Rational engineering of Streptomyces albus J1074 for the overexpression of secondary metabolite gene clusters

Microbial Cell Factories

Volumn 17, Issue 1, 2018, Pages

  Kallifidas, Dimitris ^a   Jiang, Guangde ^a   Ding, Yousong ^a   Luesch, Hendrik ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Heterologous expression; Secondary metabolism; Streptomyces albus host engineering; Synthetic biology

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ACTINORHODINE; CARISOPRODOL; CRISPR ASSOCIATED PROTEIN; RNA POLYMERASE BETA SUBUNIT; TRANSFER RNA;

ADPA GENE; AFSA-ARPA GENE; ARTICLE; ATRA GENE; BACILLUS CEREUS; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM CULTURE; BLDA GENE; CODON; CRP GENE; DASR GENE; DISULFIDE BOND; DNA ISOLATION; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SEQUENCE; HOMOLOGOUS RECOMBINATION; ION TRAP MASS SPECTROMETRY; KBPA-AFSKRS GENE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PFK GENE; PHOR-PHOP GENE; PLEIOTROPY; POLYMERASE CHAIN REACTION; PROTEIN ENGINEERING; PROTEIN MOTIF; RELA GENE; RPOB GENE; RPSL GENE; SECONDARY METABOLISM; STREPTOMYCES ALBUS; STREPTOMYCES COELICOLOR; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WBLA GENE; GENETICS; MULTIGENE FAMILY; PROCEDURES; STREPTOMYCES; WHOLE GENOME SEQUENCING;

MULTIGENE FAMILY; STREPTOMYCES; WHOLE GENOME SEQUENCING;

EID: 85042167325     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-018-0874-2     Document Type: Article

References (57)

