Role of the Streptomyces spore wall synthesizing complex SSSC in differentiation of Streptomyces coelicolor A3(2)

Vollmer, B.; Steblau, Nadja; Ladwig, Nils; Mayer, Christoph; Maček, Boris; Mitousis, Lena; Sigle, Steffen; Walter, Axel; Wohlleben, Wolfgang; Muth, Günther

doi:10.1016/j.ijmm.2019.07.001

Cited by 5 publications

(6 citation statements)

References 57 publications

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“…The role of Ser/Thr/Tyr phosphorylation in the regulation of cell shape and sporulation has been reported for Mycobacterium (Molle and Kremer 2010 ; Kang et al 2005 ; Thakur and Chakraborti 2006 ; Prisic et al 2010 ) and Streptomyces (Vollmer et al 2019 ; Ladwig et al 2015 ). The PknA and PknB Ser/Thr/Tyr kinases strongly influence Mycobacterium cell shape, with either overexpression or depletion resulting in major alterations in cell morphology (Kang et al 2005 ).…”

Section: Discussionmentioning

confidence: 90%

“…Such phenotypes are not uncommon and are found in various other bacteria that are affected in the expression of Ser/Thr/Tyr kinases (Kang et al 2005 ). In Streptomyces , the Ser/Thr/Tyr kinases PkaI and PkaH regulate the activity of the so-called Streptomyces spore-wall synthesizing complex (SSSC), modulating spore size (Vollmer et al 2019 ; Ladwig et al 2015 ). The activity of DivIVA, which mediates polar growth and hyphae branching elongation, is modulated by the Ser/Thr kinase AfsK (Willemse et al 2011 ).…”

Section: Discussionmentioning

confidence: 99%

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FtsZ phosphorylation pleiotropically affects Z-ladder formation, antibiotic production, and morphogenesis in Streptomyces coelicolor

Yagüe

Willemse

Xiao

et al. 2022

Antonie van Leeuwenhoek

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The GTPase FtsZ forms the cell division scaffold in bacteria, which mediates the recruitment of the other components of the divisome. Streptomycetes undergo two different forms of cell division. Septa without detectable peptidoglycan divide the highly compartmentalised young hyphae during early vegetative growth, and cross-walls are formed that dissect the hyphae into long multinucleoid compartments in the substrate mycelium, while ladders of septa are formed in the aerial hyphae that lead to chains of uninucleoid spores. In a previous study, we analysed the phosphoproteome of Streptomyces coelicolor and showed that FtsZ is phosphorylated at Ser 317 and Ser389. Substituting Ser–Ser for either Glu–Glu (mimicking phosphorylation) or Ala–Ala (mimicking non-phosphorylation) hinted at changes in antibiotic production. Here we analyse development, colony morphology, spore resistance, and antibiotic production in FtsZ knockout mutants expressing FtsZ alleles mimicking Ser319 and Ser387 phosphorylation and non-phosphorylation: AA (no phosphorylation), AE, EA (mixed), and EE (double phosphorylation). The FtsZ-eGFP AE, EA and EE alleles were not able to form observable FtsZ-eGFP ladders when they were expressed in the S. coelicolor wild-type strain, whereas the AA allele could form apparently normal eGFP Z-ladders. The FtsZ mutant expressing the FtsZ EE or EA or AE alleles is able to sporulate indicating that the mutant alleles are able to form functional Z-rings leading to sporulation when the wild-type FtsZ gene is absent. The four mutants were pleiotropically affected in colony morphogenesis, antibiotic production, substrate mycelium differentiation and sporulation (sporulation timing and spore resistance) which may be an indirect result of the effect in sporulation Z-ladder formation. Each mutant showed a distinctive phenotype in antibiotic production, single colony morphology, and sporulation (sporulation timing and spore resistance) indicating that the different FtsZ phosphomimetic alleles led to different phenotypes. Taken together, our data provide evidence for a pleiotropic effect of FtsZ phosphorylation in colony morphology, antibiotic production, and sporulation.

