Analysis of a genomic island housing genes for DNA S‐modification system in Streptomyces lividans 66 and its counterparts in other distantly related bacteria

The complete sequence (92 770 bp) of a genomic island (GI) named SLG from Streptomyces lividans 66, encoding a novel DNA S‐modification system (dnd), was determined. Its overall G+C content was 67.8%, lower than those of three sequenced Streptomyces genomes. Among 85 predicted open reading frames (ORFs) in SLG, 22 ORFs showed little homology with previously known proteins. SLG displays a mosaic structure composed of four modules, indicative of multiple recombination events in its formation. Spontaneous excision and circularization of SLG was observed, and the excision rate appeared to be induced at least fivefold by MNNG exposure. Using constructed mini‐islands of SLG, we demonstrated that Slg01, a P4‐like integrase, was sufficient to promote SLG integration, excision and circularization. Eleven counterpart dnd clusters, which also mapped to GIs in 10 chromosomes and a plasmid, were found in taxonomically unrelated bacterial species from various geographic niches. Additionally, c. 10% of actinomycetes were found to possess a dnd cluster in a survey involving 74 strains. Comparison of dnd clusters in the 12 bacteria strongly suggests that these dnd‐bearing elements might have evolved from a common ancestor similar to plasmid‐originated chromosome II of Pseudoalteromonas haloplanktis TAC125.

[1]  J. Tomizawa,et al.  Effect of ultraviolet irradiation on bacteriophage lambda immunity. , 1967, Journal of molecular biology.

[2]  D. Hanahan Studies on transformation of Escherichia coli with plasmids. , 1983, Journal of molecular biology.

[3]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[4]  J. Siedlecki,et al.  DNA methylation. Inhibition of de novo and maintenance methylation in vitro by RNA and synthetic polynucleotides. , 1984, The Journal of biological chemistry.

[5]  B. Migeon,et al.  Evidence for a relationship between DNA methylation and DNA replication from studies of the 5-azacytidine-reactivated allocyclic X chromosome. , 1985, Experimental cell research.

[6]  Z. Deng,et al.  Site-specific degradation of Streptomyces lividans DNA during electrophoresis in buffers contaminated with ferrous iron. , 1988, Nucleic acids research.

[7]  K. O'Brien,et al.  Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. , 1992, Gene.

[8]  D. Hopwood,et al.  A combined genetic and physical map of the Streptomyces coelicolor A3(2) chromosome , 1992, Journal of bacteriology.

[9]  J. Cullum,et al.  Physical map of the Streptomyces lividans 66 genome and comparison with that of the related strain Streptomyces coelicolor A3(2) , 1993, Journal of bacteriology.

[10]  Z. Deng,et al.  Characterization of phi HAU3, a broad-host-range temperate streptomyces phage, and development of phasmids , 1994, Journal of bacteriology.

[11]  Z. Deng,et al.  Streptomyces lividans 66 contains a gene for phage resistance which is similar to the phage λea59 endonuclease gene , 1994, Molecular microbiology.

[12]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[13]  F. Flett,et al.  High efficiency intergeneric conjugal transfer of plasmid DNA from Escherichia coli to methyl DNA-restricting streptomycetes. , 1997, FEMS microbiology letters.

[14]  P. Dyson,et al.  Novel post-replicative DNA modification in Streptomyces: analysis of the preferred modification site of plasmid pIJ101. , 1998, Nucleic acids research.

[15]  W. Wohlleben,et al.  The conjugative plasmid pSG5 from Streptomyces ghanaensis DSM 2932 differs in its transfer functions from other Streptomyces rolling-circle-type plasmids. , 1998, Microbiology.

[16]  K. Novak The complete genome sequence… , 1998, Nature Medicine.

[17]  C. Ronson,et al.  Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Volff,et al.  Genetic instability of the Streptomyces chromosome , 1998, Molecular microbiology.

[19]  J. Ishikawa,et al.  FramePlot: a new implementation of the frame analysis for predicting protein-coding regions in bacterial DNA with a high G + C content. , 1999, FEMS microbiology letters.

