?-Butyrolactone autoregulators and receptor proteins in non-Streptomyces actinomycetes producing commercially important secondary metabolites

Choi, Sun-Uk; Lee, Chang-Kwon; Hwang, Yong-Il; Kinosita, Hiroshi; Nihira, Takuya

doi:10.1007/s00203-003-0591-y

Cited by 41 publications

(30 citation statements)

References 26 publications

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“…We previously designed a primer set (AF-V and AR-1) for this region and successfully used it to amplify and clone several receptor genes from Streptomyces species (Lee et al 2005) as well as from Kitasatospora setae (Choi et al 2004), a member of non-Streptomyces actinomycetes closely related phylogenetically to the genus Streptomyces. However, all our attempts with this primer set failed to amplify homologues of a receptor gene from more distantly related non-Streptomyces actinomycetes, such as A. mediterranei, although our previous study suggested the presence of a c-butyrolactone autoregulator-dependent system in these non-Streptomyces actinomycetes (Choi et al 2003), suggesting that the sequence for the HTH motif may deviate slightly from those in the Streptomyces autoregulator receptors. Thus, we redesigned degenerate primers (F4 and R1) for the HTH motif based on the sequence of the ksbA gene of K. setae, in which the nucleotides of the forward primer (primer F4) are shorter than those of AF-V and one nucleotide is changed, and the position of the reverse primer (primer R1) moves to the 3 0 -side of the HTH region compared with that of primer AR-1.…”

Section: Resultsmentioning

confidence: 93%

“…Recently, numerous regulatory cascades have been found in the genus Streptomyces, whereas there are only a few reports of them in closely related genera, including the so-called non-Streptomyces actinomycetes, which also provide a variety of medically and commercially important secondary metabolites. We previously proposed the possibility of a c-butyrolactone-autoregulator-mediated system in non-Streptomyces actinomycetes, such as Kitasatospora setae, Actinoplanes teichomyceticus, Micromonospora echinospora and Amycolatopsis mediterranei (Choi et al 2003), and demonstrated that KsbA from K. setae is an autoregulator receptor acting as a negative regulator on the biosynthesis of secondary metabolites (Choi et al 2004). However, from the phylogenetic viewpoint, the genus Kitasatospora is very closely related to the genus Streptomyces, whereas the genera Actinoplanes, Micromonospora and Amycolatopsis are more distantly related to Streptomyces.…”

Section: Introductionmentioning

confidence: 98%

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Isolation and characterization of bamA genes, homologues of the γ-butyrolactone autoregulator-receptor gene in Amycolatopsis mediterranei, a rifamycin producer

et al. 2008

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Four genes (bamA1, bamA2, bamA3 and bamA4) encoding homologues of the gamma-butyrolactone autoregulator receptor of Streptomyces were found and cloned from Amycolatopsis mediterranei, a typical non-Streptomyces actinomycetes and a producer of rifamycin, one of the major anti-tuberculosis drugs in clinical treatment. Transcriptional analysis demonstrated that bamA1 and bamA2 are transcribed in a growth-dependent manner, while bamA3 and bamA4 are constitutively transcribed during growth. Binding assays using (3)H-labeled autoregulator analogues as ligands confirmed that all of the recombinant BamA proteins expressed in Escherichia coli have clear binding activity toward several types of Streptomyces autoregulators. The ligand specificity of the recombinant BamA1 protein was identical to that of the crude cell-free lysates of A. mediterranei reported in our previous work. These results suggest that A. mediterranei, which is phylogenetically situated in a distal clade from the genus Streptomyces as non-Streptomyces actinomycetes, has an autoregulator-mediated signaling system.

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Section: Resultsmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 98%

Isolation and characterization of bamA genes, homologues of the γ-butyrolactone autoregulator-receptor gene in Amycolatopsis mediterranei, a rifamycin producer

et al. 2008

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“…We have previously reported that ␥-butyrolactone autoregulators and/or the receptor proteins were present in several non-Streptomyces actinomycetes (Kitasatospora setae IFO14216, Actinoplanes teichomyceticus IFO13999, Amycolatopsis mediterranei IFO13415, and Micromonospora echinospora IFO13250) (3,4). In the present study, a ␥-butyrolactone autoregulator receptor gene of K. setae was cloned for the first time from the genera of non-Streptomyces actinomycetes.…”

