Identification and heterologous expression of the chaxamycin biosynthesis gene cluster from Streptomyces leeuwenhoekii

Applied and Environmental Microbiology

Volumn 81, Issue 17, 2015, Pages 5820-5831

  Castro, Jean Franco ^a,b   Razmilic, Valeria ^a,b   Gomez Escribano, Juan Pablo ^b   Andrews, Barbara ^a   Asenjo, Juan A ^a   Bibb, Mervyn J ^b  

^a UNIVERSITY OF CHILE   (Chile)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOCHEMISTRY; BIOSYNTHESIS; GENES;

ANTI-BACTERIAL ACTIVITY; ANTI-PROLIFERATIVE ACTIVITIES; ATACAMA DESERT; BIOSYNTHESIS GENE CLUSTER; HETEROLOGOUS EXPRESSION; MUTATIONAL ANALYSIS; PARTIAL CHARACTERIZATION; STREPTOMYCES COELICOLOR A3(2);

GENE EXPRESSION;

ANTIMICROBIAL ACTIVITY; BACTERIUM; ENZYME ACTIVITY; GENE EXPRESSION; IDENTIFICATION METHOD; MUTATION;

ATACAMA DESERT; CHILE;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CHAXAMYCIN A; CHAXAMYCIN D; RIFAMYCIN;

BIOSYNTHESIS; CHEMISTRY; GENETICS; METABOLISM; MULTIGENE FAMILY; STREPTOMYCES; STREPTOMYCES COELICOLOR;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOSYNTHETIC PATHWAYS; MULTIGENE FAMILY; RIFAMYCINS; STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 84938812406     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01039-15     Document Type: Article

References (72)