[20]  P. Dyson,et al.  Genetic instability associated with insertion of IS6100 into one end of the Streptomyces lividans chromosome. , 1999, Microbiology.

[21]  N. Dovichi,et al.  A multiple-capillary electrophoresis system for small-scale DNA sequencing and analysis. , 1999, Nucleic acids research.

[22]  M. Waldor,et al.  Site‐specific integration of the conjugal Vibrio cholerae SXT element into prfC , 1999, Molecular microbiology.

[23]  T. Kieser Practical streptomyces genetics , 2000 .

[24]  B. Tümmler,et al.  Achieving 100% Typeability of Pseudomonas aeruginosaby Pulsed-Field Gel Electrophoresis , 2000, Journal of Clinical Microbiology.

[25]  P. Kiley,et al.  The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  K. van Dijk,et al.  The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[27]  M. Bibb,et al.  Practical Streptomyces Genetics: A Laboratory Manual , 2000 .

[28]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[29]  Thomas L. Madden,et al.  Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. , 2001, Nucleic acids research.

[30]  R. Novick,et al.  Molecular genetics of SaPI1 – a mobile pathogenicity island in Staphylococcus aureus , 2001, Molecular microbiology.

[31]  Timothy J. Foster,et al.  Characterization of a Putative Pathogenicity Island from Bovine Staphylococcus aureus Encoding Multiple Superantigens , 2001, Journal of bacteriology.

[32]  S Karlin,et al.  Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. , 2001, Trends in microbiology.

[33]  Kelly P Williams,et al.  Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. , 2002, Nucleic acids research.

[34]  B. Barrell,et al.  Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) , 2002, Nature.

[35]  Z. Deng,et al.  'Streptomyces nanchangensis', a producer of the insecticidal polyether antibiotic nanchangmycin and the antiparasitic macrolide meilingmycin, contains multiple polyketide gene clusters. , 2002, Microbiology.

[36]  T. Finan Evolving Insights: Symbiosis Islands and Horizontal Gene Transfer , 2002, Journal of bacteriology.

[37]  Yvonne A O'Shea,et al.  Mobilization of the Vibrio pathogenicity island between Vibrio cholerae isolates mediated by CP-T1 generalized transduction. , 2002, FEMS microbiology letters.

[38]  J. R. van der Meer,et al.  Unusual Integrase Gene Expression on the clc Genomic Island in Pseudomonas sp. Strain B13 , 2003, Journal of bacteriology.

[39]  Steven J. M. Jones,et al.  IslandPath: aiding detection of genomic islands in prokaryotes , 2003, Bioinform..

[40]  J. R. van der Meer,et al.  Characterization of two alternative promoters for integrase expression in the clc genomic island of Pseudomonas sp. strain B13 , 2003, Molecular microbiology.

[41]  Iñigo Lasa,et al.  Sip, an integrase protein with excision, circularization and integration activities, defines a new family of mobile Staphylococcus aureus pathogenicity islands , 2003, Molecular microbiology.

[42]  Yoshiyuki Sakaki,et al.  Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis , 2003, Nature Biotechnology.

[43]  J. F. Tsai,et al.  Isolation and characterization of Streptomyces lividans mutants deficient in intraplasmid recombination , 1987, Molecular and General Genetics MGG.

[44]  Jerald S. Feitelson,et al.  Cloning of a Streptomyces gene for an O-methyltransferase involved in antibiotic biosynthesis , 2004, Molecular and General Genetics MGG.

[45]  K. Otsuki,et al.  Pulsed-field gel electrophoresis-based subtyping of DNA degradation-sensitive Salmonella enterica subsp. enterica serovar Livingstone and serovar Cerro isolates obtained from a chicken layer farm. , 2004, Veterinary microbiology.

[46]  Ulrich Dobrindt,et al.  Genomic islands in pathogenic and environmental microorganisms , 2004, Nature Reviews Microbiology.

[47]  Kelly P. Williams,et al.  Islander: a database of integrative islands in prokaryotic genomes, the associated integrases and their DNA site specificities , 2004, Nucleic Acids Res..

