Regulation of apical growth and hyphal branching in Streptomyces

Flärdh, Klas; Richards, David P.; Hempel, Antje M.; Howard, Martin; Buttner, Mark J.

doi:10.1016/j.mib.2012.10.012

Cited by 96 publications

(83 citation statements)

References 37 publications

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“…The localization of PopZ at the growing pole is reminiscent of other landmark proteins, such as DivIVA, which directs polar growth in Streptomyces (21,22). Despite its strict localization to the growth pole, we find that PopZ is not required to direct polar peptidoglycan biosynthesis in A. tumefaciens.…”

Section: Deletion Of Popz In a Tumefaciensmentioning

confidence: 69%

Absence of the Polar Organizing Protein PopZ Results in Reduced and Asymmetric Cell Division in Agrobacterium tumefaciens

et al. 2017

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Agrobacterium tumefaciens is a rod-shaped bacterium that grows by polar insertion of new peptidoglycan during cell elongation. As the cell cycle progresses, peptidoglycan synthesis at the pole ceases prior to insertion of new peptidoglycan at midcell to enable cell division. The A. tumefaciens homolog of the Caulobacter crescentus polar organelle development protein PopZ has been identified as a growth pole marker and a candidate polar growth-promoting factor. Here, we characterize the function of PopZ in cell growth and division of A. tumefaciens. Consistent with previous observations, we observe that PopZ localizes specifically to the growth pole in wild-type cells. Despite the striking localization pattern of PopZ, we find the absence of the protein does not impair polar elongation or cause major changes in the peptidoglycan composition. Instead, we observe an atypical cell length distribution, including minicells, elongated cells, and cells with ectopic poles. Most minicells lack DNA, suggesting a defect in chromosome segregation. Furthermore, the canonical cell division proteins FtsZ and FtsA are misplaced, leading to asymmetric sites of cell constriction. Together, these data suggest that PopZ plays an important role in the regulation of chromosome segregation and cell division.IMPORTANCE A. tumefaciens is a bacterial plant pathogen and a natural genetic engineer. However, very little is known about the spatial and temporal regulation of cell wall biogenesis that leads to polar growth in this bacterium. Understanding the molecular basis of A. tumefaciens growth may allow for the development of innovations to prevent disease or to promote growth during biotechnology applications. Finally, since many closely related plant and animal pathogens exhibit polar growth, discoveries in A. tumefaciens may be broadly applicable for devising antimicrobial strategies.KEYWORDS Agrobacterium, PopZ, cell polarity, chromosome segregation, cell division, growth polarity A grobacterium tumefaciens, the causative agent of crown gall disease in flowering plants, has been studied extensively with regard to pathogenesis and its ability to transfer engineered DNA to plant cells using the type IV secretion system encoded by multiple vir genes. More recent observations of A. tumefaciens growth have revealed that this bacterium exhibits polar growth during elongation (1, 2). In A. tumefaciens, as well as in other Rhizobiales, peptidoglycan is inserted at the new poles created by cell division until the cell doubles in length. The peptidoglycan synthesis is then directed to midcell to enable septum formation and cell division. The growth patterning of A.

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Section: Deletion Of Popz In a Tumefaciensmentioning

confidence: 69%

Absence of the Polar Organizing Protein PopZ Results in Reduced and Asymmetric Cell Division in Agrobacterium tumefaciens

et al. 2017

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“…In contrast to E. coli and B. subtilis various bacteria such as Mycobacteria, Streptomyces, are tip-growers (Flärdh et al 2012). How is rod-shape maintained for tipgrowers?…”

Section: Future Prospectsmentioning

confidence: 99%

Getting into shape: How do rod-like bacteria control their geometry?

Amir¹,

Teeffelen²

2014

Syst Synth Biol

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Rod-like bacteria maintain their cylindrical shapes with remarkable precision during growth. However, they are also capable to adapt their shapes to external forces and constraints, for example by growing into narrow or curved confinements. Despite being one of the simplest morphologies, we are still far from a full understanding of how shape is robustly regulated, and how bacteria obtain their near-perfect cylindrical shapes with excellent precision. However, recent experimental and theoretical findings suggest that cell-wall geometry and mechanical stress play important roles in regulating cell shape in rod-like bacteria. We review our current understanding of the cell wall architecture and the growth dynamics, and discuss possible candidates for regulatory cues of shape regulation in the absence or presence of external constraints. Finally, we suggest further future experimental and theoretical directions which may help to shed light on this fundamental problem.