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Section: Discussionmentioning

confidence: 90%

Section: Discussionmentioning

confidence: 99%

FtsZ phosphorylation pleiotropically affects Z-ladder formation, antibiotic production, and morphogenesis in Streptomyces coelicolor

Yagüe

Willemse

Xiao

et al. 2022

Antonie van Leeuwenhoek

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“…This cluster includes four of the five kinases belonging to the sco4775-sco4779 cluster encoding PkaH/SCO4775, SCO4776, PkaD/SCO4777, PkaI/SCO4778 (not detected), and PkaJ/SCO4779. Two of these EPK (PkaH and PkaI) were shown to be part of the spore wall synthesizing multi-protein complex SSSC which includes proteins directing peptidoglycan (MreBCD, PBP2, Sfr, RodZ) and cell wall glycopolymer synthesis (PdtA) [ 192 ]. PkaI and PkaH/SCO4775 were shown to phosphorylate MreC [ 193 ].…”

Section: Resultsmentioning

confidence: 99%

Comparative Proteomic Analysis of Transcriptional and Regulatory Proteins Abundances in S. lividans and S. coelicolor Suggests a Link between Various Stresses and Antibiotic Production

Lejeune

Cornu

Sago

et al. 2022

IJMS

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Streptomyces coelicolor and Streptomyces lividans constitute model strains to study the regulation of antibiotics biosynthesis in Streptomyces species since these closely related strains possess the same pathways directing the biosynthesis of various antibiotics but only S. coelicolor produces them. To get a better understanding of the origin of the contrasted abilities of these strains to produce bioactive specialized metabolites, these strains were grown in conditions of phosphate limitation or proficiency and a comparative analysis of their transcriptional/regulatory proteins was carried out. The abundance of the vast majority of the 355 proteins detected greatly differed between these two strains and responded differently to phosphate availability. This study confirmed, consistently with previous studies, that S. coelicolor suffers from nitrogen stress. This stress likely triggers the degradation of the nitrogen-rich peptidoglycan cell wall in order to recycle nitrogen present in its constituents, resulting in cell wall stress. When an altered cell wall is unable to fulfill its osmo-protective function, the bacteria also suffer from osmotic stress. This study thus revealed that these three stresses are intimately linked in S. coelicolor. The aggravation of these stresses leading to an increase of antibiotic biosynthesis, the connection between these stresses, and antibiotic production are discussed.

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“…Thus, our data strongly suggest that SRIM_017990 kinase likely has an important role in regulating OTC synthesis. Finally, we point out a cluster with PkaI and PkaH kinases involved in the regulation of sporulation septation and spore wall synthesis ( 60 ). We speculate that S. rimosus kinases, which exhibit phylogenetic relatedness to these kinases, might be involved in the regulation of pellet fragmentation in submerged cultures of S. rimosus when bacteria enter into the stationary phase ( 61 ).…”

Section: Resultsmentioning

confidence: 99%

Phosphoproteome Dynamics of Streptomyces rimosus during Submerged Growth and Antibiotic Production

et al. 2022

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Role of the Streptomyces spore wall synthesizing complex SSSC in differentiation of Streptomyces coelicolor A3(2)

Cited by 5 publications

References 57 publications

FtsZ phosphorylation pleiotropically affects Z-ladder formation, antibiotic production, and morphogenesis in Streptomyces coelicolor

FtsZ phosphorylation pleiotropically affects Z-ladder formation, antibiotic production, and morphogenesis in Streptomyces coelicolor

Comparative Proteomic Analysis of Transcriptional and Regulatory Proteins Abundances in S. lividans and S. coelicolor Suggests a Link between Various Stresses and Antibiotic Production

Phosphoproteome Dynamics of Streptomyces rimosus during Submerged Growth and Antibiotic Production

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