The complete genome sequence of the acarbose producer Actinoplanes sp. SE50/110

Schwientek, Patrick; Szczepanowski, Rafael; Rückert, Christian; Kalinowski, Jörn; Klein, Andreas; Selber, Klaus; Wehmeier, Udo F.; Stoye, Jens; Pühler, Alfred

doi:10.1186/1471-2164-13-112

Cited by 73 publications

(47 citation statements)

References 110 publications

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“…strain SE50/110, Actinoplanes sp. strain N902-109, and Actinoplanes friuliensis (see Table S4 in the supplemental material) (18,33). Next, we used our previous RNA-Seq analysis data as the second selection filter, because performing a transcriptional analysis of weakly transcribed genes is difficult.…”

Section: Resultsmentioning

confidence: 99%

Regulation of Sporangium Formation by BldD in the Rare Actinomycete Actinoplanes missouriensis

et al. 2017

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The rare actinomycete Actinoplanes missouriensis forms sporangia, including hundreds of flagellated spores that start swimming as zoospores after their release. Under conditions suitable for vegetative growth, zoospores stop swimming and germinate. A comparative proteome analysis between zoospores and germinating cells identified 15 proteins that were produced in larger amounts in germinating cells. They include an orthologue of BldD (herein named AmBldD [BldD of A. missouriensis]), which is a transcriptional regulator involved in morphological development and secondary metabolism in Streptomyces. AmBldD was detected in mycelia during vegetative growth but was barely detected in mycelia during the sporangiumforming phase, in spite of the constant transcription of AmbldD throughout growth. An AmbldD mutant started to form sporangia much earlier than the wild-type strain, and the resulting sporangia were morphologically abnormal. Recombinant AmBldD bound a palindromic sequence, the AmBldD box, located upstream from AmbldD. 3=,5=-Cyclic di-GMP significantly enhanced the in vitro DNA-binding ability of AmBldD. A chromatin immunoprecipitation-sequencing analysis and an in silico search for AmBldD boxes revealed that AmBldD bound 346 genomic loci that contained the 19-bp inverted repeat 5=-NN(G/A)TNACN(C/G)N(G/C)NGTNA(C/T)NN-3= as the consensus AmBldDbinding sequence. The transcriptional analysis of 27 selected AmBldD target gene candidates indicated that AmBldD should repress 12 of the 27 genes, including bldM, ssgB, whiD, ddbA, and wblA orthologues. These genes are involved in morphological development in Streptomyces coelicolor A3(2). Thus, AmBldD is a global transcriptional regulator that seems to repress the transcription of tens of genes during vegetative growth, some of which are likely to be required for sporangium formation.IMPORTANCE The rare actinomycete Actinoplanes missouriensis undergoes complex morphological differentiation, including sporangium formation. However, almost no molecular biological studies have been conducted on this bacterium. BldD is a key global regulator involved in the morphological development of streptomycetes. BldD orthologues are highly conserved among sporulating actinomycetes, but no BldD orthologues, except one in Saccharopolyspora erythraea, have been studied outside the streptomycetes. Here, it was revealed that the BldD orthologue AmBldD is essential for normal developmental processes in A. missouriensis. The AmBldD regulon seems to be different from the BldD regulon in Streptomyces coelicolor A3(2), but they share four genes that are involved in morphological differentiation in S. coelicolor A3(2).KEYWORDS gene regulation, rare actinomycete, regulon, sporangium formation, transcriptional factor A ctinomycetes are Gram-positive, mainly soil-inhabiting bacteria. Many genera of actinomycetes show filamentous growth and produce spores, and therefore, actinomycetes are generally characterized by a complex morphological development. For

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Section: Resultsmentioning

confidence: 99%

Regulation of Sporangium Formation by BldD in the Rare Actinomycete Actinoplanes missouriensis

et al. 2017

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“…SE50/110 (GenBank accession no. NC_017803 [34]), Actinoplanes friuliensis HAG 010964 (GenBank accession no. NC_022657 [35]), and Actinoplanes sp.…”

