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Detection of Eubacterial 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductases from Natural Populations of Actinomycetes

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Abstract

Three natural populations of actinomycetes were investigated by PCR for the presence of type I 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMG CoA), a gene associated with isoprenoid biosynthesis. The populations were obtained from an agricultural site (69 isolates), a coastal salt marsh (220 isolates), and a desert soil (96 isolates). A set (34) of standard actinomycete reference strains were also investigated. The target gene was only detected in 5 of the 419 actinomycetes screened, which represented 4 from the coastal salt marsh and one reference strain. The isolates that contained the gene were taxonomically diverse (4 Streptomyces spp. and 1 Nocardia sp.). These results suggest that type I HMG CoA containing pathways are rare in actinomycetes and their distribution within actinomycetes populations is not random.

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References

  1. SF Altschul W Gish E Miller W Myers DJ Lipman (1990) ArticleTitleBasic local alignment search tool. J Mol Biol 215 403–410 Occurrence Handle10.1006/jmbi.1990.9999 Occurrence Handle1:CAS:528:DyaK3MXitVGmsA%3D%3D Occurrence Handle2231712

    Article  CAS  PubMed  Google Scholar 

  2. Anderson AS, Clark DJ, Gagliardi M, Gibbons P, Monaghan R, Zink D (1999) Detection and analysis of macrocyclic compounds. In: Abstracts from the 11th International Symposium on the Biology of Actinomycetes, Crete, Greece, 1999

  3. SD Bentley KF Chater AM Cerdeno-Tarraga GL Challis NR Thomson KD James DE Harris MA Quail H Kieser D Harper A Bateman S Brown G Chandra CW Chen M Collins A Cronin A Fraser A Goble J Hidalgo T Hornsby S Howarth CH Huang T Kieser L Larke L Murphy K Oliver S O’Neil E Rabbinowitsch MA Rajandream K Rutherford S Rutter K Seeger D Saunders S Sharp R Squares S Squares K Taylor T Warren A Wietzorrek J Woodward BG Barrell J Parkhill DA Hopwood (2002) ArticleTitleComplete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417 141–147 Occurrence Handle12000953

    PubMed  Google Scholar 

  4. Y Boucher WF Doolittle (2001) ArticleTitleThe role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Mol Microbiol 37 703–716

    Google Scholar 

  5. DE Cane (1995) Isoprenoid antibiotics. LC Vining C Stuttard (Eds) Genetics and Biochemistry of Antibiotic Production. Butterworth-Heinemann 633–655

    Google Scholar 

  6. T Dairi Y Motohira T Kuzuyama S Takahashi N Itoh H Seto (2000) ArticleTitleCloning of the gene encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase from terpenoid antibiotic-producing Streptomyces strains. Mol Gen Genet 262 957–964 Occurrence Handle1:CAS:528:DC%2BD3cXhtlSisbk%3D Occurrence Handle10660057

    CAS  PubMed  Google Scholar 

  7. S Egan P Weiner D Kallifidas EMH Wellington (2001) ArticleTitlePhylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters. Antonie Van Leeuwenhoek 79 127–133 Occurrence Handle1:CAS:528:DC%2BD3MXmslWkt7w%3D Occurrence Handle11519998

    CAS  PubMed  Google Scholar 

  8. J Felenstein (1981) ArticleTitleEvolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17 368–376 Occurrence Handle1:CAS:528:DyaL3MXls1Cisr8%3D Occurrence Handle7288891

    CAS  PubMed  Google Scholar 

  9. JL Goldstein MS Brown (1990) ArticleTitleRegulation of the mevalonate pathway. Nature 343 425–430 Occurrence Handle1:CAS:528:DyaK3cXhtlCmtbw%3D Occurrence Handle1967820

    CAS  PubMed  Google Scholar 

  10. M Goodfellow AG O’Donnell (1985) Search and discovery of industrially significant actinomycetes. S Baumberg (Eds) Microbial Products: New Approaches. Cambridge University Press Cambridge, UK 343–383

    Google Scholar 

  11. Y Hamano T Dairi M Yamamoto T Kawasaki K Kaneda T Kuzuyama N Itoh H Seto (2001) ArticleTitleCloning of a gene cluster encoding enzymes responsible for the mevalonate pathway from a terpenoid-antibiotic-producing Streptomyces strain. Biosci Biotechnol Biochem 65 1627–1635 Occurrence Handle1:CAS:528:DC%2BD3MXlvVSmtrs%3D Occurrence Handle11515548

