Biotechnology of polyketides: New breath of life for the novel antibiotic genetic pathways discovery through metagenomics

Brazilian Journal of Microbiology

Volumn 44, Issue 4, 2013, Pages 1007-1034

  Gomes, Elisângela Soares ^a   Schuch, Viviane ^a   Lemos, Eliana Gertrudes de Macedo ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Environmental samples; New drugs; Pharmacology; PKSs

Indexed keywords

ANTIINFECTIVE AGENT; POLYKETIDE;

ANIMAL; BIOSYNTHESIS; BIOTECHNOLOGY; DRUG DEVELOPMENT; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLIC ENGINEERING; METABOLISM; METAGENOMICS; PROCEDURES; SECONDARY METABOLISM; TRENDS;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOSYNTHETIC PATHWAYS; BIOTECHNOLOGY; DRUG DISCOVERY; HUMANS; METABOLIC ENGINEERING; METAGENOMICS; POLYKETIDES; SECONDARY METABOLISM;

EID: 84897417190     PISSN: 15178382     EISSN: 16784405     Source Type: Journal    
DOI: 10.1590/S1517-83822013000400002     Document Type: Review

References (108)

1. Amann R. I, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Mol Biol Rev 59:143-169.
2. Bachmann B. O, Ravel J (2009) Methods for in silico prediction of microbial polyketide and nonribosomal peptide biosynthetic pathways from DNA sequence data. Methods Enzymol 458:181-217.
3. Baerson S. R, Rimando, AM (2007). A Plethora of Polyketides: Structures, Biological Activities, and Enzymes. In: Rimando, A.M., Baerson, S.R. (eds). Polyketides: Biosynthesis, Biological Activity, and Genetic Engineering. American Chemical Society, Washington, USA, 2-14.
4. Baltz H. (2006) Molecular engineering approaches to peptide, polyketide and other antibiotics. Nat Biotech 24:1533-1540.
5. Banikand J. J, Brady SF(2010) Recent application of metagenomic approaches toward the Discovery of antimicrobials and other bioactive small molecules. Current Opinion in Microbiology 13:603-609.
6. Bentley S. D, Chater KF, Cerdeno-Tarraga A-M, Challis GL, Thomson N. R, James KD, Harris DE, Quail MA, Kieser H, Harper D., Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S., Huang C-H, Kieser T, Larke L, Murphy L, Oliver K, O'Neil S, Rabbinowitsch E, Rajandream M-A, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R., Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J., Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3 (2). Nature 417:141-147.
7. Bibb M. J, Ward JM, Hopwood DA (1978) Transformation of plasmid DNA into Streptomyces at high frequence. Nature 274:398-400.
8. Brachmann A. O, Joyce SA, Jenke-Kodama H, Schwär G, Clarke DJ, Bode HB (2007) A Type II Polyketide Synthase is Responsible for Anthraquinone Biosynthesis in Photorhabdus luminescens. Chem Bio Chem 8:1721-1728.
9. Brady S. F, Chao CJ, Handelsman J, Clard J (2001) Cloning and Heterologous Expression of a Natural Product Biosynthetic Gene Cluster from eDNA. Org Lett 3:1981-1984.
10. Bull A. T, Ward AC, Goodfellow M (2000) Search and discovery strategies for biotechnology: the paradigm shift. Microbiol Mol Biol Rev 64:573-606.
11. Castaldo G., Zucko J, Heidelberger S, Vujaklija D, Hranueli D, Cullum J., Wattana-Amorn P, Crump MP, Crosby J, Long PF (2008) Proposed Arrangement of Proteins Forming a Bacterial Type II Polyketide Synthase. Chem Biol 15:1156-1165.
12. Charter K. F (1993) Genetics of differentiation in Streptomyces. Annu Rev Microbiol 47:685-713.
13. Charusanti P., Fong NL, Nagarajan H, Pereira AR, Li HJ, Abate EA, Su Y, Gerwick WH, Palsson BO (2012) Exploiting Adaptive Laboratory Evolution of Streptomyces clavuligerus for Antibiotic Discovery and Overproduction. PLoS ONE 7:e33727(1-12).
