Chromosomal Circularization in<i>Streptomyces griseus</i>by Nonhomologous Recombination of Deletion Ends

Inoue, Shoichi; Higashiyama, Koji; Uchida, Tetsuya; Hiratsu, Keiichiro; Kinashi, Haruyasu

doi:10.1271/bbb.67.1101

Cited by 12 publications

(12 citation statements)

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“…Simple circularization (15,17) and arm replacement (35) of the S. griseus linear chromosome have been reported previously. Qin and Cohen (31) analyzed similar structural changes of pSLA2 derivatives and discussed the strategies of Streptomyces linear replicons after telomere damage.…”

Section: Discussionmentioning

confidence: 55%

“…The chromosomes with deletions subsequently display several types of rearrangements, including circularization, arm replacement, and amplification. Chromosomal circularization in Streptomyces was indicated by detection of a new fusion fragment (7,25,28) and was confirmed by cloning and sequencing of the fusion junction of the circularized chromosome (15,17). No homology and microhomology were detected between the right and left deletion ends of the circularized chromosomes.…”

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confidence: 99%

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Circularized Chromosome with a Large Palindromic Structure inStreptomyces griseusMutants

et al. 2004

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Streptomyces linear chromosomes display various types of rearrangements after telomere deletion, including circularization, arm replacement, and amplification. We analyzed the new chromosomal deletion mutants Streptomyces griseus 301-22-L and 301-22-M. In these mutants, chromosomal arm replacement resulted in long terminal inverted repeats (TIRs) at both ends; different sizes were deleted again and recombined inside the TIRs, resulting in a circular chromosome with an extremely large palindrome. Short palindromic sequences were found in parent strain 2247, and these sequences might have played a role in the formation of this unique structure. Dynamic structural changes of Streptomyces linear chromosomes shown by this and previous studies revealed extraordinary strategies of members of this genus to keep a functional chromosome, even if it is linear or circular.The filamentous soil bacteria belonging to the genus Streptomyces are unusual because they have an 8-to 9-Mb linear chromosome (5,26,37). Streptomyces genome projects have been completed for Streptomyces coelicolor A3(2), a model strain for Streptomyces genetics (3), and for Streptomyces avermitilis, an avermectin producer (14). Streptomyces species are also known to frequently have linear plasmids, which range from 12 to 1,700 kb long (10,19,21). For the most part these Streptomyces linear replicons have the same structural features; terminal inverted repeats (TIRs) are present at both ends, and a terminal protein is linked covalently to the 5Ј end (1, 39). Intramolecular interaction of two terminal proteins may combine two telomeres in circular form in living cells (40).Streptomyces linear chromosomes undergo telomere deletion spontaneously or after various mutagenic treatments (23,36). The sizes of deletions sometimes are up to 2 Mb (7). The chromosomes with deletions subsequently display several types of rearrangements, including circularization, arm replacement, and amplification. Chromosomal circularization in Streptomyces was indicated by detection of a new fusion fragment (7,25,28) and was confirmed by cloning and sequencing of the fusion junction of the circularized chromosome (15,17). No homology and microhomology were detected between the right and left deletion ends of the circularized chromosomes. This suggested that chromosomal circularization occurs by nonhomologous recombination between deletion ends. Furthermore, Qin and Cohen (31) reported that nonhomologous recombination also produced circular plasmids from linear plasmids with damaged telomeres. Therefore, circularization may be a common strategy of Streptomyces linear replicons when both of the telomeres are deleted.In addition to circularization, Streptomyces chromosomes have other structural changes that allow them to survive after the loss of an extreme end that is essential for terminal replication (12, 29). Fischer et al. (8) reported that homologous recombination of two sigma factor-like open reading frames (ORFs) caused chromosomal arm replacement in Streptomyces ambofaciens, wh...