1. Davies SC. 2013. Annual report of the Chief Medical Officer, vol 2, 2011, Infections and the rise of antimicrobial resistance. Department of Health, London, United Kingdom.
2. Centers for Disease Control and Prevention. 2013. Antimicrobial resistance threats in the United States, 2013. Centers for Disease Control and Prevention, Atlanta, GA.
3. World Health Organization. 2014. Antimicrobial resistance: global report on surveillance. World Health Organization, Geneva, Switzerland.
4. Baltz RH. 2008. Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8:557-563. http://dx.doi.org/10.1016/j.coph.2008.04.008.
5. Shoichet BK. 2013. Drug discovery: nature's pieces. Nat Chem 5:9-10. http://dx.doi.org/10.1038/nchem.1537.
6. Wright GD. 2014. Something old, something new: revisiting natural products in antibiotic drug discovery. Can J Microbiol 60:147-154. http://dx.doi.org/10.1139/cjm-2014-0063.
7. Okoro CK, Brown R, Jones AL, Andrews BA, Asenjo JA, Goodfellow M, Bull AT. 2009. Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert, Chile. Antonie Van Leeuwenhoek 95:121-133. http://dx.doi.org/10.1007/s10482-008-9295-2.
8. Bull AT, Asenjo JA. 2013. Microbiology of hyper-arid environments: recent insights from the Atacama Desert, Chile. Antonie Van Leeuwenhoek 103:1173-1179. http://dx.doi.org/10.1007/s10482-013-9911-7.
9. Rateb ME, Houssen WE, Arnold M, Abdelrahman MH, Deng H, Harrison WTA, Okoro CK, Asenjo JA, Andrews BA, Ferguson G, Bull AT, Goodfellow M, Ebel R, Jaspars M. 2011. Chaxamycins A-D, bioactive ansamycins from a hyper-arid desert Streptomyces sp. J Nat Prod 74:1491-1499. http://dx.doi.org/10.1021/np200320u.
10. Rateb ME, Houssen WE, Harrison WTA, Deng H, Okoro CK, Asenjo JA, Andrews BA, Bull AT, Goodfellow M, Ebel R, Jaspars M. 2011. Diverse metabolic profiles of a Streptomyces strain isolated from a hyperarid environment. J Nat Prod 74:1965-1971. http://dx.doi.org/10.1021/np200470u.
11. Nachtigall J, Kulik A, Helaly S, Bull AT, Goodfellow M, Asenjo JA, Maier A, Wiese J, Imhoff JF, Süssmuth RD, Fiedler H-P. 2011. Atacamycins A-C, 22-membered antitumor macrolactones produced by Streptomyces sp. C38. J Antibiot 64:775-780. http://dx.doi.org/10.1038/ja.2011.96.
12. Busarakam K, Bull AT, Girard G, Labeda DP, van Wezel GP, Goodfellow M. 2014. Streptomyces leeuwenhoekii sp. nov., the producer of chaxalactins and chaxamycins, forms a distinct branch in Streptomyces gene trees. Antonie Van Leeuwenhoek 105:849-861. http://dx.doi.org/10.1007/s10482-014-0139-y.
13. Kang Q, Shen Y, Bai L. 2012. Biosynthesis of 3,5-AHBA-derived natural products. Nat Prod Rep 29:243-263. http://dx.doi.org/10.1039/C2NP00019A.
14. 7N units in ansamycin and mitomycin antibiotics: a review. J Antibiot 64:35-44. http://dx.doi.org/10.1038/ja.2010.139.
15. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
16. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, United Kingdom.
17. Jones AC, Gust B, Kulik A, Heide L, Buttner MJ, Bibb MJ. 2013. Phage P1-derived artificial chromosomes facilitate heterologous expression of the FK506 gene cluster. PLoS One 8:e69319. http://dx.doi.org/10.1371/journal.pone.0069319.
18. Shima J, Hesketh A, Okamoto S, Kawamoto S, Ochi K. 1996. Induction of actinorhodin production by rpsL (encoding ribosomal protein S12) mutations that confer streptomycin resistance in Streptomyces lividans and Streptomyces coelicolor A3(2). J Bacteriol 178:7276-7284.
19. Gomez-Escribano JP, Castro JF, Razmilic V, Chandra G, Andrews B, Asenjo JA, Bibb MJ. 2015. The Streptomyces leeuwenhoekii genome: de novo sequencing and assembly in single contigs of the chromosome, circular plasmid pSLE1 and linear plasmid pSLE2. BMC Genomics 16:485. http://dx.doi.org/10.1186/s12864-015-1652-8.
20. Staden R, Beal KF, Bonfield JK. 1999. The Staden package, 1998, p 115-130. In Misener S, Krawetz SA (ed), Bioinformatics methods and protocols. Humana Press, New York, NY.
21. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389.
22. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. http://dx.doi.org/10.1186/1471-2105-10-421.
23. Priyam A, Woodcroft BJ, Rai V, Wurm Y. 2011. SequenceServer: BLAST search made easy. http://sequenceserver.com. Accessed 11 June 2015.
24. Santiago-Sotelo P, Ramirez-Prado JH. 2012. prfectBLAST: a platformindependent portable front end for the command terminal BLAST+ stand-alone suite. Biotechniques 53:299-300. http://dx.doi.org/10.2144/000113953.
25. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71-W74. http://dx.doi.org/10.1093/nar/gkm306.
26. Ichikawa N, Sasagawa M, Yamamoto M, Komaki H, Yoshida Y, Yamazaki S, Fujita N. 2013. DoBISCUIT: a database of secondary metabolite biosynthetic gene clusters. Nucleic Acids Res 41:D408-D414. http://dx.doi.org/10.1093/nar/gks1177.
27. Sosio M, Giusino F, Cappellano C, Bossi E, Puglia AM, Donadio S. 2000. Artificial chromosomes for antibiotic-producing actinomycetes. Nat Biotechnol 18:343-345. http://dx.doi.org/10.1038/73810.
28. Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26:589-595. http://dx.doi.org/10.1093/bioinformatics/btp698.
29. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/btp352.
30. Bonfield JK, Whitwham A. 2010. Gap5-editing the billion fragment sequence assembly. Bioinformatics 26:1699-1703. http://dx.doi.org/10.1093/bioinformatics/btq268.
31. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. http://dx.doi.org/10.1186/1471-2105-11-119.
32. Van Domselaar GH, Stothard P, Shrivastava S, Cruz JA, Guo A, Dong X, Lu P, Szafron D, Greiner R, Wishart DS. 2005. BASys: a web server for automated bacterial genome annotation. Nucleic Acids Res 33:W455-W459. http://dx.doi.org/10.1093/nar/gki593.
33. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945. http://dx.doi.org/10.1093/bioinformatics/16.10.944.
34. Bibb MJ, Findlay PR, Johnson MW. 1984. The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of protein-coding sequences. Gene 30:157-166. http://dx.doi.org/10.1016/0378-1119(84)90116-1.
35. Rausch H, Lehmann M. 1991. Structural analysis of the actinophage phi C31 attachment site. Nucleic Acids Res 19:5187-5189. http://dx.doi.org/10.1093/nar/19.19.5187.
36. Gregory MA, Till R, Smith MCM. 2003. Integration site for Streptomyces phage phiBT1 and development of site-specific integrating vectors. J Bacteriol 185:5320-5323. http://dx.doi.org/10.1128/JB.185.17.5320-5323.2003.
37. Bibb MJ, White J, Ward JM, Janssen GR. 1994. The mRNA for the 23S rRNA methylase encoded by the ermE gene of Saccharopolyspora erythraea is translated in the absence of a conventional ribosome-binding site. Mol Microbiol 14:533-545. http://dx.doi.org/10.1111/j.1365-2958.1994.tb02187.x.
38. Myronovskyi M, Welle E, Fedorenko V, Luzhetskyy A. 2011. Beta-glucuronidase as a sensitive and versatile reporter in actinomycetes. Appl Environ Microbiol 77:5370-5383. http://dx.doi.org/10.1128/AEM.00434-11.
39. Sherwood EJ, Bibb MJ. 2013. The antibiotic planosporicin coordinates its own production in the actinomycete Planomonospora alba. Proc Natl Acad Sci U S A 110:E2500-E2509. http://dx.doi.org/10.1073/pnas.1305392110.
40. Muth G, Nußbaumer B, Wohlleben W, Pühler A. 1989. A vector system with temperature-sensitive replication for gene disruption and mutational cloning in streptomycetes. Mol Gen Genet 219:341-348. http://dx.doi.org/10.1007/BF00259605.
41. Seipke RF, Loria R. 2009. Hopanoids are not essential for growth of Streptomyces scabies 87-22. J Bacteriol 191:5216-5223. http://dx.doi.org/10.1128/JB.00390-09.
42. Poralla K, Muth G, Hartner T. 2000. Hopanoids are formed during transition from substrate to aerial hyphae in Streptomyces coelicolor A3(2). FEMS Microbiol Lett 189:93-95. http://dx.doi.org/10.1111/j.1574-6968.2000.tb09212.x.
43. Yu TW, Müller R, Müller M, Zhang X, Draeger G, Kim CG, Leistner E, Floss HG. 2001. Mutational analysis and reconstituted expression of the biosynthetic genes involved in the formation of 3-amino-5-hydroxybenzoic acid, the starter unit of rifamycin biosynthesis in Amycolatopsis mediterranei S699. J Biol Chem 276:12546-12555. http://dx.doi.org/10.1074/jbc.M009667200.
44. Wilson MC, Gulder TAM, Mahmud T, Moore BS. 2010. Shared biosynthesis of the saliniketals and rifamycins in Salinispora arenicola is controlled by the sare1259-encoded cytochrome P450. J Am Chem Soc 132:12757-12765. http://dx.doi.org/10.1021/ja105891a.
45. Yuan H, Zhao W, Zhong Y, Wang J, Qin Z, Ding X, Zhao G-P. 2011. Two genes, rif15 and rif16, of the rifamycin biosynthetic gene cluster in Amycolatopsis mediterranei likely encode a transketolase and a P450 monooxygenase, respectively, both essential for the conversion of rifamycin SV into B. Acta Biochim Biophys Sin (Shanghai) 43:948-956. http://dx.doi.org/10.1093/abbs/gmr091.
46. August PR, Tang L, Yoon YJ, Ning S, Müller R, Yu TW, Taylor M, Hoffmann D, Kim CG, Zhang X, Hutchinson CR, Floss HG. 1998. Biosynthesis of the ansamycin antibiotic rifamycin: deductions from the molecular analysis of the rif biosynthetic gene cluster of Amycolatopsis mediterranei S699. Chem Biol 5:69-79. http://dx.doi.org/10.1016/S1074-5521(98)90141-7.
47. Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T. 2013. antiSMASH 2.0-a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res 41:W204-W212. http://dx.doi.org/10.1093/nar/gkt449.
48. Minowa Y, Araki M, Kanehisa M. 2007. Comprehensive analysis of distinctive polyketide and nonribosomal peptide structural motifs encoded in microbial genomes. J Mol Biol 368:1500-1517. http://dx.doi.org/10.1016/j.jmb.2007.02.099.
49. Yadav G, Gokhale RS, Mohanty D. 2003. Computational approach for prediction of domain organization and substrate specificity of modular polyketide synthases. J Mol Biol 328:335-363. http://dx.doi.org/10.1016/S0022-2836(03)00232-8.