1. Baltz RH. Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol. 2008;8:557-63.
2. Liu G, Chater KF, Chandra G, Niu G, Tan H. Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev. 2013;77:112-43.
3. Tan GY, Deng K, Liu X, Tao H, Chang Y, Chen J, Chen K, Sheng Z, Deng Z, Liu T. Heterologous biosynthesis of spinosad: an omics-guided large polyketide synthase gene cluster reconstitution in Streptomyces. ACS Synth Biol. 2017;6:995-1005.
4. Shao Z, Rao G, Li C, Abil Z, Luo Y, Zhao H. Refactoring the silent spectinabilin gene cluster using a plug-and-play scaffold. ACS Synth Biol. 2013;2:662-9.
5. Zaburannyi N, Rabyk M, Ostash B, Fedorenko V, Luzhetskyy A. Insights into naturally minimised Streptomyces albus J1074 genome. BMC Genom. 2014;15:97.
6. Baltz RH. Streptomyces and Saccharopolyspora hosts for heterologous expression of secondary metabolite gene clusters. J Ind Microbiol Biotechnol. 2010;15:759-72.
7. Lombó F, Velasco A, Castro A, de la Calle F, Braña AF, Sánchez-Puelles JM, Méndez C, Salas JA. Deciphering the biosynthesis pathway of the antitumor thiocoraline from a marine actinomycete and its expression in two Streptomyces species. ChemBioChem. 2006;15:366-76.
8. Bilyk O, Sekurova ON, Zotchev SB, Luzhetskyy A. Cloning and heterologous expression of the grecocycline biosynthetic gene cluster. PLoS ONE. 2016;11:e0158682.
9. Kallifidas D, Kang HS, Brady SF. Tetarimycin A, an MRSA-active antibiotic identified through induced expression of environmental DNA gene clusters. J Am Chem Soc. 2012;134:19552-5.
10. Feng Z, Kallifidas D, Brady SF. Functional analysis of environmental DNA-derived type II polyketide synthases reveals structurally diverse secondary metabolites. Proc Natl Acad Sci USA. 2011;108:12629-34.
11. Olano C, García I, González A, Rodriguez M, Rozas D, Rubio J, Sánchez-Hidalgo M, Braña AF, Méndez C, Salas JA. Activation and identification of five clusters for secondary metabolites in Streptomyces albus J1074. Microb Biotechnol. 2014;7:242-56.
12. Gomez-Escribano JP, Bibb MJ. Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters. Microb Biotechnol. 2011;4:207-15.
13. Fowler-Goldsworthy K, Gust B, Mouz S, Chandra G, Findlay KC, Chater KF. The actinobacteria-specific gene wblA controls major developmental transitions in Streptomyces coelicolor A3(2). Microbiology. 2011;157:1312-28.
14. Kang SH, Huang J, Lee HN, Hur A, Cohen SN, Kim ES. Interspieces DNA microarray analysis identifies WblA as a pleiotropic down-regulator of antibiotic biosynthesis in Streptomyces. J Bacteriol. 2007;189:4315-9.
15. Lee HN, Kim JS, Kim P, Lee HS, Kim ES. Repression of antibiotic down-regulator by AdpA in Streptomyces coelicolor. Appl Environ Microbiol. 2013;79:4159-63.
16. Higo A, Hara H, Horinouchi S, Ohnishi Y. Genome-wide distribution of AdpA, a global regulator for secondary metabolism and morphological differentiation in Streptomyces, revealed the extent and complexity of the AdpA regulatory network. DNA Res. 2012;193:259-73.
17. Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, Hopwood DA, van Wezel GP. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep. 2008;9:670-5.
18. Li X, Yu T, He Q, McDowall KJ, Jiang B, Jiang Z, Wu L, Li G, Li Q, Wang S, Shi Y, Wang L, Hong B. Binding of a biosynthetic intermediate to AtrA modulates the production of lidamycin by Streptomyces globisporus. Mol Microbiol. 2015;96:1257-71.
19. van Wezela Gilles P, McDowall Kenneth J. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep. 2011;28:1311-33.
20. Borodina I, Siebring J, Zhang J, Smith CP, van Keulen G, Dijkhuizen L, Nielsen J. Antibiotic overproduction in Streptomyces coelicolor A3(2) mediated by phosphofructokinase deletion. J Biol Chem. 2008;283:25186-99.
21. Dang L, Liu J, Wang C, Liu H, Wen J. Enhancement of rapamycin production by metabolic engineering in Streptomyces hygroscopicus based on genome-scale metabolic model. J Ind Microbiol Biotechnol. 2017;44:259-70.
22. Horinouchi S. AfsR as an integrator of signals that are sensed by multiple serine/threonine kinases in Streptomyces coelicolor A3(2). J Ind Microbiol Biotechnol. 2003;30:462-7.
23. Sola-Landa A, Moura RS, Martin JF. The two-component PhoRPhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc Natl Acad Sci USA. 2003;100:6133-8.
24. Martín JF, Rodríguez-García A, Liras P. The master regulator PhoP coordinates phosphate and nitrogen metabolism, respiration, cell differentiation and antibiotic biosynthesis: comparison in Streptomyces coelicolor and Streptomyces avermitilis. J Antibiot. 2017;70:534-41.
25. Horinouchi S. A microbial hormone, A-factor, as a master switch for morphological differentiation and secondary metabolism in Streptomyces griseus. Front Biosci. 2002;7:d2045-57.
26. Ando N, Matsumori N, Sakuda S, Beppu T, Horinouchi S. Involvement of afsA in A-factor biosynthesis as a key enzyme. J Antibiot. 1997;50:847-52.
27. Gao C, Mulder D, Yin C, Elliot MA. Crp is a global regulator of antibiotic production in Streptomyces. MBio. 2012;3:e00407-12.
28. McKenzie NL, Nodwell JR. Phosphorylated AbsA2 negatively regulates antibiotic production in Streptomyces coelicolor through interactions with pathway-specific regulatory gene promoters. J Bacteriol. 2007;189:5284-92.
29. Shu D, Chen L, Wang W, Yu Z, Ren C, Zhang W, Yang S, Lu Y, Jiang W. afsQ1-Q2-sigQ is a pleiotropic but conditionally required signal transduction system for both secondary metabolism and morphological development in Streptomyces coelicolor. Appl Microbiol Biotechnol. 2009;81:1149-60.
30. Hesketh A, Sun J, Bibb M. Induction of ppGpp synthesis in Streptomyces coelicolor A3(2) grown under conditions of nutritional sufficiency elicits actII-ORF4 transcription and actinorhodin biosynthesis. Mol Microbiol. 2001;39:136-44.