14. Committee On Metagenomics, Board of Life Sciences (2007) The New Science of Metagenomics Revealing the Secrets of Our Microbial Planet. The National Academies Press, Washington, DC.
15. Courtois S., Cappellano CM, Ball M, Francou F-X, Normand P, Helynck G., Martinez A, Kolvek SJ, Hopke J, Osburne MS, August P. R, Nalin R, Guérineau M, Jeannin P, Simonet P, Pernodet J-L (2003) Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl Environ Microbiol 6:49-55.
16. Cowan D., Meyer Q, Stafford W, Muyanga S, Cameron R, Wittwer P. (2005) Metagenomic gene discovery: past, present and future. Trends Biotechnol 23:321-329.
17. D'Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD (2011) Antibiotic resistance is ancient. Nature 477:457-461.
18. Da Silveira NJF, Uchôa HB, Pereira JH, Canduri F, Basso LA, Palma M. S, Santos DS, Azevedo jr WF (2005) Molecular models of protein targets from Mycobacterium tuberculosis. J Mol Model 11:160-166.
19. Demain A. L, Sanchez S (2009) Microbial drug discovery: 80 years of progress. J Antibiot(Tokyo) 62:5-16.
20. Embrapa (2007) O programa Blast: Guia prático de utilização. Embrapa Recursos Genéticos e Biotecnologia. Brasília, DF, Brazil.
21. Ewing B., Green P (1998) Base-calling of automated sequencer traces using Phred II Error probabilities. Genome Res 8:186-194.
22. Ewing B., Hilier LD, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using Phred I Accuracy assessment. Genome Res 8:175-185.
23. Feng Z., Kallifidas D, Brady SF (2011) Functional analysis of environmental DNA-derived type II polyketide synthases reveals structurally diverse secondary metabolites. Proc Natl Acad Sci USA 108:12629-12634.
24. Feng Z., Kim JH, Brady SF (2010) Fluostatins produced by the heterologous expression of a TAR reassembled environmental DNA derived type II PKS gene cluster. J Am Chem Soc 132:11902-11903.
25. Fernandez-Moreno MA, Caballero JL, Hopwood DA, Malpartida F (1991) The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces. Cell 66:769-780.
26. Fischbach M. A, Walsh CT, Lardy J (2008) The evolution of gene collectives: How natural selection drives chemical innovation. Proc Natl Acad Sci (USA) 105:4601-4608.
27. Fischbach M. A, Walsh CT (2009) Antibiotics for Emerging Pathogens. Science, 325:1089-1093.
28. Fischer A., Enkler N, Neudert G, Bocola M, Sterner R, Merkl R (2009) TransCent: computational enzyme design by transferring active sites and considering constraints relevant for catalysis. BMC Bioinformatics 10:54.
29. Fu J., Wenzel SC, Perlova O, Wang J, Gross F, Tang Z, Yin Y, Stewart A. F, Muller R, Zhang Y (2008) Efficient transfer of two large secondary metabolite pathway gene clusters into heterologous hosts by transposition. Nucleic Acids Res, 36:(e113)1-14.
30. Ginolhac A., Jarrin C, Gillet B, Robe P, Pujic P, Tuphile K, Bertrand H., Vogel TM, Perrière G, Simonet P, Nalin R (2004) Phylogenetic analysis of polyketide synthase I domains from soil metagenomic libraries allows selection of promising clones. Appl Environ Microbiol 70:5522-5527.
31. Gladek A., Zabrzewsk AJ (1984) Genome size of Streptomyces. FEMS Microbiol Lett, 24: 73-6.
32. Gomes, ES (2008) Utilização da metagenômica como ferramenta para prospecção de novos genes do sistema PKS tipo II. Jaboticabal, Brazil, 76p. (Graduation thesis, Faculdade de Ciências Agrárias e Veterinárias, UNESP).
