Systems perspectives on erythromycin biosynthesis by comparative genomic and transcriptomic analyses of S. erythraea E3 and NRRL23338 strains

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Li, Yuan Yuan ^a   Chang, Xiao ^a,c,e   Yu, Wen Bang ^b   Li, Hao ^b   Ye, Zhi Qiang ^a,d   Yu, Hui ^a,c   Liu, Bao Hong ^a   Zhang, Yan ^b   Zhang, Si Liang ^b   Ye, Bang Ce ^a,b   Li, Yi Xue ^a,c  

^a SHANGHAI CENTER FOR BIOINFORMATION TECHNOLOGY   (China)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c Chinese Academy of Sciences   (China)

^d PEKING UNIVERSITY   (China)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Erythromycin biosynthesis; Functional comparative genetics; Regulation mechanism; S. erythraea

Indexed keywords

ERYTHROMYCIN;

ANTIBIOTIC BIOSYNTHESIS; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BIOENERGY; COMPARATIVE STUDY; CONTROLLED STUDY; FUNCTIONAL GENOMICS; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; NONHUMAN; SACCHAROPOLYSPORA; STRAIN DIFFERENCE; STREPTOMYCES ERYTHRAEUS; WILD TYPE;

BACTERIA (MICROORGANISMS); POSIBACTERIA;

COMPARATIVE GENOMIC HYBRIDIZATION; ERYTHROMYCIN; GENOME, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE ANNOTATION; SACCHAROPOLYSPORA; TRANSCRIPTOME;

EID: 84880864034     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-523     Document Type: Article

References (65)