31. Jin W, Ryu YG, Kang SG, Kim SK, Saito N, Ochi K, Lee SH, Lee KJ. Two relA/spoT homologous genes are involved in the morphological and physiological differentiation of Streptomyces clavuligerus. Microbiology. 2004;150:1485-93.
32. Hu H, Zhang Q, Ochi K. Activation of antibiotic biosynthesis by specified mutations in the rpoB gene (encoding the RNA polymerase beta subunit) of Streptomyces lividans. J Bacteriol. 2002;184:3984-91.
33. Wang G, Hosaka T, Ochi K. Dramatic activation of antibiotic production in Streptomyces coelicolor by cumulative drug resistance mutations. Appl Environ Microbiol. 2008;74:2834-40.
34. Koshla O, Lopatniuk M, Rokytskyy I, Yushchuk O, Dacyuk Y, Fedorenko V, Luzhetskyy A, Ostash B. Properties of Streptomyces albus J1074 mutant deficient in tRNALeuUAA gene bldA. Arch Microbiol. 2017. https://doi.org/10.1007/s00203-017-1389-7.
35. Chater KF, Chandra G. The use of the rare UUA codon to define "expression space" for genes involved in secondary metabolism, development and environmental adaptation in Streptomyces. J Microbiol. 2008;46:1-11.
36. Lee HN, Huang J, Im JH, Kim SH, Noh JH, Cohen SN, Kim ES. Putative TetR family transcriptional regulator SCO1712 encodes an antibiotic downregulator in Streptomyces coelicolor. Appl Environ Microbiol. 2010;76:3039-43.
37. Kieser T, Bibb MJ, Chater K, Hopwood DA. Practical Streptomyces genetics. Norwich: Norwich Research Park; 2000.
38. Bystrykh L, Fernandez-Moreno MA, Herrema JK, Malpartida F, Hopwood DA, Dijkhuizen L. Production of actinorhodin-related "blue pigments" by Streptomyces coelicolor A3(2). J Bacteriol. 1996;178:2238-44.
39. Paget MS, Kang JG, Roe JH, Buttner MJ. sigmaR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J. 1998;17:5776-82.
40. Gust B, Challis GL, Fowler K, Kieser T, Chater KF. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA. 2003;100:1541-6.
41. Huang X, Ma T, Tian J, Shen L, Zuo H, Hu C, Liao G. wblA, a pleiotropic regulatory gene modulating morphogenesis and daptomycin production in Streptomyces roseosporus. J Appl Microbiol. 2017;123:669-77.
42. Lu C, Liao G, Zhang J, Tan H. Identification of novel tylosin analogues generated by a wblA disruption mutant of Streptomyces ansochromogenes. Microb Cell Fact. 2015;14:173.
43. Rabyk M, Ostash B, Rebets Y, Walker S, Fedorenko V. Streptomyces ghanaensis pleiotropic regulatory gene wblA(gh) influences morphogenesis and moenomycin production. Biotechnol Lett. 2011;33:2481-6.
44. Medina-Rivera A, Defrance M, Sand O, Herrmann C, Castro-Mondragon JA, Delerce J, Jaeger S, Blanchet C, Vincens P, Caron C, Staines DM, Contreras-Moreira B, Artufel M, Charbonnier-Khamvongsa L, Hernandez C, Thieffry D, Thomas-Chollier M, van Helden J. RSAT 2015: regulatory sequence analysis tools. Nucleic Acids Res. 2015;43:W50-6.
45. Coze F, Gilard F, Tcherkez G, Virolle MJ, Guyonvarch A. Carbon-flux distribution within Streptomyces coelicolor metabolism: a comparison between the actinorhodin-producing strain M145 and its non-producing derivative M1146. PLoS ONE. 2013;8(12):e84151.
46. Esnault C, Dulermo T, Smirnov A, Askora A, David M, Deniset-Besseau A, Holland IB, Virolle MJ. Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145. Sci Rep. 2017;7:200.
47. Tierrafría VH, Cuauhtemoc LC, Nidia MC, Alba RR, Sara CL, Esteban M, Romina RS, Ruiz-Villafán B, Nielsen LK, Sánchez S. Deletion of the hypothetical protein SCO2127 of Streptomyces coelicolor allowed identification of a new regulator of actinorhodin production. Appl Microbiol Biotechnol. 2016;100:9229-37.
48. Ikeda H, Kotaki H, Tanaka H, Omura S. Involvement of glucose catabolism in avermectin production by Streptomyces avermitilis. Antimicrob Agents Chemother. 1988;32:282-4.
49. Kim JS, Lee HN, Kim P, Lee HS, Kim ES. Negative role of wblA in response to oxidative stress in Streptomyces coelicolor. J Microbiol Biotechnol. 2012;22:736-41.
50. Huang H, Hou L, Li H, Qiu Y, Ju J, Li W. Activation of a plasmid-situated type III PKS gene cluster by deletion of a wbl gene in deepsea-derived Streptomyces somaliensis SCSIO ZH66. Microb Cell Fact. 2016;15:116.
51. Noh JH, Kim SH, Lee HN, Lee SY, Kim ES. Isolation and genetic manipulation of the antibiotic down-regulatory gene, wblA ortholog for doxorubicin-producing Streptomyces strain improvement. Appl Microbiol Biotechnol. 2010;86(4):1145-53.
52. Woo Min-Woo, Nah Hee-Ju, Choi Si-Sun, Kim Eung-Soo. Pikromycin production stimulation through antibiotic down-regulatory gene disruption in Streptomyces venezuelae. Biotechnol Bioprocess Eng. 2014;19:973-7.
53. Derouaux A, Halici S, Nothaft H, Neutelings T, Moutzourelis G, Dusart J, Titgemeyer F, Rigali S. Deletion of a cyclic AMP receptor protein homologue diminishes germination and affects morphological development of Streptomyces coelicolor. J Bacteriol. 2004;186:1893-7.
54. Süsstrunk U, Pidoux J, Taubert S, Ullmann A, Thompson CJ. Pleiotropic effects of cAMP on germination, antibiotic biosynthesis and morphological development in Streptomyces coelicolor. Mol Microbiol. 1998;30:33-46.
55. Iqbal HA, Low-Beinart L, Obiajulu JU, Brady SF. Natural product discovery through improved functional metagenomics in Streptomyces. J Am Chem Soc. 2016;138:9341.
56. Nah JH, Kim HJ, Lee HN, Lee MJ, Choi SS, Kim ES. Identification and biotechnological application of novel regulatory genes involved in Streptomyces polyketide overproduction through reverse engineering strategy. Biomed Res Int. 2013;2013:549737.
57. Lee HN, Kim HJ, Kim P, Lee HS, Kim ES. Minimal polyketide pathway expression in an actinorhodin cluster-deleted and regulation-stimulated Streptomyces coelicolor. J Ind Microbiol Biotechnol. 2012;39:805-11.