33. Gomes, ES (2011) Análise in silico de um novo "cluster" de PKS II Metagenômico Jaboticabal, Brazil, 118 p (M. Sc Dissertation. Programa de pós-graduação em Microbiologia Agropecuárea, Universidade Estadual Paulista "Júlio de Mesquita Filho". UNESP).
34. Gomes E. S, Navarrete AA, Lemos EGM, Tsai SM, Moreira FMS (2010) A nova ciência da metagenômica: revelando os segredos do planeta microbiano. Boletim informativo da SBCS 34:20-22.
35. Gordon D., Abajian C, Green P (1998) Consed: A graphical tool for sequence finishing. Genome Res 8:195-202.
36. Gustafsson C., Govindarajan S, Minshull J (2004) Codon bias and heterologous protein expression. Trends Biotechnol 22:346-353.
37. Hamad B. (2010) The antibiotics market. Nat Rev Drug Discov 9:675-676.
38. Hopwood D. A (1978) Extrachromosomally determined antibiotic production. Annu Rev Microbiol 32:373-392.
39. Hopwood D. A (1997) Genetic Contribuitions to Understanding Polyketide Syntases. Chem Rev 97:2465-2497.
40. Hopwood D. A (2004) Cracking the polyketide code. Plos Biol 2:(E35)166-169.
41. Hopwood D. A, Charter KF, Bibb MJ (1995) Genetics of antibiotic production in Streptomyces coelicolor A3(2), a model Streptomycete. Biotechnology 28:65-102.
42. Horinouchi S., Beppu T (1992) Autoregulatory factors and communication in actinomycetes. Annu Rev Microbiol 46:377-398.
43. Hsiao N., Kirby R (2008) Comparative genomics of Streptomyces avermitilis, Streptomyces cattleya, Streptomyces maritimus and Kitasatospora aureofaciens using a Streptomyces coelicolor microarray system. Antonie van Leeuwenhoek 93:1-25.
44. Hutchinson C. R (1997) Biosynthetic Studies of Daunorubicin and Tetracenomycin C. Chem Rev 97:2525-2535.
45. Hutchinson C. R, Fujii I (1995) Polyketide synthase gene manipulation: a structure-function approach in engineering novel antibiotics. Annu Rev Microbiol 49:201-238.
46. Iqbal H. A, Feng Z, Brady SF (2012) Biocatalysts and small molecule products from metagenomic studies. Curr Opin Chem Biol 16:109-116.
47. Jenke-Kodama H, Elke Dittmann E (2009) Evolution of metabolic diversity: insights from microbial polyketide synthases. Phytochemistry 70:1858-1866.
48. Kaitin K. (2010) Deconstructing the Drug Development Process: The New Face of Innovation. Clin Pharmacol Ther 87:356-361.
49. Katz L. (2009) The DEBS paradigm for type I modular polyketide synthases and beyond. Methods Enzymol 459:113-142.
50. Keatinge-Clay AT, Shelat AA, Savage DF, Tsai SC, Miercke LJ, O'Connell JD III, Khosla C, Stroud RM (2003) Catalysis, specificity, and ACP docking site of Streptomyces coelicolor malonyl-CoA:ACP trans-acylase. Structure 11:147-154.
51. Kim J. H, Simmons TL, Brady SF (2010) Comprehensive Natural Products I. I, Unlocking Environmental DNA Derived Gene Clusters Using a Metagenomics Approach. Chem Biol 2:455-474.
52. Kinashi H. (2011) Giant linear plasmids in Streptomyces: a treasure trove of antibiotic biosynthetic clusters. J Antibiot (Tokyo) 64:19-25.
53. Kinashi H., Shimaji M, Sakai A (1987) Giant linear plasmids in Streptomyces which code for antibiotic biosynthetic genes. Nature 328:454-56.