1. Oliynyk M, Samborskyy M, Lester JB, Mironenko T, Scott N, et al. Complete genome sequence of the erythromycin-producing bacterium Saccharopolyspora erythraea NRRL23338. Nat Biotechnol 2007, 25:447-453. 10.1038/nbt1297, 17369815.
2. Mironov VA, Sergienko OV, Nastasiak IN, Danilenko VN. Biogenesis and regulation of biosynthesis of erythromycins in Saccharopolyspora erythraea: a review. Prikl Biokhim Mikrobiol 2004, 40:613-624.
3. McDaniel R, Licari P, Khosla C. Process development and metabolic engineering for the overproduction of natural and unnatural polyketides. Adv Biochem Eng Biotechnol 2001, 73:31-52.
4. Leadlay PF. Combinatorial approaches to polyketide biosynthesis. Curr Opin Chem Biol 1997, 1:162-168. 10.1016/S1367-5931(97)80005-1, 9734993.
5. Adrio JL, Demain AL. Genetic improvement of processes yielding microbial products. FEMS Microbiol Rev 2006, 30:187-214. 10.1111/j.1574-6976.2005.00009.x, 16472304.
6. Carata E, Peano C, Tredici SM, Ferrari F, Tala A, et al. Phenotypes and gene expression profiles of Saccharopolyspora erythraea rifampicin-resistant (rif) mutants affected in erythromycin production. Microb Cell Fact 2009, 8:18. 10.1186/1475-2859-8-18, 2667423, 19331655.
7. El-Enshasy HA, Mohamed NA, Farid MA, El-Diwany AI. Improvement of erythromycin production by Saccharopolyspora erythraea in molasses based medium through cultivation medium optimization. Bioresour Technol 2008, 99:4263-4268. 10.1016/j.biortech.2007.08.050, 17936622.
8. Zou X, Hang HF, Chu J, Zhuang YP, Zhang SL. Enhancement of erythromycin A production with feeding available nitrogen sources in erythromycin biosynthesis phase. Bioresour Technol 2009, 100:3358-3365. 10.1016/j.biortech.2009.01.064, 19268575.
9. Donadio S, Staver MJ, McAlpine JB, Swanson SJ, Katz L. Modular organization of genes required for complex polyketide biosynthesis. Science 1991, 252:675-679. 10.1126/science.2024119, 2024119.
10. Weber JM, Leung JO, Maine GT, Potenz RH, Paulus TJ, et al. Organization of a cluster of erythromycin genes in Saccharopolyspora erythraea. J Bacteriol 1990, 172:2372-2383. 208872, 2185216.
11. Reeves AR, English RS, Lampel JS, Post DA, Vanden Boom TJ. Transcriptional organization of the erythromycin biosynthetic gene cluster of Saccharopolyspora erythraea. J Bacteriol 1999, 181:7098-7106. 94186, 10559177.
12. McDaniel R, Thamchaipenet A, Gustafsson C, Fu H, Betlach M, et al. Multiple genetic modifications of the erythromycin polyketide synthase to produce a library of novel " unnatural" natural products. Proc Natl Acad Sci USA 1999, 96:1846-1851. 10.1073/pnas.96.5.1846, 26699, 10051557.
13. Pfeifer BA, Admiraal SJ, Gramajo H, Cane DE, Khosla C. Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli. Science 2001, 291:1790-1792. 10.1126/science.1058092, 11230695.
14. Kealey JT, Liu L, Santi DV, Betlach MC, Barr PJ. Production of a polyketide natural product in nonpolyketide-producing prokaryotic and eukaryotic hosts. Proc Natl Acad Sci USA 1998, 95:505-509. 10.1073/pnas.95.2.505, 18449, 9435221.
15. Reeves AR, Cernota WH, Brikun IA, Wesley RK, Weber JM. Engineering precursor flow for increased erythromycin production in Aeromicrobium erythreum. Metab Eng 2004, 6:300-312. 10.1016/j.ymben.2004.03.003, 15491860.
16. Elliot M, Damji F, Passantino R, Chater K, Leskiw B. The bldD gene of Streptomyces coelicolor A3(2): a regulatory gene involved in morphogenesis and antibiotic production. J Bacteriol 1998, 180:1549-1555. 107056, 9515925.
17. Elliot MA, Bibb MJ, Buttner MJ, Leskiw BK. BldD is a direct regulator of key developmental genes in Streptomyces coelicolor A3(2). Mol Microbiol 2001, 40:257-269. 10.1046/j.1365-2958.2001.02387.x, 11298292.
18. Chng C, Lum AM, Vroom JA, Kao CM. A key developmental regulator controls the synthesis of the antibiotic erythromycin in Saccharopolyspora erythraea. Proc Natl Acad Sci USA 2008, 105:11346-11351. 10.1073/pnas.0803622105, 2516264, 18685110.
19. Chen Y, Deng W, Wu J, Qian J, Chu J, et al. Genetic modulation of the overexpression of tailoring genes eryK and eryG leading to the improvement of erythromycin A purity and production in Saccharopolyspora erythraea fermentation. Appl Environ Microbiol 2008, 74:1820-1828. 10.1128/AEM.02770-07, 2268306, 18223111.
20. Reeves AR, Brikun IA, Cernota WH, Leach BI, Gonzalez MC, et al. Engineering of the methylmalonyl-CoA metabolite node of Saccharopolyspora erythraea for increased erythromycin production. Metab Eng 2007, 9:293-303. 10.1016/j.ymben.2007.02.001, 2722834, 17482861.