[48]  Sudhir Kumar,et al.  MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment , 2004, Briefings Bioinform..

[49]  Zixin Deng,et al.  Streptomyces coelicolor A3(2) Lacks a Genomic Island Present in the Chromosome of Streptomyces lividans 66 , 2004, Applied and Environmental Microbiology.

[50]  J. Heesemann,et al.  A novel integrative and conjugative element (ICE) of Escherichia coli: the putative progenitor of the Yersinia high‐pathogenicity island , 2003, Molecular microbiology.

[51]  D. Hui,et al.  Evidence for a Symbiosis Island Involved in Horizontal Acquisition of Pederin Biosynthetic Capabilities by the Bacterial Symbiont of Paederus fuscipes Beetles , 2004, Journal of bacteriology.

[52]  C. Thompson,et al.  pIJ101, a multi-copy broad host-range Streptomyces plasmid: Functional analysis and development of DNA cloning vectors , 2004, Molecular and General Genetics MGG.

[53]  Zixin Deng,et al.  A novel DNA modification by sulphur , 2005, Molecular microbiology.

[54]  M. Mulvey,et al.  The Salmonella genomic island 1 is an integrative mobilizable element , 2005, Molecular microbiology.

[55]  Haeyoung Jeong,et al.  Genomic blueprint of Hahella chejuensis, a marine microbe producing an algicidal agent , 2005, Nucleic acids research.

[56]  Kumar Rajakumar,et al.  ArrayOme: a program for estimating the sizes of microarray-visualized bacterial genomes , 2005, Nucleic acids research.

[57]  A. Danchin,et al.  Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. , 2005, Genome research.

[58]  Antoine H. C. van Kampen,et al.  delta rho-Web, an online tool to assess composition similarity of individual nucleic acid sequences , 2005, Bioinform..

[59]  Johan A. Kers,et al.  A large, mobile pathogenicity island confers plant pathogenicity on Streptomyces species , 2004, Molecular microbiology.

[60]  C. Ronson,et al.  Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS , 2006, Molecular microbiology.

[61]  V. Barbe,et al.  Evolution of the terminal regions of the Streptomyces linear chromosome. , 2006, Molecular biology and evolution.

[62]  Ulrich Dobrindt,et al.  Role of pathogenicity island‐associated integrases in the genome plasticity of uropathogenic Escherichia coli strain 536 , 2006, Molecular microbiology.

[63]  Robert D. Finn,et al.  Pfam: clans, web tools and services , 2005, Nucleic Acids Res..

[64]  Kumar Rajakumar,et al.  A novel strategy for the identification of genomic islands by comparative analysis of the contents and contexts of tRNA sites in closely related bacteria , 2006, Nucleic acids research.

[65]  Pierre Brézellec,et al.  DomainSieve: a protein domain-based screen that led to the identification of dam-associated genes with potential link to DNA maintenance , 2006, Bioinform..

[66]  S. Lory,et al.  Acquisition and Evolution of the exoU Locus in Pseudomonas aeruginosa , 2006, Journal of bacteriology.

[67]  D. Hopwood,et al.  Streptomyces in nature and medicine : the antibiotic makers , 2007 .

[68]  Stephen Lory,et al.  MobilomeFINDER: web-based tools for in silico and experimental discovery of bacterial genomic islands , 2007, Nucleic Acids Res..

[69]  L. Black,et al.  A type IV modification dependent restriction nuclease that targets glucosylated hydroxymethyl cytosine modified DNAs. , 2007, Journal of molecular biology.

[70]  Z. Deng,et al.  A novel DNA modification by sulfur: DndA is a NifS-like cysteine desulfurase capable of assembling DndC as an iron-sulfur cluster protein in Streptomyces lividans. , 2007, Biochemistry.

[71]  Z. Deng,et al.  DNA modification by sulfur: analysis of the sequence recognition specificity surrounding the modification sites , 2007, Nucleic acids research.

[72]  Z. Deng,et al.  A genetic and bioinformatic analysis of Streptomyces coelicolor genes containing TTA codons, possible targets for regulation by a developmentally significant tRNA. , 2007, FEMS microbiology letters.