54. King R. W, Bauer JD, Brady, SF (2009) An environmental DNAderived type II polyketide biosynthetic pathway encodes the biosynthesis of the pentacyclic polyketide erdacin. Angew Chem 48:6257-6261.
55. Kneller R. (2010) The importance of new companies for drug discovery: origins of a decade of new drugs. Nat Rev Drug Discov 9:867-882.
56. Knight V., Sanglier JJ, DiTullio D, Braccili S, Bonner P, Waters J, Hughes D., Zhang L (2003) Diversifyng microbial natural products for drug discovery. Appl Microbiol Biotechnol 62:446-458.
57. Kvist T., Ahring BK, Lasken RS, Westermann P (2007) Specific single-cell isolation and genomic amplification of uncultured microorganisms. Appl Microbiol Biotechnol 74:926-935.
58. Larkin M. A, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and Clustal X version 20. Bioinformatics 23:2947-2948.
59. Lechevalier H. A, Lechevalier MP (1981) Introduction to the order Actinomycetales. In: Starr, M.P., Stalp, H., Tryper, H.G., Balawi, A., Schlegel, H.G. (eds) Prokaryotes A Handbook on Habitats, Isolation and Identification of Bacteria. Springer, New York, 1915-1922.
60. Liles M. R, Williamson LL, Rodbumrer J, Torsvik V, Goodman RM, Handelsman J (2008) Recovery, purification, and cloning of high molecular-weight DNA from soil microorganisms. Appl Environ Microbiol 74:3302-3305.
61. Lovell S. C, Davis IW, Arendall WB III, Bakker PI, Word JM, Prisant M. G, Richardson JS, Richardson DC (2003) Structure Validation by CVVGeometry: and CaaDeviation. Proteins Struct Funct Genet 50:437-450.
62. Malpartida F., Hopwood DA (1984) Molecular cloning of the whole biosynthetic pathway of a Streptomyces antibiotic and its expression in a heterologous host. Nature 309:462-464.
63. Martin J. F, Demain AL (1980) Control of antibiotic biosyntesis. Microbiol Rev 44:230-251.
64. Massini K. C (2009) Bioprospecção de Genes Biossintéticos de Policetídeos em DNA Metagenômico de Solo de Mata Atlântica São Paulo, Brazil, 114 p (Dr. Sc. Thesis. Instituto de Ciências Biomédicas. USP).
65. McCarthy AJ, Williams ST (1992) Actinomycetes as agents of biodegradation in the environment-a review. Gene 115:189-192.
66. Méndez C., Salas JA (1998) ABC transporters in antibiotic-producing actinomycetes. FEMS Microbiol Lett 158:1-8.
67. Metsä-Ketelä M, Salo V, Halo L, Hautala A, Hakala J, Mäntsälä P, Ylihonko K (1999) An eficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180:1-6.
68. Moffitt M. C, Neilan BA (2003) Evolutionary affiliations within the superfamily of Ketosynthases reflect complex pathway associations. J Mol Evol 56:446-457.
69. Motche M., Dehesh K, Edwards P, Lindqvist Y (2001) The Crystal Structure of S-Ketoacyl-Acyl Carrier Protein Synthase II from Synechocystis sp at 154 Å Resolution and Its Relationship to Other Condensing Enzymes. J Mol Biol 305:491-503.
70. Olano C. (2011) Hutchinson's legacy: keeping on polyketide biosynthesis. J Antibiot (Tokyo) 64:51-57.
71. Omura S., Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H., Shiba T, Sakaki Y, HattoriM(2001) Genome sequence of an industrial Microorganism Streptomyces avermitilis: Deducing the ability of producing secondary metabolites. Proc Natl Acad Sci USA 98:12215-12220.
72. Padilla G. (1998) Biologia molecular de Streptomyces e suas aplicações industriais In: Melo, I.S., Azevedo, J.L.(eds) Ecologia Microbiana, Embrapa, Brazil, 328-347.
