Chassis optimization as a cornerstone for the application of synthetic biology based strategies in microbial secondary metabolism

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Beites, Tiago ^a,b,c   Mendes, Marta V ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Chassis; Genome reduction; Genome streamlining; Heterologous expression; Specialized metabolites; Streptomyces

Indexed keywords

GENE CLUSTER; GENE EXPRESSION; GENOME; MICROBIAL METABOLISM; MUTAGENESIS; NONHUMAN; REVIEW; RIBOSOME; SACCHAROMYCES CEREVISIAE; SECONDARY METABOLISM; STREPTOMYCES; STREPTOMYCES AVERMITILIS;

EID: 84946746207     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00906     Document Type: Review

References (81)

1. Alexander, D. C., Rock, J., He, X., Brian, P., Miao, V., and Baltz, R. H. (2010). Development of a genetic system for combinatorial biosynthesis of lipopeptides in Streptomyces fradiae and heterologous expression of the A54145 biosynthesis gene cluster. Appl. Environ. Microbiol. 76, 6877-6887. doi: 10.1128/aem.01248-10
2. Baltz, R. H. (2008). Renaissance in antibacterial discovery from actinomycetes. Curr. Opin. Pharmacol. 8, 557-563. doi: 10.1016/j.coph.2008.04.008
3. Berdy, J. (2005). Bioactive microbial metabolites. J. Antibiot. (Tokyo) 58, 1-26. doi: 10.1038/ja.2005.1
4. Branda, C. S., and Dymecki, S. M. (2004). Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 6, 7-28. doi: 10.1016/S1534-5807(03)00399-X
5. Brito, Â., Gaifem, J., Ramos, V., Glukhov, E., Dorrestein, P. C., Gerwick, W. H., et al. (2015). Bioprospecting Portuguese Atlantic coast cyanobacteria for bioactive secondary metabolites reveals untapped chemodiversity. Algal Res. 9, 218-226. doi: 10.1016/j.algal.2015.03.016
6. Channon, K., Bromley, E. H., and Woolfson, D. N. (2008). Synthetic biology through biomolecular design and engineering. Curr. Opin. Struct. Biol. 18, 491-498. doi: 10.1016/j.sbi.2008.06.006
7. Danchin, A. (2012). Scaling up synthetic biology: do not forget the chassis. FEBS Lett. 586, 2129-2137. doi: 10.1016/j.febslet.2011.12.024
8. de las Heras, A., Carreno, C. A., and De Lorenzo, V. (2008). Stable implantation of orthogonal sensor circuits in Gram-negative bacteria for environmental release. Environ. Microbiol. 10, 3305-3316. doi: 10.1111/j.1462-2920.2008.01722.x
9. de Lorenzo, V. (2011). Beware of metaphors: chasses and orthogonality in synthetic biology. Bioeng. Bugs 2, 3-7. doi: 10.4161/bbug.2.1.13388
10. Eustaquio, A. S., Gust, B., Galm, U., Li, S. M., Chater, K. F., and Heide, L. (2005). Heterologous expression of novobiocin and clorobiocin biosynthetic gene clusters. Appl. Environ. Microbiol. 71, 2452-2459. doi: 10.1128/AEM.71.5.2452-2459.2005
11. Fernandez-Martinez, L. T., and Bibb, M. J. (2014). Use of the meganuclease I-SceI of Saccharomyces cerevisiae to select for gene deletions in actinomycetes. Sci. Rep. 4, 7100. doi: 10.1038/srep07100
12. Flinspach, K., Kapitzke, C., Tocchetti, A., Sosio, M., and Apel, A. K. (2014). Heterologous expression of the thiopeptide antibiotic GE2270 from Planobispora rosea ATCC 53733 in Streptomyces coelicolor requires deletion of ribosomal genes from the expression construct. PLoS ONE 9:e90499. doi: 10.1371/journal.pone.0090499
13. Floriano, B., and Bibb, M. (1996). afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol. Microbiol. 21, 385-396. doi: 10.1046/j.1365-2958.1996.6491364.x
14. Gibson, D. G., Glass, J. I., Lartigue, C., Noskov, V. N., Chuang, R. Y., Algire, M. A., et al. (2010). Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329, 52-56. doi: 10.1126/science.1190719
15. Gomez-Escribano, J. P., and Bibb, M. J. (2011). Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters. Microb. Biotechnol. 4, 207-215. doi: 10.1111/j.1751-7915.2010.00219.x
16. Gross, H., and Loper, J. E. (2009). Genomics of secondary metabolite production by Pseudomonas spp. Nat. Prod. Rep. 26, 1408-1446. doi: 10.1039/b817075b
17. Guenther, C. M., Kuypers, B. E., Lam, M. T., Robinson, T. M., Zhao, J., and Suh, J. (2014). Synthetic virology: engineering viruses for gene delivery. WIREs Nanomed. Nanobiotechnol. 6, 548-558. doi: 10.1002/wnan.1287
18. Gullon, S., Olano, C., Abdelfattah, M. S., Brana, A. F., Rohr, J., Mendez, C., et al. (2006). Isolation, characterization, and heterologous expression of the biosynthesis gene cluster for the antitumor anthracycline steffimycin. Appl. Environ. Microbiol. 72, 4172-4183. doi: 10.1128/aem.00734-06
19. Haft, D. H., Selengut, J., Mongodin, E. F., and Nelson, K. E. (2005). A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput. Biol. 1:e60. doi: 10.1371/journal.pcbi.0010060
20. Hamamoto, T., Gunji, S., Tsuji, H., and Beppu, T. (1983). Leptomycins A and B, new antifungal antibiotics. I. Taxonomy of the producing strain and their fermentation, purification and characterization. J. Antibiot. (Tokyo) 36, 639-645.
