

Vatsa

Sanchez

et al. 2016

Microbiol Mol Biol Rev

1,600

1,048

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“…2 D-G). Segregation of chromosomes is controlled by ParA and ParB in S. coelicolor and, interestingly, ParA forms distinct foci at the tips of the aerial hyphae before polymerization into ParA helices that act as scaffolds for the regular arrangement of ParB foci along the sporogenic aerial hyphae (37). It is conceivable that the nucleation of ParA at the tip of the aerial hyphae depends on the TIPOC.…”

Section: Discussionmentioning

confidence: 99%

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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“…Chromosomal Par proteins have been studied in many bacteria, including B. subtilis (35,48), Burkholderia cenocepacia (19), Caulobacter crescentus (12,21,53), Helicobacter pylori (42), Mycobacterium smegmatis (36,37), Pseudomonas aeruginosa (8,41), Pseudomonas putida (30,46), Streptomyces coelicolor (37), and Vibrio cholerae (25,64). These studies revealed several features of the par genes.…”

mentioning

confidence: 99%

“…(2) Their absence or overproduction causes at least some segregation defect, indicated by increased formation of anucleate cells, abnormal nucleoid compactness, and reduced separation of origin-proximal markers. (3) They contribute to other cellular processes, which include chromosome replication, cell division, and sporulation in B. subtilis (35,54), cell division in C. crescentus and S. coelicolor (12,21,37,52), and cell motility in P. aeruginosa (41).…”

mentioning

confidence: 99%

Participation of Chromosome Segregation Protein ParAI ofVibrio choleraein Chromosome Replication

et al. 2011

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Vibrio cholerae carries homologs of plasmid-borne parA and parB genes on both of its chromosomes. The par genes help to segregate many plasmids and chromosomes. Here we have studied the par genes of V. cholerae chromosome I. Earlier studies suggested that ParBI binds to the centromeric site parSI near the origin of replication (oriI), and parSI-ParBI complexes are placed at the cell poles by ParAI. Deletion of parAI and parSI caused the origin-proximal DNA to be less polar. Here we found that deletion of parBI also resulted in a less polar localization of oriI. However, unlike the deletion of parAI, the deletion of parBI increased the oriI number. Replication was normal when both parAI and parBI were deleted, suggesting that ParBI mediates its action through ParAI. Overexpression of ParAI in a parABI-deleted strain also increased the DNA content. The results are similar to those found for Bacillus subtilis, where ParA (Soj) stimulates replication and this activity is repressed by ParB (SpoOJ). As in B. subtilis, the stimulation of replication most likely involves the replication initiator DnaA. Our results indicate that control of chromosomal DNA replication is an additional function of chromosomal par genes conserved across the Gram-positive/Gram-negative divide.Replication and segregation are the two major processes needed to maintain a chromosome stably. In bacteria, there has been considerable progress in our understanding of the process of chromosome replication. How the replicated sister chromosomes segregate to opposite cell halves is also becoming clear (62,73). Other than those of Escherichia coli and its close homologs in the gammaproteobacteria, such as Haemophilus influenzae, most sequenced bacterial genomes have homologs of plasmid partition genes, parA and parB (29). Plasmid partitioning also requires a cis-acting sequence, parS (a centromere analog), to which ParB binds. The parS sequence is also well conserved in bacterial chromosomes (49). The par genes have been studied mostly in low-copy-number plasmids, such as P1, F, and R1, where they confer segregational stability (3,28,57). ParA is an ATPase and can be of three types (27). The actin-like ATPase belonging to plasmid R1 polymerizes to form filaments that link at each end with ParB-bound plasmid parS sites. Continued polymerization drives the plasmids to opposite cell poles (13). The second type of ATPase, characterized by Walker-box motifs, is more common. Members of this class of ParA also polymerize but appear to function by different mechanisms. The mechanisms involve a dynamic behavior of the ATPase, which seems to depend on the ParB/ parS complex, and in some cases chromosomal DNA that somehow distributes the plasmid copies maximally away from each other, thereby increasing the probability of their presence in opposite cell halves (1,6,14,22,33,34,47,65,74). Recently, a third type of par system, which uses tubulin-like GTPases (dubbed TubZ) in plasmid segregation, has been discovered (2,5,40,55).The chromosomally encoded Par proteins a...

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Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae

Cited by 71 publications

References 59 publications

Taxonomy, Physiology, and Natural Products of Actinobacteria

Taxonomy, Physiology, and Natural Products of Actinobacteria

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

Participation of Chromosome Segregation Protein ParAI ofVibrio choleraein Chromosome Replication

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