Section: Resultsmentioning

confidence: 99%

Genetic and Transcriptional Analyses of the Flagellar Gene Cluster in Actinoplanes missouriensis

et al. 2016

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Actinoplanes missouriensis, a Gram-positive and soil-inhabiting bacterium, is a member of the rare actinomycetes. The filamentous cells produce sporangia, which contain hundreds of flagellated spores that can swim rapidly for a short period of time until they find niches for germination. These swimming cells are called zoospores, and the mechanism of this unique temporal flagellation has not been elucidated. Here, we report all of the flagellar genes in the bacterial genome and their expected function and contribution for flagellar morphogenesis. We identified a large flagellar gene cluster composed of 33 genes that encode the majority of proteins essential for assembling the functional flagella of Gram-positive bacteria. One noted exception to the cluster was the location of the fliQ gene, which was separated from the cluster. We examined the involvement of four genes in flagellar biosynthesis by gene disruption, fliQ, fliC, fliK, and lytA. Furthermore, we performed a transcriptional analysis of the flagellar genes using RNA samples prepared from A. missouriensis grown on a sporangium-producing agar medium for 1, 3, 6, and 40 days. We demonstrated that the transcription of the flagellar genes was activated in conjunction with sporangium formation. Eleven transcriptional start points of the flagellar genes were determined using the rapid amplification of cDNA 5= ends (RACE) procedure, which revealed the highly conserved promoter sequence CTCA(N 15-17 )GCCGAA. This result suggests that a sigma factor is responsible for the transcription of all flagellar genes and that the flagellar structure assembles simultaneously. IMPORTANCEThe biology of a zoospore is very interesting from the viewpoint of morphogenesis, survival strategy, and evolution. Here, we analyzed flagellar genes in A. missouriensis, which produces sporangia containing hundreds of flagellated spores each. Zoospores released from the sporangia swim for a short time before germination occurs. We identified a large flagellar gene cluster and an orphan flagellar gene (fliQ). These findings indicate that the zoospore flagellar components are typical of Gram-positive bacteria. However, the transcriptional analysis revealed that all flagellar genes are transcribed simultaneously during sporangium formation, a pattern differing from the orderly, regulated expression of flagellar genes in other bacteria, such as Salmonella and Escherichia coli. These results suggest a novel regulatory mechanism for flagellar formation in A. missouriensis.A ctinomycetes exhibit filamentous growth, and their hyphae are not motile. However, actinomycetes, which belong to a range of genera, including Actinoplanes, Catenuloplanes, Kineosporia, and Spirillospora, produce spores that can swim using the flagella prior to germination. These motile cells are called zoospores and are thought to specifically function for expansion into new habitats. Thus, zoospore-producing actinomycetes are motile only for a very short period of their complex life cycle. The zoospore biology is o...

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“…Furthermore, the widely used anti-diabetic drug acarbose (an alpha glucosidase inhibitor) was discovered in a bacterium [32]. The present study sought to identify novel ethnobotanical compounds which preferentially stimulate GLP-1 secretion but not GIP secretion.…”

Section: Introductionmentioning

confidence: 99%

Naturally-occurring TGR5 agonists modulating glucagon-like peptide-1 biosynthesis and secretion

et al. 2016

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The complete genome sequence of the acarbose producer Actinoplanes sp. SE50/110

Cited by 73 publications

References 110 publications

Regulation of Sporangium Formation by BldD in the Rare Actinomycete Actinoplanes missouriensis

Regulation of Sporangium Formation by BldD in the Rare Actinomycete Actinoplanes missouriensis

Genetic and Transcriptional Analyses of the Flagellar Gene Cluster in Actinoplanes missouriensis

Naturally-occurring TGR5 agonists modulating glucagon-like peptide-1 biosynthesis and secretion

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