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confidence: 55%

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Circularized Chromosome with a Large Palindromic Structure inStreptomyces griseusMutants

et al. 2004

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“…This may be the reason that the sizes of TIRs vary greatly in Streptomyces strains and that homologous genes or insertion elements are frequently found at the inside ends of TIRs, and this possibility was pointed out previously (34). When both telomeres are deleted, the extreme ends cannot be recovered, and therefore the chromosome will be circularized by nonhomologous recombination to survive (25,28). Long TIRs, which are formed by chromosomal arm replacement, also suffer telomere deletions.…”

Section: Discussionmentioning

confidence: 99%

Two Chimeric Chromosomes ofStreptomyces coelicolorA3(2) Generated by Single Crossover of the Wild-Type Chromosome and Linear Plasmid SCP1

Yamasaki

Kinashi

2004

J Bacteriol

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Streptomyces coelicolor A3(2) strain 2106 carries a 1.85-Mb linear plasmid, SCP1-cysD, in addition to a 7.2-Mb linear chromosome. Macrorestriction analysis indicated that both linear DNAs are hybrids of the wild-type chromosome and the linear plasmid SCP1 on each side. Nucleotide sequencing of the fusion junctions revealed no homology between the recombination regions. SCP1-cysD contains an SCP1 telomere and a chromosomal telomere at each end and therefore does not have terminal inverted repeats. In addition, SCP1-cysD could not be eliminated from strain 2106 by various mutagenic treatments. Thus, we concluded that both the 7.2-Mb chromosome and SCP1-cysD are chimeric chromosomes generated by a single crossover of the wild-type chromosome and SCP1. This may be regarded as a model of chromosomal duplication in genome evolution.Streptomyces species are gram-positive filamentous soil bacteria with a high GϩC composition (70 to 74%) and are well known for the production of a large number of secondary metabolites. Moreover, this genus is unusual among bacteria because its members have a linear chromosome (7,38,39,52) and a linear plasmid(s) (16,30,33). Streptomyces linear chromosomes and plasmids have the same principal structural features: terminal inverted repeats (TIRs) are present at both ends and a terminal protein is covalently linked to the 5Ј ends (1, 55).Streptomyces coelicolor A3(2), the genetically best studied Streptomyces species, contains a linear chromosome (45) as well as two sex plasmids, the linear plasmid SCP1 (18, 50) and the circular plasmid SCP2 (4, 47). Recently, genome projects have been completed for all three of these replicons, namely, the S. coelicolor A3(2) chromosome (8,668 kb) (2), SCP1 (356 kb) (3), and SCP2*, a derivative of SCP2 (31 kb) (15).Considerable attention has been given to SCP1 because of its interaction with the host chromosome. Hopwood and colleagues isolated variants carrying a hybrid SCP1-chromosome structure (18,19,21). Namely, SCP1 is integrated into the central region or other regions of the S. coelicolor A3(2) chromosome. Free SCP1-prime plasmids containing a certain chromosomal DNA stretch were also found. In matings with SCP1-free partners, SCP1-integrated strains showed either a unidirectional or bidirectional gradient of transfer of genetic markers with respect to the SCP1 integration site.Previous studies reported the integrated structures of SCP1 in the normal fertility (NF) strain 2612 and the NF-like strain A634 (14, 54). These strains show similar types of bidirectional DNA transfer, although the directions of SCP1 integration are opposite and the deletion sizes at each end are totally different. Therefore, the molecular reason for directional DNA transfer is still unknown. On the other hand, genetic studies of the cysB donor strain 1984 and the cysD donor strain 2106 suggested that they contained an SCP1-prime plasmid, either SCP1Ј-cysB or . A preliminary physical analysis revealed that SCP1Ј-cysB and SCP1Ј-cysD are giant linear plasmids, of 550 and 1,700 k...

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“…83, by generation of a fused fragment that hybridized to both the left and right deletion end probes (Lezhava et al, 1997). The fused fragments were cloned and sequenced, which revealed microhomology or no homology between the left and right deletion ends (Kameoka et al, 1999;Inoue et al, 2003). Thus, it was proved that chromosomal circularization occurred by nonhomologous recombination of deletion ends, and Streptomyces chromosomes could be replicated and maintained in both linear and circular forms (Fig.…”

Section: Rearrangements Of Streptomyces Linear Chromosomesmentioning

confidence: 99%

Antibiotic production, linear plasmids and linear chromosomes in Streptomyces

Kinashi¹

2008

Actinomycetologica

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Chromosomal Circularization inStreptomyces griseusby Nonhomologous Recombination of Deletion Ends

Cited by 12 publications

References 31 publications

Circularized Chromosome with a Large Palindromic Structure inStreptomyces griseusMutants

Circularized Chromosome with a Large Palindromic Structure inStreptomyces griseusMutants

Two Chimeric Chromosomes ofStreptomyces coelicolorA3(2) Generated by Single Crossover of the Wild-Type Chromosome and Linear Plasmid SCP1

Antibiotic production, linear plasmids and linear chromosomes in Streptomyces

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