73. Peirú S., Rodríguez E, Menzella HG, Carney JR, Gramajo H (2008) Metabolically engineered Escherichia coli for efficient production of glycosylated natural products. Microb Biotechnol 1:476-486.
74. Pereira A. L, Pita JR (2005) Alexander Fleming (1881-1955), Da descoberta da penicilina (1928) ao Prémio Nobel (1945). Revista da Faculdade de Letras: História Porto 6:129-151.
75. Pereira R. M, Silveira EL, Scaquitto DC, Pedrinho EAN, Val-Moraes S. P, Wickert E, Carareto-Alves LM, Lemos EGM (2006) Molecular Characterization of Bacterial Populations of Different Soils. Braz J Microbiol 37:439-447.
76. Piel J. (2011) Approaches to Capturing and Designing Biologically Active Small Molecules Produced by Uncultured Microbes. Annu Rev Microbiol 65:431-453.
77. Prosdocimi F., Cerqueira GC, Binneck E, Silva AF, Reis AN, Junqueira A. CM, Santos ACF, Nhani-Júnior A, Wust CI, Camargo-Filho F, Kessedjian JL, Petretski JH, Camargo LP, Ferreira R. GM, Lima RP, Pereira RM, Jardim S, Sampaio VS, Folgueras-Flatschart AV (2001) Bioinformática: Manual do usuário n. 29, Biotecnologia Ciência & Desenvolvimento, Brasília, Brazil.
78. Quevillon E., Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R., Lopez R (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33:W116-W120.
79. Rajendhran J., Gunasekaran P (2008) Strategies for accessing soil metagenome for desired applications. Biotechnology Advances 26:576-590.
80. Rivero-Muller A, Lajic S, Huhtaniem I (2007) Assisted large fragment insertion by Red/ET-recombination (ALFIRE)-An alternative and enhanced method for large fragment recombineering. Nucleic Acids Res 35/78:(1-8).
81. Rix U., Fischer C, Remsing LL, Rohr J (2002) Modification of post-PKS tailoring steps through combinatorial biosynthesis. Nat Prod Rep 19:542-580.
82. Romero D., Traxler MF, López D, Kolter R (2011) Antibiotics as Signal Molecules. Chem Rev 111:5492-5505.
83. Sambrook J., Russell DW (2001) Molecular cloning: A laboratory manual (3ed), Cold Spring harbor Laboratory, Cold Spring Harbor, New York.
84. Schmieder R., Edwards R (2012) Insights into antibiotic resistance through metagenomic approaches. Future Microbiol 7:73-89.
85. Schuch V. (2007) Prospecção de genes envolvidos na biossíntese de antibióticos através da abordagem metagenômica Jaboticabal, Brazil, 118p (M. Sc. Dissertation. Programa de Pósgraduação em Microbiologia Agropecuárea, Universidade Estadual Paulista "Júlio de Mesquita Filho". UNESP).
86. Shen B. (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7:285-295.
87. Shen B., Shen Y, Yoon P, Yu T-W, Floss HG, Hopwood D, Moore BS (1999) Ectopic expression of the minimal whiE polyketide synthase generates a library of aromatic polyketides of diverse sizes and shapes. Proc Natl Acad Sci USA 96:3622-3627.
88. Silakowski B., Schairer HU, Ehret H, Kunze B, Weinig S, Nordsiek G., Brandt P, Blöcker H, Höfle G, Beyer S, Müller R (1999) New lessons for combinatorial biosynthesis from myxobacteria: the myxothiazol biosynthetic gene cluster of Stigmatella aurantiaca DW4/3-1. J Biol Chem 274:37391-37399.
89. Silveira E. L, Pereira RM, Scaquitto DC, Pedrinho EAN, Val-Moraes S. P, Wickert E, Carareto-Alves LM, Lemos EGM (2006) Bacterial diversity of soil under eucalyptus assessed by 16S rDNA sequencing analysis. Pesq Agropec Bras 41:1507-1516.