21. Stephanopoulos G, Kelleher J. Biochemistry. How to make a superior cell. Science 2001, 292:2024-2025. 10.1126/science.1062556, 11408647.
22. Bro C, Nielsen J. Impact of 'ome' analyses on inverse metabolic engineering. Metab Eng 2004, 6:204-211. 10.1016/j.ymben.2003.11.005, 15256210.
23. Lee SY, Lee DY, Kim TY. Systems biotechnology for strain improvement. Trends Biotechnol 2005, 23:349-358. 10.1016/j.tibtech.2005.05.003, 15923052.
24. Stafford DE, Stephanopoulos G. Metabolic engineering as an integrating platform for strain development. Curr Opin Microbiol 2001, 4:336-340. 10.1016/S1369-5274(00)00214-9, 11378489.
25. van der Werf MJ, Jellema RH, Hankemeier T. Microbial metabolomics: replacing trial-and-error by the unbiased selection and ranking of targets. J Ind Microbiol Biotechnol 2005, 32:234-252. 10.1007/s10295-005-0231-4, 15895265.
26. Askenazi M, Driggers EM, Holtzman DA, Norman TC, Iverson S, et al. Integrating transcriptional and metabolite profiles to direct the engineering of lovastatin-producing fungal strains. Nat Biotechnol 2003, 21:150-156. 10.1038/nbt781, 12536215.
27. Zhuo Y, Zhang W, Chen D, Gao H, Tao J, et al. Reverse biological engineering of hrdB to enhance the production of avermectins in an industrial strain of Streptomyces avermitilis. Proc Natl Acad Sci U S A 2010, 107:11250-11254. 10.1073/pnas.1006085107, 2895102, 20534557.
28. Peano C, Bicciato S, Corti G, Ferrari F, Rizzi E, et al. Complete gene expression profiling of Saccharopolyspora erythraea using GeneChip DNA microarrays. Microb Cell Fact 2007, 6:37. 10.1186/1475-2859-6-37, 2206050, 18039355.
29. Lum AM, Huang J, Hutchinson CR, Kao CM. Reverse engineering of industrial pharmaceutical-producing actinomycete strains using DNA microarrays. Metab Eng 2004, 6:186-196. 10.1016/j.ymben.2003.12.001, 15256208.
30. Chang X, Liu S, Yu YT, Li YX, Li YY. Identifying modules of coexpressed transcript units and their organization of Saccharopolyspora erythraea from time series gene expression profiles. PLoS One 2010, 5:e12126. 10.1371/journal.pone.0012126, 2920828, 20711345.
31. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. The COG database: an updated version includes eukaryotes. BMC Bioinforma 2003, 4:41.
32. Reeve L, Baumberg S. Physiological controls of erythromycin production by Saccharopolyspora erythraea are exerted at least in part at the level of transcription. Biotechnol Lett 1998, 20:585-589.
33. de la Fuente A. From 'differential expression' to 'differential networking' - identification of dysfunctional regulatory networks in diseases. Trends Genet 2010, 26:326-333. 10.1016/j.tig.2010.05.001, 20570387.
34. Yu H, Liu BH, Ye ZQ, Li C, Li YX, et al. Link-based quantitative methods to identify differentially coexpressed genes and gene pairs. BMC Bioinforma 2011, 12:315.
35. Liu BH, Yu H, Tu K, Li C, Li YX, et al. DCGL: an R package for identifying differentially coexpressed genes and links from gene expression microarray data. Bioinformatics 2010, 26:2637-2638. 10.1093/bioinformatics/btq471, 2951087, 20801914.
36. Friedland N, Mack TR, Yu M, Hung LW, Terwilliger TC, et al. Domain orientation in the inactive response regulator Mycobacterium tuberculosis MtrA provides a barrier to activation. Biochemistry 2007, 46:6733-6743. 10.1021/bi602546q, 2528954, 17511470.
37. Brocker M, Bott M. Evidence for activator and repressor functions of the response regulator MtrA from Corynebacterium glutamicum. FEMS Microbiol Lett 2006, 264:205-212. 10.1111/j.1574-6968.2006.00456.x, 17064374.
38. Zahrt TC, Deretic V. An essential two-component signal transduction system in Mycobacterium tuberculosis. J Bacteriol 2000, 182:3832-3838. 10.1128/JB.182.13.3832-3838.2000, 94557, 10851001.
39. Cangelosi GA, Do JS, Freeman R, Bennett JG, Semret M, et al. The two-component regulatory system mtrAB is required for morphotypic multidrug resistance in Mycobacterium avium. Antimicrob Agents Chemother 2006, 50:461-468. 10.1128/AAC.50.2.461-468.2006, 1366905, 16436697.
40. Fol M, Chauhan A, Nair NK, Maloney E, Moomey M, et al. Modulation of Mycobacterium tuberculosis proliferation by MtrA, an essential two-component response regulator. Mol Microbiol 2006, 60:643-657. 10.1111/j.1365-2958.2006.05137.x, 16629667.