    CAS  PubMed  Google Scholar 

  12. DA Hopwood MJ Bibb KF Chater T Kieser CJ Bruton HM Kieser DJ Lydicate CP Smith JM Ward H Schrempf (1985) Genetic Manipulation of Streptomyces, a Laboratory Manual, 1st ed, vol 1. The John Innes Foundation Norwich, UK

    Google Scholar 

  13. TA Huck N Porter ME Bushell (1991) ArticleTitlePositive selection of antibiotic-producing soil isolates. J Gen Microbiol 137 2321–2329 Occurrence Handle1:CAS:528:DyaK3MXmsFajsL8%3D Occurrence Handle1770349

    CAS  PubMed  Google Scholar 

  14. AS Huddleston N Cresswell MC Neves JE Beringer S Baumberg DI Thomas EMH Wellington (1997) ArticleTitleMolecular detection of streptomycin-producing streptomycetes in Brazilian soils. Appl Environ Microbiol 63 1288–1297 Occurrence Handle1:CAS:528:DyaK2sXisVSqsro%3D Occurrence Handle9097426

    CAS  PubMed  Google Scholar 

  15. ES Istvan (2001) ArticleTitleBacterial and mammalian HMG-CoA reductases: related enzymes with distinct architectures. Curr Opin Struct Biol 11 746–751 Occurrence Handle1:CAS:528:DC%2BD3MXpt1aqsLo%3D Occurrence Handle11751057

    CAS  PubMed  Google Scholar 

  16. K Komiyama S Funayama Y Anraku M Ishibashi Y Takahashi S Omura (1990) ArticleTitleNovel antibiotics, furaquinocins A and B. Taxonomy, fermentation, isolation and physico-chemical and biological characteristics. J Antibiotics 43 247–252 Occurrence Handle1:CAS:528:DyaK3cXktVejsbo%3D

    CAS  Google Scholar 

  17. M Krsek N Morris S Egan EMH Wellington (2000) Actinomycetes. L Lederberg (Eds) Encyclopedia of Microbiology, vol 1. Academic Press New York 28–41

    Google Scholar 

  18. BM Lange T Rujan W Martin R Croteau (2000) ArticleTitleIsoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci 97 13172–13177 Occurrence Handle1:CAS:528:DC%2BD3cXosVKqur0%3D Occurrence Handle11078528

    CAS  PubMed  Google Scholar 

  19. BM Lange MR Wildung D McCaskill R Croteau (1998) ArticleTitleA family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc Natl Acad Sci 95 2100–2104 Occurrence Handle10.1073/pnas.95.5.2100 Occurrence Handle1:CAS:528:DyaK1cXhslejtbo%3D Occurrence Handle9482845

    Article  CAS  PubMed  Google Scholar 

  20. SM Li S Hennig L Heide (1998) ArticleTitleBiosynthesis of the dimethylallyl moiety of novobiocin via a non-mevalonate pathway. Tetrahedron Letts 39 2717–2720 Occurrence Handle1:CAS:528:DyaK1cXivVeitb8%3D

    CAS  Google Scholar 

  21. S Omura H Ikrda J Ishikawa A Hanamoto C Takahashi M Shinose Y Takahashi H Horokawa H Nakazawa T Osonoe H Kikuchi T Shiba Y Sakaki M Hattori (2001) ArticleTitleGenome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci 98 12215–12220 Occurrence Handle1:CAS:528:DC%2BD3MXns1Cjtrk%3D Occurrence Handle11572948

    CAS  PubMed  Google Scholar 

  22. M Otoguro M Hayakawa T Yamazaki Y Iimura (2001) ArticleTitleAn integrated method for the enrichment and selective isolation of Actinokineospora spp. in soil and plant litter. J Appl Microbiol 91 118–130 Occurrence Handle1:CAS:528:DC%2BD3MXlslaltLs%3D Occurrence Handle11442721

    CAS  PubMed  Google Scholar 

  23. L Phillips EMH Wellington SB Rees (1994) ArticleTitleThe distribution of antibiotic resistance patterns within streptomycetes and their use in secondary metabolite screening. J Ind Microbiol 13 53–62 Occurrence Handle1:CAS:528:DyaK2cXjtF2iu7g%3D

