Skip to main content
SpringerLink
Log in

Identification of genes necessary for jinggangmycin biosynthesis from Streptomyces hygroscopicus 10-22

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

A series of large chromosomal deletions in Streptomyces hygroscopicus 10-22 were aligned on the physical map of the wild-type strain and the mutants were assessed for their ability to produce the aminocyclitol antibiotic 5102-I (jinggangmycin). Twenty-eight mutants were blocked for jinggangmycin production and all of them were found to lack a 300 kb AseI-F fragment of the wild-type chromosome. An ordered cosmid library of the 300 kb AseI-F fragment was made and one of the cosmids conferred jinggangmycin productivity to Streptomyces lividans ZX1. Three of the overlapping cosmids (18G7, 5H3 and 9A2) also hybridized to the valA gene of the validamycin pathway from S. hygroscopicus 5008 as a probe. This gene resembles acbC from Actinoplanes sp. 50/110, which encodes a C7-cyclitol synthase that catalyses the transformation of sedoheptulose 7-phosphate into 2-5-epi-valiolone for acarbose biosynthesis. The valA/acbC-homolog (orf1) of S. hygroscopicus 10-22 was shown to be essential for jinggangmycin biosynthesis as an engineered mutant with a specific in-frame deletion removing a 609 bp sequence internal to orf1 completely abolished jinggangmycin production and the corresponding knock-out mutant (JXH4) could be complemented for jinggangmycin production by the introduction of an orf1-containing construct. Concurrently, the identities of the genes common to S. hygroscopicus strains 10-22 and 5008 prompted a comparison of the chemical structures of jinggangmycin and validamycin, which led to a clear demonstration that they are identical.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

PFGE:

pulsed-field gel electrophoresis

HPLC:

high performance liquid chromatography

References

  • Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. (1990). Basic local alignement search tool. J. Mol. Biol. 5:403–410

    Google Scholar 

  • Bao K., Cohen S.N. (2001). Terminal proteins essential for the replication of linear plasmids and chromosomes in Streptomyces. Genes. Dev. 15(12):1518–1527

    Article  PubMed  CAS  Google Scholar 

  • Bentley S.D., Chater K.F., Cerdeno-Tarraga A.M., Challis G.L., Thomson N.R., James K.D., Harris D.E., Quail M.A., Kieser H., Harper D., Bateman A., Brown S., Chandra G., Chen C.W., Collins M., Cronin A., Fraser A., Goble A., Hidalgo J., Hornsby T., Howarth S., Huang C.H., Kieser T., Larke L., Murphy L., Oliver K., O’Neil S., Rabbinowitsch E., Rajandream M.A., Rutherford K., Rutter S., Seeger K., Saunders D., Sharp S., Squares R., Squares S., Taylor K., Warren T., Wietzorrek A., Woodward J., Barrell B.G., Parkhill J., Hopwood D.A. (2002). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417(6885):141–147

    Article  PubMed  Google Scholar 

  • Bierman M., Logan R., O’Brien K., Seno E.T., Rao R.N., Schoner B.E. (1992). Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116(1):43–49

    Article  PubMed  CAS  Google Scholar 

  • Birch A., Husler A., Vutli M., Krek W., Huter R. (1989). Extremely large chromosomal deletions are intimately involved in genetic instability and genomic rearrangements in Streptomyces glaucescens. Mol.Gen. Genet. 217:447–458

    Article  PubMed  CAS  Google Scholar 

  • Chater K.F. (1993). Genetics of differentiation in Streptomyces. Annu. Rev. Microbiol. 47:685–713

    Article  PubMed  CAS  Google Scholar 

  • Chen C.W., Yu T.W., Lin Y.-S., Kieser H.M., Hopwood D.A. (1993). The conjugative plasmid SLP2 of Streptomyces lividans is a 50 kb linear molecule. Mol. Microbiol. 7:925–932

    Article  PubMed  CAS  Google Scholar 

  • Fischer G., Decaris B., Leblond P. (1997). Occurrence of deletions associated with genetic instability in Streptomyces ambofaciens, is independent of the linearity of the chromosomal DNA. J. Bacteriol. 179:4553–4558

    PubMed  CAS  Google Scholar 

  • Flett F., Platt J., Cullum J. (1987). DNA rearrangements associated with instability of an arginine gene in Streptomyces coelicolor A(3)2. J. Basic Microbiol. 27:3–10

    Article  PubMed  CAS  Google Scholar 

  • Gravius B., Bezmalinovic T., Hranueli D., Cullum J. (1993). Genetic instability and strain degeneration in Streptomyces rimosus. Appl. Environ. Microbiol. 59(7):2220–2228

    PubMed  CAS  Google Scholar 

  • Hopwood D.A., Chater K.F., Bibb M.J. (1995). Genetics of antibiotic production in Streptomyces coelicolor A3(2), a model streptomycete. Biotechnology 28:65–102