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confidence: 77%

Cloning and Functional Analysis by Gene Disruption of a Gene Encoding a γ-Butyrolactone Autoregulator Receptor fromKitasatospora setae

Choi

Lee²,

Hwang

et al. 2004

J Bacteriol

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␥-Butyrolactone autoregulator receptors of the genus Streptomyces have a common activity as DNA-binding transcriptional repressors, controlling secondary metabolism and/or morphological differentiation. A gene encoding a ␥-butyrolactone autoregulator receptor was cloned from a bafilomycin B 1 producer, Kitasatospora setae, for the first time from a non-Streptomyces genus of actinomycetes, and its function was evaluated by in vitro and in vivo analyses. The gene fragment was initially cloned by PCR with primers designed from two highly conserved regions of Streptomyces autoregulator receptors (BarA, FarA, ScbR, and ArpA), followed by genomic Southern hybridization yielding a 7-kb BamHI fragment on which a 654-bp receptor gene (ksbA) was identified. The recombinant KsbA protein demonstrated clear binding activity toward 3 H-labeled autoregulators, especially toward [ 3 H]SCB1, confirming that ksbA encodes a real autoregulator receptor of K. setae. To clarify the in vivo function of ksbA, a ksbA-disrupted strain was constructed by means of homologous recombination after introducing a ksbA disruption construct via transconjugation from Escherichia coli. No difference in morphology was found between the wild-type strain and the ksbA disruptants. However, the ksbA disruptants started producing bafilomycin 18 h earlier than the wild-type strain and showed a 2.4-fold-higher accumulation of bafilomycin. The phenotype was restored to the original wild-type phenotype by complementation with intact ksbA, indicating that the autoregulator receptor protein of K. setae acts as a primary negative regulator of the biosynthesis of bafilomycin but plays no role in cytodifferentiation of K. setae. This indicates that, unlike the A-factor receptor of Streptomyces griseus, the autoregulator receptor (ksbA) of K. setae belongs to a family of autoregulator receptors which control secondary metabolism but play no role in morphological differentiation.The ␥-butyrolactone autoregulators found in several species of the genus Streptomyces are regarded as microbial hormones that control secondary metabolism and/or morphological differentiation. The effectiveness of these autoregulators, which are active at nanomolar concentrations, as well as the presence of specific receptor proteins [BarA as a virginiae butanolide (VB)-specific receptor in Streptomyces virginiae (11,12,22), FarA as an IM-2-specific receptor in Streptomyces lavendulae 29,35), ScbR as an SCB1-specific receptor in Streptomyces coelicolor A3(2) (33), and ArpA as an A-factor-specific receptor in Streptomyces griseus (25)] as mediators of autoregulator signaling implies that these ␥-butyrolactone autoregulators should be regarded as Streptomyces hormones. In vitro studies of the autoregulator receptors have indicated that these autoregulator receptors are dimeric DNA-binding proteins that, in the absence of autoregulators, recognize and bind to specific DNA sequences situated in the promoter region of target genes (13,14,16,33). Autoregulator binding to the corresponding recepto...

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“…39 These quorumdependent autoregulators, analogous to the homoserine lactones of some Gram-negative bacteria, 40 have been implicated in regulation of secondary metabolism and cellular differentiation in a number of actinomycetes. 41,42 …”

Section: Structures and Biosynthesismentioning

confidence: 99%

Streptogramins, Oxazolidinones, and Other Inhibitors of Bacterial Protein Synthesis

Mukhtar

Wright

2005

ChemInform

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?-Butyrolactone autoregulators and receptor proteins in non-Streptomyces actinomycetes producing commercially important secondary metabolites

Cited by 41 publications

References 26 publications

Isolation and characterization of bamA genes, homologues of the γ-butyrolactone autoregulator-receptor gene in Amycolatopsis mediterranei, a rifamycin producer

Isolation and characterization of bamA genes, homologues of the γ-butyrolactone autoregulator-receptor gene in Amycolatopsis mediterranei, a rifamycin producer

Cloning and Functional Analysis by Gene Disruption of a Gene Encoding a γ-Butyrolactone Autoregulator Receptor fromKitasatospora setae

Streptogramins, Oxazolidinones, and Other Inhibitors of Bacterial Protein Synthesis

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