50. Admiraal SJ, Walsh CT, Khosla C. 2001. The loading module of rifamycin synthetase is an adenylation-thiolation didomain with substrate tolerance for substituted benzoates. Biochemistry 40:6116-6123. http://dx.doi.org/10.1021/bi010080z.
51. Admiraal SJ, Khosla C, Walsh CT. 2002. The loading and initial elongation modules of rifamycin synthetase collaborate to produce mixed aryl ketide products. Biochemistry 41:5313-5324. http://dx.doi.org/10.1021/bi0200312.
52. Bevitt DJ, Cortes J, Haydock SF, Leadlay PF. 1992. 6-Deoxyerythronolide-B synthase 2 from Saccharopolyspora erythraea. Cloning of the structural gene, sequence analysis and inferred domain structure of the multifunctional enzyme. Eur J Biochem 204:39-49.
53. Valenzano CR, You Y-O, Garg A, Keatinge-Clay A, Khosla C, Cane DE. 2010. Stereospecificity of the dehydratase domain of the erythromycin polyketide synthase. J Am Chem Soc 132:14697-14699. http://dx.doi.org/10.1021/ja107344h.
54. Reid R, Piagentini M, Rodriguez E, Ashley G, Viswanathan N, Carney J, Santi DV, Hutchinson CR, McDaniel R. 2003. A model of structure and catalysis for ketoreductase domains in modular polyketide synthases. Biochemistry 42:72-79. http://dx.doi.org/10.1021/bi0268706.
55. Zheng J, Keatinge-Clay AT. 2011. Structural and functional analysis of C2-type ketoreductases from modular polyketide synthases. J Mol Biol 410:105-117. http://dx.doi.org/10.1016/j.jmb.2011.04.065.
56. Yu T-W, Shen Y, Doi-Katayama Y, Tang L, Park C, Moore BS, Hutchinson CR, Floss HG. 1999. Direct evidence that the rifamycin polyketide synthase assembles polyketide chains processively. Proc Natl Acad Sci U S A 96:9051-9056. http://dx.doi.org/10.1073/pnas.96.16.9051.
57. Claxton HB, Akey DL, Silver MK, Admiraal SJ, Smith JL. 2009. Structure and functional analysis of RifR, the type II thioesterase from the rifamycin biosynthetic pathway. J Biol Chem 284:5021-5029. http://dx.doi.org/10.1074/jbc.M808604200.
58. Doi-Katayama Y, Yoon YJ, Choi CY, Yu TW, Floss HG, Hutchinson CR. 2000. Thioesterases and the premature termination of polyketide chain elongation in rifamycin B biosynthesis by Amycolatopsis mediterranei S699. J Antibiot 53:484-495. http://dx.doi.org/10.7164/antibiotics.53.484.
59. Xu J, Wan E, Kim C-J, Floss HG, Mahmud T. 2005. Identification of tailoring genes involved in the modification of the polyketide backbone of rifamycin B by Amycolatopsis mediterranei S699. Microbiology 151:2515-2528. http://dx.doi.org/10.1099/mic.0.28138-0.
60. Xiong Y, Wu X, Mahmud T. 2005. A homologue of the Mycobacterium tuberculosis PapA5 protein, Rif-Orf20, is an acetyltransferase involved in the biosynthesis of antitubercular drug rifamycin B by Amycolatopsis mediterranei S699. Chembiochem 6:834-837. http://dx.doi.org/10.1002/cbic.200400387.
61. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M. 2014. Pfam: the protein families database. Nucleic Acids Res 42:D222-D230. http://dx.doi.org/10.1093/nar/gkt1223.
62. Galperin MY. 2010. Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13:150-159. http://dx.doi.org/10.1016/j.mib.2010.01.005.
63. Absalón AE, Fernández FJ, Olivares PX, Barrios-González J, Campos C, Mejía A. 2007. RifP; a membrane protein involved in rifamycin export in Amycolatopsis mediterranei. Biotechnol Lett 29:951-958. http://dx.doi.org/10.1007/s10529-007-9340-7.
64. Floss HG, Yu T-W. 2005. Rifamycin-mode of action, resistance, and biosynthesis. Chem Rev 105:621-632. http://dx.doi.org/10.1021/cr030112j.
65. Grant SG, Jessee J, Bloom FR, Hanahan D. 1990. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylationrestriction mutants. Proc Natl Acad SciUSA 87:4645-4649. http://dx.doi.org/10.1073/pnas.87.12.4645.
66. MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH, MacNeil T. 1992. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111:61-68. http://dx.doi.org/10.1016/0378-1119(92)90603-M.
67. Gomez-Escribano JP, Bibb MJ. 2011. Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters. Microb Biotechnol 4:207-215. http://dx.doi.org/10.1111/j.1751-7915.2010.00219.x.
68. Alting-Mees MA, Short JM. 1989. pBluescript II: gene mapping vectors. Nucleic Acids Res 17:9494. http://dx.doi.org/10.1093/nar/17.22.9494.
69. Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, Schoner BE. 1992. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43-49. http://dx.doi.org/10.1016/0378-1119(92)90627-2.
70. Rodríguez-García A, Santamarta I, Pérez-Redondo R, Martín JF, Liras P. 2006. Characterization of a two-gene operon epeRA involved in multidrug resistance in Streptomyces clavuligerus. Res Microbiol 157:559-568. http://dx.doi.org/10.1016/j.resmic.2005.12.008.
71. Hong H-J, Hutchings MI, Hill LM, Buttner MJ. 2005. The role of the novel Fem protein VanK in vancomycin resistance in Streptomyces coelicolor. J Biol Chem 280:13055-13061. http://dx.doi.org/10.1074/jbc.M413801200.
72. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH. 2015. CDD: NCBI's conserved domain database. Nucleic Acids Res 43:D222-D226. http://dx.doi.org/10.1093/nar/gku1221.