    CAS  Google Scholar 

  24. K Poralla G Muth T Hartner (2000) ArticleTitleHopanoids are formed during transition from substrate to aerial hyphae in Streptomyces coelicolor A3(2). FEMS Microbiol Lett 189 93–95 Occurrence Handle1:CAS:528:DC%2BD3cXltVOmu7s%3D Occurrence Handle10913872

    CAS  PubMed  Google Scholar 

  25. CEG Scholler H Gurtler R Pedersen S Molin K Wilkins (2002) ArticleTitleVolatile metabolites from actinomycetes. J Agric Food Chem 50 2615–2621 Occurrence Handle11958631

    PubMed  Google Scholar 

  26. H Seto H Watanabe K Furihata (1996) ArticleTitleSimultaneous operation of the mevalonate and non-mevalonate pathways in the biosynthesis of isopentenyl diphosphate in Streptomyces aeriouvifer. Tetrahedron Lett 44 7979–7982

    Google Scholar 

  27. K Shin-ya S Imai K Furihata Y Hayakawa Y Kato GD Vanduyne J Clardy H Seto (1990) ArticleTitleIsolation and structural elucidation of an antioxidative agent, naphterpin. J Antibiotics 43 444–447 Occurrence Handle1:CAS:528:DyaK3cXkslCgu7Y%3D

    CAS  Google Scholar 

  28. K Shiomi H Nakamura H Iinuma H Naganawa K Isshiki T Takeuchi H Umezawa Y Iitaka (1986) ArticleTitleStructures of new antibiotics napyradiomycins. J Antibiotics 39 494–501 Occurrence Handle1:CAS:528:DyaL28Xmt1Kisb4%3D

    CAS  Google Scholar 

  29. E Stackebrandt FA Rainey NL Ward-Rainey (1997) ArticleTitleProposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol 41 479–491

    Google Scholar 

  30. WR Strohl (1997) Industrial antibiotics: Today and the future. WR Strohl (Eds) Biotechnology of Antibiotics. Marcel Dekker New York 1–48

    Google Scholar 

  31. S Takahashi T Kuzuyama H Seto (1999) ArticleTitlePurification, characterization, and cloning of a eubacterial 3-hydroxy-3-methylglutaryl coenzyme A reductase, a key enzyme involved in biosynthesis of terpenoids. J Bacteriol 181 1256–1263 Occurrence Handle1:CAS:528:DyaK1MXhsV2qs7w%3D Occurrence Handle9973353

    CAS  PubMed  Google Scholar 

  32. JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673–4680 Occurrence Handle7984417

    PubMed  Google Scholar 

  33. EMH Wellington IK Toth (1993) Actinomycetes. Methods of soil analysis, Part 2. Chemical and Microbiological Properties—Agronomy Monograph no. 9, 3rd ed, ASA-SSA book series no 5 269–290

    Google Scholar 

  34. P Wiener S Egan AS Huddleston EMH Wellington (1998) ArticleTitleEvidence for transfer of antibiotic-resistance genes in soil populations of streptomycetes. Mol Ecol 7 1205–1216 Occurrence Handle1:CAS:528:DyaK1cXmtFOisb0%3D Occurrence Handle9734076

    CAS  PubMed  Google Scholar 

  35. EI Wilding JR Brown AP Bryant AF Chalker DJ Holmes KA Ingraham S Iordanescu CY So M Rosenberg MN Gwynn (2000) ArticleTitleIdentification, evolution, and essentiality of the mevalonate pathway for isopentenyl diphosphate biosynthesis in gram-positive cocci. J Bacteriol 182 4319–4327 Occurrence Handle1:CAS:528:DC%2BD3cXlt1Sgs7c%3D Occurrence Handle10894743

    CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to William Strohl and Jan Tkacz for insightful advice throughout this work and John Barrett, Maria Losada, and Jennifer Nielson-Kahn for their helpful comments on this manuscript.

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Authors and Affiliations

  1. Merck Research Laboratories, P.O. Box 2000, RY80Y-235, Rahway, NJ 07065, USA

    J. M. Sigmund, D. C. Clark & A. S. Anderson

  2. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA

    F. A. Rainey

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  1. J. M. Sigmund
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  2. D. C. Clark
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  3. F. A. Rainey
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  4. A. S. Anderson
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Correspondence to A. S. Anderson.

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Sigmund, J., Clark, D., Rainey, F. et al. Detection of Eubacterial 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductases from Natural Populations of Actinomycetes . Microb Ecol 46, 106–112 (2003). https://doi.org/10.1007/s00248-002-2029-5

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