21. Harrison, J., and Studholme, D. J. (2014). Recently published Streptomyces genome sequences. Microb. Biotechnol. 7, 373-380. doi: 10.1111/1751-7915.12143
22. Herrmann, S., Siegl, T., Luzhetska, M., Petzke, L., Jilg, C., Welle, E., et al. (2012). Site-specific recombination strategies for engineering actinomycete genomes. Appl. Environ. Microbiol. 78, 1804-1812. doi: 10.1128/aem.06054-11
23. Ijaq, J., Chandrasekharan, M., Poddar, R., Bethi, N., and Sundararajan, V. S. (2015). Annotation and curation of uncharacterized proteins-challenges. Front. Genet. 6:119. doi: 10.3389/fgene.2015.00119
24. Ikeda, H., Shin-Ya, K., and Omura, S. (2013). Genome mining of the Streptomyces avermitilis genome and development of genome-minimized hosts for heterologous expression of biosynthetic gene clusters. J. Ind. Microbiol. Biotechnol. 41, 233-250. doi: 10.1007/s10295-013-1327-x
25. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821. doi: 10.1126/science.1225829
26. Jones, A. C., Gust, B., Kulik, A., Heide, L., Buttner, M. J., and Bibb, M. J. (2013). Phage p1-derived artificial chromosomes facilitate heterologous expression of the FK506 gene cluster. PLoS ONE 8:e69319. doi: 10.1371/journal.pone.0069319
27. Juhas, M., Reuss, D. R., Zhu, B., and Commichau, F. M. (2014). Bacillus subtilis and Escherichia coli essential genes and minimal cell factories after one decade of genome engineering. Microbiology 160, 2341-2351. doi: 10.1099/mic.0.079376-0
28. Karlinsey, J. E. (2007). Lambda-Red genetic engineering in Salmonella enterica serovar Typhimurium. Methods Enzymol. 421, 199-209. doi: 10.1016/s0076-6879(06)21016-4
29. Khodakaramian, G., Lissenden, S., Gust, B., Moir, L., Hoskisson, P. A., Chater, K. F., et al. (2006). Expression of Cre recombinase during transient phage infection permits efficient marker removal in Streptomyces. Nucleic Acids Res. 34, e20. doi: 10.1093/nar/gnj019
30. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F., and Hopwood, D. A. (2000). Practical Streptomyces Genetics. Norwich: The John Innes Foundation.
31. Kim, J. N., Kim, Y., Jeong, Y., Roe, J. H., Kim, B. G., and Cho, B. K. (2015). Comparative genomics reveals the core and accessory genomes of Streptomyces species. J. Microbiol. Biotechnol. doi: 10.4014/jmb.1504.04008 [Epub ahead of print].