41. Hoskisson PA, Hutchings MI. MtrAB-LpqB: a conserved three-component system in actinobacteria?. Trends Microbiol 2006, 14:444-449. 10.1016/j.tim.2006.08.005, 16934981.
42. Rajagopalan M, Dziedzic R, Al Zayer M, Stankowska D, Ouimet MC, et al. Mycobacterium tuberculosis origin of replication and the promoter for immunodominant secreted antigen 85B are the targets of MtrA, the essential response regulator. J Biol Chem 2010, 285:15816-15827. 10.1074/jbc.M109.040097, 2871449, 20223818.
43. Weirauch MT, Hughes TR. Dramatic changes in transcription factor binding over evolutionary time. Genome Biol 2010, 11:122. 10.1186/gb-2010-11-6-122, 2911098, 20519030.
44. Snider J, Houry WA. MoxR AAA + ATPases: a novel family of molecular chaperones?. J Struct Biol 2006, 156:200-209. 10.1016/j.jsb.2006.02.009, 16677824.
45. Reeves AR, Brikun IA, Cernota WH, Leach BI, Gonzalez MC, et al. Effects of methylmalonyl-CoA mutase gene knockouts on erythromycin production in carbohydrate-based and oil-based fermentations of Saccharopolyspora erythraea. J Ind Microbiol Biotechnol 2006, 33:600-609. 10.1007/s10295-006-0094-3, 16491356.
46. Reeves A, Haldenwang WG. Isolation and characterization of dominant mutations in the Bacillus subtilis stressosome components RsbR and RsbS. J Bacteriol 2007, 189:1531-1541. 10.1128/JB.01649-06, 1855730, 17158665.
47. Lian W, Jayapal KP, Charaniya S, Mehra S, Glod F, et al. Genome-wide transcriptome analysis reveals that a pleiotropic antibiotic regulator, AfsS, modulates nutritional stress response in Streptomyces coelicolor A3(2). BMC Genomics 2008, 9:56. 10.1186/1471-2164-9-56, 2267785, 18230178.
48. Martin JF, Liras P. Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr Opin Microbiol 2010, 13:263-273. 10.1016/j.mib.2010.02.008, 20303823.
49. Martin JF. Phosphate control of the biosynthesis of antibiotics and other secondary metabolites is mediated by the PhoR-PhoP system: an unfinished story. J Bacteriol 2004, 186:5197-5201. 10.1128/JB.186.16.5197-5201.2004, 490900, 15292120.
50. Santos-Beneit F, Rodriguez-Garcia A, Sola-Landa A, Martin JF. Cross-talk between two global regulators in Streptomyces: PhoP and AfsR interact in the control of afsS, pstS and phoRP transcription. Mol Microbiol 2009, 72:53-68. 10.1111/j.1365-2958.2009.06624.x, 19220751.
51. Rodriguez-Garcia A, Sola-Landa A, Apel K, Santos-Beneit F, Martin JF. Phosphate control over nitrogen metabolism in Streptomyces coelicolor: direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP. Nucleic Acids Res 2009, 37:3230-3242. 10.1093/nar/gkp162, 2691820, 19321498.
52. Blanco AG, Sola M, Gomis-Ruth FX, Coll M. Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 2002, 10:701-713. 10.1016/S0969-2126(02)00761-X, 12015152.
53. Peano C, Tala A, Corti G, Pasanisi D, Durante M, et al. Comparative genomics and transcriptional profiles of Saccharopolyspora erythraea NRRL 2338 and a classically improved erythromycin over-producing strain. Microb Cell Fact 2012, 11:32. 10.1186/1475-2859-11-32, 3359211, 22401291.
54. Lukashin AV, Borodovsky M. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 1998, 26:1107-1115. 10.1093/nar/26.4.1107, 147337, 9461475.
55. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res 1999, 27:4636-4641. 10.1093/nar/27.23.4636, 148753, 10556321.
56. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
57. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29. 10.1038/75556, 3037419, 10802651.
58. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964. 146525, 9023104.
59. Smyth GK. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. New York: Springer, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W.
60. Tai YC. timecourse: Statistical Analysis for Develepmental Microarray Time Course Data 2007, http://wwwbioconductororg.
61. Tai YC, Speed TP. A multivariate empirical Bayes statistic for replicated microarray time course data. Ann Statist 2006, 34:2387-2412.
62. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
63. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 1993, 234:779-815. 10.1006/jmbi.1993.1626, 8254673.
64. Hartmann H, Guthöhrlein EW, Siebert M, Luehr S, Söding J. P-value-based regulatory motif discovery using positional weight matrices. Genome Res 2013, 23:181-194. 10.1101/gr.139881.112, 3530678, 22990209.
65. Hertz GZ, Stormo GD. Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 1999, 15:563-577. 10.1093/bioinformatics/15.7.563, 10487864.