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“…The Streptomyces life cycle can be broadly divided into two stages: vegetative growth and reproductive development. Unlike most bacteria, Streptomyces organisms are filamentous, and during the vegetative phase of their life cycle, they grow by hyphal tip extension and branching, ultimately forming an interwoven network of cells known as the vegetative mycelium (3). Under certain as yet poorly defined stress conditions, vegetative growth ceases, and reproductive growth ensues.…”

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confidence: 99%

Resuscitation-Promoting Factors Are Cell Wall-Lytic Enzymes with Important Roles in the Germination and Growth of Streptomyces coelicolor

et al. 2015

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Dormancy is a common strategy adopted by bacterial cells as a means of surviving adverse environmental conditions. For Streptomyces bacteria, this involves developing chains of dormant exospores that extend away from the colony surface. Both spore formation and subsequent spore germination are tightly controlled processes, and while significant progress has been made in understanding the underlying regulatory and enzymatic bases for these, there are still significant gaps in our understanding. One class of proteins with a potential role in spore-associated processes are the so-called resuscitation-promoting factors, or Rpfs, which in other actinobacteria are needed to restore active growth to dormant cell populations. The model species Streptomyces coelicolor encodes five Rpf proteins (RpfA to RfpE), and here we show that these proteins have overlapping functions during growth. Collectively, the S. coelicolor Rpfs promote spore germination and are critical for growth under nutrient-limiting conditions. Previous studies have revealed structural similarities between the Rpf domain and lysozyme, and our in vitro biochemical assays revealed various levels of peptidoglycan cleavage capabilities for each of these five Streptomyces enzymes. Peptidoglycan remodeling by enzymes such as these must be stringently governed so as to retain the structural integrity of the cell wall. Our results suggest that one of the Rpfs, RpfB, is subject to a unique mode of enzymatic autoregulation, mediated by a domain of previously unknown function (DUF348) located within the N terminus of the protein; removal of this domain led to significantly enhanced peptidoglycan cleavage. Streptomyces species are Gram-positive bacteria that abound in soil environments. They are renowned for their secondary metabolic capabilities; they produce a multitude of compounds that have found utility in both medicine and agriculture, including a vast array of antibiotics, chemotherapeutics, immunosuppressants, and antiparasitic agents (1). They are also well known for their complex, multicellular developmental cycle (2). The Streptomyces life cycle can be broadly divided into two stages: vegetative growth and reproductive development. Unlike most bacteria, Streptomyces organisms are filamentous, and during the vegetative phase of their life cycle, they grow by hyphal tip extension and branching, ultimately forming an interwoven network of cells known as the vegetative mycelium (3). Under certain as yet poorly defined stress conditions, vegetative growth ceases, and reproductive growth ensues. Here, unbranched filamentous cells, termed aerial hyphae, grow away from the vegetative mycelium and extend into the air. These cells then undergo a synchronous round of chromosome segregation, cell division, and cell wall modification to yield chains of dormant exospores (4). These spores are resistant to a wide variety of environmental insults and can be widely dispersed.A dormant cell state is not unique to the streptomycetes, and indeed many well-studied bacteria (e...

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Regulation of apical growth and hyphal branching in Streptomyces

Cited by 96 publications

References 37 publications

Absence of the Polar Organizing Protein PopZ Results in Reduced and Asymmetric Cell Division in Agrobacterium tumefaciens

Absence of the Polar Organizing Protein PopZ Results in Reduced and Asymmetric Cell Division in Agrobacterium tumefaciens

Getting into shape: How do rod-like bacteria control their geometry?

Resuscitation-Promoting Factors Are Cell Wall-Lytic Enzymes with Important Roles in the Germination and Growth of Streptomyces coelicolor

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