90. Sjölander K. (2004) Phylogenomic inference of protein molecular function: advances and challenges Bioinformatics 20:170-179.
91. Smith T. F, WatermanMS(1981) Identification of common molecular subsequences. J Mol Biol 147:95-197.
92. Smolke C. D (2010) The metabolic pathway engineering handbook: Fundamentals (1 ed), CRC Press:Taylor & Francis Group, Boca Raton, FL.
93. Solecka J., Zajko J, Postek M, Rajnisz A (2012) Biologically active secondary metabolites from Actinomycetes. Cent Eur J Biol 7:373-390.
94. Starcevic A., Zucko J, Simunkovic J, Long PF, Cullum J, Hranueli D (2008) ClustScan: An integrated program package for the semi-automatic annotation of modular biosynthetic gene clusters and in silico prediction of novel chemical structures. Nucleic Acids Res 36:6882-6892.
95. Stevens D. C, Henry MR, Murphy KA, Boddy CN (2010) Heterologous Expression Of The Oxytetracycline Biosynthetic Pathway in Myxococcus xanthus. Appl Environ Microbiol 76:2681-2683.
96. Takagi M., Shin-Ya K (2011) New species of actinomycetes do not always produce new compounds with high frequency. J Antibiot (Tokyo) 64:699-701.
97. The Journal of Antibiotics (2011) Special issue of The Journal of Antibiotics dedicated to the late Professor C Richard Hutchinson. J Antibiot (Tokyo) 64:3-5.
98. Tovchigrechko A., Vakser IA (2006) Gramm-X Public Web Server For Protein-Protein Docking. Nucleic Acids Res 34:W310-W314.
99. Val-Moraes SP, Marcondes J, Carareto-Alves LM, Lemos EGM (2011) Impact of sewage sludge on the soil bacterial communities by DNA microarray analysis. World J Microbiol Biotechnol 27:1997-2003.
100. Vidotti C. CF, De Castro LL C, Calil SS (2008) New drugs in Brazil: Do they meet Brazilian public health needs? Rev Panam Salud Publica 24:36-45.
101. Vining L. C (1990) Functions of secondary metabolites. Annu Rev Microbiol 44:395-427.
102. Wadt M. (2003) Análise Econômica de Novos Fármacos Licenciados no Brasil entre 1998 e 2001. São Paulo, Brazil, 236 p. (M. Sc. Dissertation. Faculdade de Ciências Farmacêuticas. USP).
103. Wang G. Y, Graziani E, Waters B, Pan W, Li X, McDermott J, Meurer G., Saxena G, Andersen RJ, Davies J (2000) Novel natural products from soil DNA libraries in a Streptomycete host. Org Lett 2:2401-2404.
104. Weissman K. J (2009) Introduction to polyketide biosynthesis In: Hopwood, D.A. (ed) Complex Enzymes in Microbial Natural Product Biosynthesis, Part B: Polyketides, Aminocoumarins and Carbohydrates Methods in Enzymology, Academic Press, 3-16.
105. Yadav G., Gokhale RS, Mohanty D (2003) SEARCHPKS: a program for detection and analysis of polyketide synthase domains. Nucleic Acids Res 31:3654-3658.
106. Yu T-W, Shen Y, McDaniel R, Floss HG, Khosla C, Hopwood DA, Moore BS (1998) Engineered Biosynthesis of Novel Polyketides from Streptomyces Spore Pigment Polyketide Synthases. J Am Chem Soc 120:7749-7759.
107. Zaehner H., Fieldler HP (1995) The need for new antibiotics: possible ways forward In: Russel, N.J.(ed) Fifty years of antimicrobials: past perspectives and future trends Cambridge University Press, Cambridge, England, 67-84.
108. Zaleta-Rivera K, Charkoudian LK, Ridley CP, Khosla C (2010) Cloning, Sequencing, Heterologous Expression, and Mechanistic Analysis of A-74528 Biosynthesis. J Am Chem Soc 132:9122-9128.