    PubMed  CAS  Google Scholar 

  • Hu Z., Bao K., Zhou X., Zhou Q., Hopwood D.A., Kieser T., Deng Z. (1994). Repeated polyketide synthase modules involved in the biosynthesis of a heptaene macrolide byStreptomyces sp. FR-008. Mol. Microbiol. 14(1):163–172

    Article  PubMed  CAS  Google Scholar 

  • Ikeda H., Ishikawa J., Hanamoto A., Shinose M., Kikuchi H., Shiba T., Sakaki Y., Hattori M., Omura S. (2003). Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 14:14

    Google Scholar 

  • Janssen G.R., Bibb M.J. (1993). Derivatives of pUC18 that have BglII sites flanking a modified multiple cloning site and that retain the ability to identify recombinant clones by visual screening of colonies. Gene 124(1):133–134

    Article  PubMed  CAS  Google Scholar 

  • Kieser T., Bibb M.J., Buttner M.J., Chater K.F., Hopwood D.A. (2000). Practical Streptomyces Genetics. John Innes Foundation, Norwich, UK

    Google Scholar 

  • Lezhava A., Kameoka D., Sugino H., Goshi K., Shinkawa H., Nimi O., Horinouchi S., Beppu S., Kinashi H. (1997). Chromosomal deletions in Streptomyces griseus that remove the afsA locus. Mol. Gen. Genet. 253:478–483

    Article  PubMed  CAS  Google Scholar 

  • Liang R.F., Zhou Q. (1991). Blocked mutants of antibiotic 5102-III obtained by acridine orange treatment of S. hygroscopicus 10-22. J. Huahong. Agric. Univ. 10:362–366

    Google Scholar 

  • Lin Y.S., Kieser H.M., Hopwood D.A., Chen C.W. (1993). The chromosomal DNA of Streptomyces lividans 66 is linear. Mol. Microbiol.10:923–933

    Article  PubMed  CAS  Google Scholar 

  • Omura S., Ikeda H., Ishikawa J., Hanamoto A., Takahashi C., Shinose M., Takahashi Y., Horikawa H., Nakazawa H., Osonoe T., Kikuchi H., Shiba T., Sakaki Y., Hattori M. (2001). Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sci. U.S.A. 98(21):12215–12220

    Article  PubMed  CAS  Google Scholar 

  • Paget M.S.B., Chamberlin L., Atrih A., Foster S.J., Buttner M.J. (1999). Evidence that the extracytoplasmic function sigma factor sE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J. Bacteriol. 181:204–211

    PubMed  CAS  Google Scholar 

  • Pandza K., Pfalzer G., Cullum J., Hranueli D. (1997). Physical mapping shows that the unstable oxytetracycline gene cluster of Streptomyces rimosus lies close the ends of the linear chromosome. Microbiology 143:1493–1501

    Article  PubMed  CAS  Google Scholar 

  • Pang X., Aigle B., Girardet J.M., Mangenot S., Pernodet J.L., Decaris B., Leblond P. (2004). Functional angucycline-like antibiotic gene cluster in the terminal inverted repeats of the Streptomyces ambofaciens linear chromosome. Antimicrob. Agents Chemother. 48(2):575–588

    Article  PubMed  CAS  Google Scholar 

  • Pang X., Zhou X., Sun Y., Deng Z. (2002a). Physical map of the linear chromosome of Streptomyces hygroscopicus 10-22 deduced by analysis of overlapping large chromosomal deletions. J. Bacteriol. 184(7):1958–1965

    Article  CAS  Google Scholar 

  • Pang X., Liu J., Zhou X., Deng Z. (2002b). A linear plasmid temperature-sensitive for replication in Streptomyces hygroscopicus 10-22. FEMS Microbiology Letters 208(1):25–28

    Article  CAS  Google Scholar 

  • Qin Z., Peng K., Zhou X., Liang R., Zhou Q., Chen H., Hopwood D.A., Kieser T., Deng Z. (1994). Development of a gene cloning system for Streptomyces hygroscopicus subsp. yingchengensis, a producer of three useful antifungal compounds, by elimination of three barriers to DNA transfer. J. Bacteriol. 176(7):2090–2095

    PubMed  CAS  Google Scholar 

  • Qin Z.J. 1992. The development of vector-host system and genetic manipulation of Streptomyces hygroscopicus 10-22, PhD thesis, Huazhong Agricultural University, Wuhan, People’s Republic of China

  • Sambrook J., Fritsch E.F., Maniatis T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor. New-York, Cold Spring Harbor Laboratory Press