32. Kim, S. Y., Zhao, P., Igarashi, M., Sawa, R., Tomita, T., Nishiyama, M., et al. (2009). Cloning and heterologous expression of the cyclooctatin biosynthetic gene cluster afford a diterpene cyclase and two p450 hydroxylases. Chem. Biol. 16, 736-743. doi: 10.1016/j.chembiol.2009.06.007
33. Komatsu, M., Komatsu, K., Koiwai, H., Yamada, Y., Kozone, I., Izumikawa, M., et al. (2013). Engineered Streptomyces avermitilis host for heterologous expression of biosynthetic gene cluster for secondary metabolites. ACS Synth. Biol. 2, 384-396. doi: 10.1021/sb3001003
34. Komatsu, M., Uchiyama, T., Omura, S., Cane, D. E., and Ikeda, H. (2010). Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism. Proc. Natl. Acad. Sci. U.S.A. 107, 2646-2651. doi: 10.1073/pnas.0914833107
35. Kuhn, R., and Torres, R. M. (2002). Cre/loxP recombination system and gene targeting. Methods Mol. Biol. 180, 175-204. doi: 10.1385/1-59259-178-7:175
36. Kurihara, K., Tamura, M., Shohda, K., Toyota, T., Suzuki, K., and Sugawara, T. (2011). Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nat. Chem. 3, 775-781. doi: 10.1038/nchem.1127
37. Laureti, L., Song, L., Huang, S., Corre, C., Leblond, P., Challis, G. L., et al. (2011). Identification of a bioactive 51-membered macrolide complex by activation of a silent polyketide synthase in Streptomyces ambofaciens. Proc. Natl. Acad. Sci. U.S.A. 108, 6258-6263. doi: 10.1073/pnas.1019077108
38. Leprince, A., De Lorenzo, V., Voller, P., Van Passel, M. W., and Martins Dos Santos, V. A. (2012a). Random and cyclical deletion of large DNA segments in the genome of Pseudomonas putida. Environ. Microbiol. 14, 1444-1453. doi: 10.1111/j.1462-2920.2012.02730.x
39. Leprince, A., Van Passel, M. W., and Dos Santos, V. A. (2012b). Streamlining genomes: toward the generation of simplified and stabilized microbial systems. Curr. Opin. Biotechnol. 23, 651-658. doi: 10.1016/j.copbio.2012.05.001
40. Li, R., and Townsend, C. A. (2006). Rational strain improvement for enhanced clavulanic acid production by genetic engineering of the glycolytic pathway in Streptomyces clavuligerus. Metab. Eng. 8, 240-252. doi: 10.1016/j.ymben.2006.01.003
41. Li, X. T., Thomason, L. C., Sawitzke, J. A., Costantino, N., and Court, D. L. (2013). Bacterial DNA polymerases participate in oligonucleotide recombination. Mol. Microbiol. 88, 906-920. doi: 10.1111/mmi.12231
42. Liu, G., Chater, K. F., Chandra, G., Niu, G., and Tan, H. (2013). Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol. Mol. Biol. Rev. 77, 112-143. doi: 10.1128/MMBR.00054-12
43. Luo, Y., Zhang, L., Barton, K. W., and Zhao, H. (2015). Systematic identification of a panel of strong constitutive promoters from Streptomyces albus. ACS Synth. Biol. doi: 10.1021/acssynbio.5b00016 [Epub ahead of print].
44. Martinez-Burgo, Y., Alvarez-Alvarez, R., Perez-Redondo, R., and Liras, P. (2014). Heterologous expression of Streptomyces clavuligerus ATCC 27064 cephamycin C gene cluster. J. Biotechnol. 186, 21-29. doi: 10.1016/j.jbiotec.2014.06.002
45. Martinez-Castro, M., Salehi-Najafabadi, Z., Romero, F., Perez-Sanchiz, R., Fernandez-Chimeno, R. I., Martin, J. F., et al. (2013). Taxonomy and chemically semi-defined media for the analysis of the tacrolimus producer Streptomyces tsukubaensis. Appl. Microbiol. Biotechnol. 97, 2139-2152. doi: 10.1007/s00253-012-4364-x
46. Miyamoto, K. T., Komatsu, M., and Ikeda, H. (2014). Discovery of gene cluster for mycosporine-like amino acid biosynthesis from Actinomycetales microorganisms and production of a novel mycosporine-like amino acid by heterologous expression. Appl. Environ. Microbiol. 80, 5028-5036. doi: 10.1128/AEM.00727-14
47. Mondol, M. A., Shin, H. J., and Islam, M. T. (2013). Diversity of secondary metabolites from marine Bacillus species: chemistry and biological activity. Mar. Drugs 11, 2846-2872. doi: 10.3390/md11082846
48. Morimoto, T., Kadoya, R., Endo, K., Tohata, M., Sawada, K., Liu, S., et al. (2008). Enhanced recombinant protein productivity by genome reduction in Bacillus subtilis. DNA Res. 15, 73-81. doi: 10.1093/dnares/dsn002
49. Murphy, K. C. (1998). Use of bacteriophage lambda recombination functions to promote gene replacement in Escherichia coli. J. Bacteriol. 180, 2063-2071.