    Google Scholar 

  • Stratmann A., Mahmud T., Lee S., Distler J., Floss H.G., Piepersberg W. (1999). The AcbC protein from Actinoplanes species is a C7-cyclitol synthase related to 3-dehydroquinate synthases and is involved in the biosynthesis of the alpha-glucosidase inhibitor acarbose. J. Biol. Chem. 274(16):10889–10896

    Article  PubMed  CAS  Google Scholar 

  • Sun Y., Zhou X., Liu J., Bao K., Zhang G., Tu G., Kieser T., Deng Z. (2002). ‘Streptomyces nanchangensis’, a producer of the insecticidal polyether antibiotic nanchangmycin and the antiparasitic macrolide meilingmycin, contains multiple polyketide gene clusters. Microbiology 148(Pt 2):361–371

    PubMed  CAS  Google Scholar 

  • Volff J.N., Altenbuchner J. (1998). Genetic instability of the Streptomyces chromosome. Mol. Microbiol. 27(2):239–246

    Article  PubMed  CAS  Google Scholar 

  • Volff J.N., Vandewiele D., Simonet J.M., Decaris B. (1993). Ultraviolet light, mitomycin C and nitrous acid induce genetic instability in Streptomyces ambofaciens ATCC23877. Mutat. Res. 287:141–156

    PubMed  CAS  Google Scholar 

  • Yu Y., Bai L., Minagawa K., Jian J., Li L., Li J., Chen S., Cao E., Mahmud T., Floss H.G., Zhou X., Deng Z. (2005). A gene cluster encoding validamycin biosynthesis in Streptomyces hygroscopicus var. jinggangensis 5008. Appl. Enviro. Microbiol. 71(9):5066–5076

    Article  CAS  Google Scholar 

  • Zhang C.S., Stratmann A., Block O., Bruckner R., Podeschwa M., Altenbach H.J., Wehmeier U.F., Piepersberg W. (2002). Biosynthesis of the C(7)-cyclitol moiety of acarbose in Actinoplanes species SE50/110. 7-O-phosphorylation of the initial cyclitol precursor leads to proposal of a new biosynthetic pathway. J. Biol. Chem. 277(25):22853–22862

    Article  PubMed  CAS  Google Scholar 

  • Zhang S.H., Zhao H.Z., Liu J.L. (1982). Studies on the agricultural antibiotic 5102-III. Isolation and characterization of antibiotic 5102-III. J. Huazhong Agric. College 1:39–43

    Google Scholar 

  • Zhang S.H., Zhao S.Z., Liu J.L. (1981). Studies on the agricultural antibiotic 5102-II. Isolation and characterization of antibiotic 5102-II. Acta Microbiol. Sin 22:145–150

    Google Scholar 

  • Zhou Q., Liu J.L. (1981). Studies on antifungal activities of the agricultural antibiotic 5102. Chin. J. Antibiot. 6:1–6

    Google Scholar 

  • Zhou X., He X., Li A., Lei F., Kieser T., Deng Z. (2004). Streptomyces coelicolor A3(2) lacks a genomic island present in the chromosome of Streptomyces lividans 66. Appl. Environ. Microbiol. 70(12):7110–7118

    Article  PubMed  CAS  Google Scholar 

  • Zhou X., He X., Liang J., Li A., Xu T., Kieser T., Helmann J.D., Deng Z. (2005). A novel DNA modification by sulphur. Mol Microbiol 57(5):1428–1438

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank David A. Hopwood, FRS for valuable comments and critical reading of the manuscript. This work received support from 973 (2003CB114205) and 863 programs of the Ministry of Science and Technology, the National Science Foundation of China, the Ph.D. Training Fund from the Ministry of Education, and the Shanghai Municipal Council of Science and Technology.

Author information

Author notes

  1. Xiaohong Jian

    Present address: Laboratory of Microbial Metabolism and School of Life Science & Biotechnology, Shanghai Jiaotong University, Shanghai, 200030, China

  2. Xiuhua Pang

    Present address: School of Life Science and Technology, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

Authors and Affiliations

  1. Laboratory of Microbial Metabolism and School of Life Science & Biotechnology, Shanghai Jiaotong University, Shanghai, 200030, China

    Xiuhua Pang, Yi Yu, Xiufen Zhou & Zixin Deng

  2. School of Life Science and Technology, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Yi Yu, Xiufen Zhou & Zixin Deng

Authors
  1. Xiaohong Jian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiuhua Pang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yi Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiufen Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zixin Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zixin Deng.

Additional information

The first two authors contributed equally to this study.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jian, X., Pang, X., Yu, Y. et al. Identification of genes necessary for jinggangmycin biosynthesis from Streptomyces hygroscopicus 10-22. Antonie Van Leeuwenhoek 90, 29–39 (2006). https://doi.org/10.1007/s10482-006-9058-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-006-9058-x

Keywords

Search

Navigation