50. Nett, M., Ikeda, H., and Moore, B. S. (2009). Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat. Prod. Rep. 26, 1362-1384. doi: 10.1039/b817069j
51. Nieminen, L., Webb, S., Smith, M. C., and Hoskisson, P. A. (2013). A flexible mathematical model platform for studying branching networks: experimentally validated using the model actinomycete, Streptomyces coelicolor. PLoS ONE 8:e54316. doi: 10.1371/journal.pone.0054316
52. Ochi, K., and Hosaka, T. (2012). New strategies for drug discovery: activation of silent or weakly expressed microbial gene clusters. Appl. Microbiol. Biotechnol. 97, 87-98. doi: 10.1007/s00253-012-4551-9
53. Olano, C., Garcia, I., Gonzalez, A., Rodriguez, M., Rozas, D., Rubio, J., et al. (2014). Activation and identification of five clusters for secondary metabolites in Streptomyces albus J1074. Microb. Biotechnol. 7, 242-256. doi: 10.1111/1751-7915.12116
54. Olano, C., Lombo, F., Mendez, C., and Salas, J. A. (2008). Improving production of bioactive secondary metabolites in actinomycetes by metabolic engineering. Metab. Eng. 10, 281-292. doi: 10.1016/j.ymben.2008.07.001
55. Omura, S., Ikeda, H., Ishikawa, J., Hanamoto, A., Takahashi, C., Shinose, M., et al. (2001). Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sci. U.S.A. 98, 12215-12220. doi: 10.1073/pnas.211433198
56. Peano, C., Bicciato, S., Corti, G., Ferrari, F., Rizzi, E., Bonnal, R. J., et al. (2007). Complete gene expression profiling of Saccharopolyspora erythraea using GeneChip DNA microarrays. Microb. Cell Fact. 6, 37. doi: 10.1186/1475-2859-6-37
57. Peano, C., Tala, A., Corti, G., Pasanisi, D., Durante, M., Mita, G., et al. (2012). Comparative genomics and transcriptional profiles of Saccharopolyspora erythraea NRRL 2338 and a classically improved erythromycin over-producing strain. Microb. Cell Fact. 11, 32. doi: 10.1186/1475-2859-11-32
58. Penn, J., Li, X., Whiting, A., Latif, M., Gibson, T., Silva, C. J., et al. (2006). Heterologous production of daptomycin in Streptomyces lividans. J. Ind. Microbiol. Biotechnol. 33, 121-128. doi: 10.1007/s10295-005-0033-8
59. Posfai, G., Plunkett, G. III, Feher, T., Frisch, D., Keil, G. M., Umenhoffer, K., et al. (2006). Emergent properties of reduced-genome Escherichia coli. Science 312, 1044-1046. doi: 10.1126/science.1126439
60. Richardson, M. A., Kuhstoss, S., Huber, M. L., Ford, L., Godfrey, O., Turner, J. R., et al. (1990). Cloning of spiramycin biosynthetic genes and their use in constructing Streptomyces ambofaciens mutants defective in spiramycin biosynthesis. J. Bacteriol. 172, 3790-3798.
61. Rudolph, M. M., Vockenhuber, M. P., and Suess, B. (2013). Synthetic riboswitches for the conditional control of gene expression in Streptomyces coelicolor. Microbiology 159, 1416-1422. doi: 10.1099/mic.0.067322-0
62. Sansinenea, E., and Ortiz, A. (2011). Secondary metabolites of soil Bacillus spp. Biotechnol. Lett. 33, 1523-1538. doi: 10.1007/s10529-011-0617-5
63. Schweizer, H. P. (2003). Applications of the Saccharomyces cerevisiae Flp-FRT system in bacterial genetics. J. Mol. Microbiol. Biotechnol. 5, 67-77. doi: 10.1159/000069976
64. Shao, Z., Rao, G., Li, C., Abil, Z., Luo, Y., and Zhao, H. (2013). Refactoring the silent spectinabilin gene cluster using a plug-and-play scaffold. ACS Synth. Biol. 2, 662-669. doi: 10.1021/sb400058n
65. Siegl, T., and Luzhetskyy, A. (2012). Actinomycetes genome engineering approaches. Antonie Van Leeuwenhoek 102, 503-516. doi: 10.1007/s10482-012-9795-y
66. Swingle, B., Markel, E., Costantino, N., Bubunenko, M. G., Cartinhour, S., and Court, D. L. (2010). Oligonucleotide recombination in Gram-negative bacteria. Mol. Microbiol. 75, 138-148. doi: 10.1111/j.1365-2958.2009.06976.x
67. Tocchetti, A., Maffioli, S., Iorio, M., Alt, S., Mazzei, E., Brunati, C., et al. (2013). Capturing linear intermediates and C-terminal variants during maturation of the thiopeptide GE2270. Chem. Biol. 20, 1067-1077. doi: 10.1016/j.chembiol.2013.07.005
68. Tong, Y., Charusanti, P., Zhang, L., Weber, T., and Lee, S. Y. (2015). CRISPR-Cas9 based engineering of actinomycetal genomes. ACS Synth. Biol. doi: 10.1021/acssynbio.5b00038 [Epub ahead of print].
69. Tsou, H. R., Ahmed, Z. H., Fiala, R. R., Bullock, M. W., Carter, G. T., Goodman, J. J., et al. (1989). Biosynthetic origin of the carbon skeleton and oxygen atoms of the LL-F28249 alpha, a potent antiparasitic macrolide. J. Antibiot. (Tokyo) 42, 398-406. doi: 10.7164/antibiotics.42.398
70. Unthan, S., Baumgart, M., Radek, A., Herbst, M., Siebert, D., Bruhl, N., et al. (2015). Chassis organism from Corynebacterium glutamicum-a top-down approach to identify and delete irrelevant gene clusters. Biotechnol. J. 10, 290-301. doi: 10.1002/biot.201400041
71. Wang, H. H., Isaacs, F. J., Carr, P. A., Sun, Z. Z., Xu, G., Forest, C. R., et al. (2009). Programming cells by multiplex genome engineering and accelerated evolution. Nature 460, 894-898. doi: 10.1038/nature08187
72. Wang, K., Neumann, H., Peak-Chew, S. Y., and Chin, J. W. (2007). Evolved orthogonal ribosomes enhance the efficiency of synthetic genetic code expansion. Nat. Biotechnol. 25, 770-777. doi: 10.1038/nbt1314
73. Weber, T., Blin, K., Duddela, S., Krug, D., Kim, H. U., Bruccoleri, R., et al. (2015). antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 43, 1-7. doi: 10.1093/nar/gkv437
74. Weissman, K. J., and Muller, R. (2010). Myxobacterial secondary metabolites: bioactivities and modes-of-action. Nat. Prod. Rep. 27, 1276-1295. doi: 10.1039/c001260m
75. Wendt-Pienkowski, E., Huang, Y., Zhang, J., Li, B., Jiang, H., Kwon, H., et al. (2005). Cloning, sequencing, analysis, and heterologous expression of the fredericamycin biosynthetic gene cluster from Streptomyces griseus. J. Am. Chem. Soc. 127, 16442-16452. doi: 10.1021/ja054376u
76. Winter, J. M., Moffitt, M. C., Zazopoulos, E., Mcalpine, J. B., Dorrestein, P. C., and Moore, B. S. (2007). Molecular basis for chloronium-mediated meroterpene cyclization: cloning, sequencing, and heterologous expression of the napyradiomycin biosynthetic gene cluster. J. Biol. Chem. 282, 16362-16368. doi: 10.1074/jbc.M611046200
77. Wolpert, M., Heide, L., Kammerer, B., and Gust, B. (2008). Assembly and heterologous expression of the coumermycin A1 gene cluster and production of new derivatives by genetic engineering. Chembiochem 9, 603-612. doi: 10.1002/cbic.200700483
78. Yamada, Y., Arima, S., Nagamitsu, T., Johmoto, K., Uekusa, H., Eguchi, T., et al. (2015). Novel terpenes generated by heterologous expression of bacterial terpene synthase genes in an engineered Streptomyces host. J. Antibiot. (Tokyo) 68, 385-394. doi: 10.1038/ja.2014.171
79. Young, T. S., and Walsh, C. T. (2011). Identification of the thiazolyl peptide GE37468 gene cluster from Streptomyces ATCC 55365 and heterologous expression in Streptomyces lividans. Proc. Natl. Acad. Sci. U.S.A. 108, 13053-13058. doi: 10.1073/pnas.1110435108
80. Zaburannyi, N., Rabyk, M., Ostash, B., Fedorenko, V., and Luzhetskyy, A. (2014). Insights into naturally minimised Streptomyces albus J1074 genome. BMC Genomics 15:97. doi: 10.1186/1471-2164-15-97
81. Zhou, M., Jing, X., Xie, P., Chen, W., Wang, T., Xia, H., et al. (2012). Sequential deletion of all the polyketide synthase and nonribosomal peptide synthetase biosynthetic gene clusters and a 900-kb subtelomeric sequence of the linear chromosome of Streptomyces coelicolor. FEMS Microbiol. Lett. 333, 169-179. doi: 10.1111/j.1574-6968.2012.02609.x