Functional screening of metagenome and genome libraries for detection of novel flavonoid-modifying enzymes

Applied and Environmental Microbiology

Volumn 79, Issue 15, 2013, Pages 4551-4563

  Rabausch, U ^a   Juergensen, J ^a   Ilmberger, N ^a   Bohnke S ^a   Fischer, S ^b   Schubach, B ^b   Schulte, M ^b   Streit, W V ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

^b MERCK KGAA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; BACILLUS THURINGIENSIS; FUNCTIONAL SCREENING; GENOME LIBRARIES; GLYCOSYL TRANSFERASE; HIGH PERFORMANCE THIN LAYER CHROMATOGRAPHY; SCREENING METHODS; SCREENING PROCEDURES;

AMINO ACIDS; BACTERIOLOGY; CHROMATOGRAPHY; CLONING; ENZYMES; GENES; LIBRARIES; MOLECULES;

FLAVONOIDS;

BACTERIAL DNA; FLAVONOID;

AMINO ACID; BACTERIUM; CLONE; ENZYME ACTIVITY; GENOME; MODEL VALIDATION; SECONDARY METABOLITE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; BACTERIUM; DNA SEQUENCE; EVALUATION; GENE LIBRARY; GENETICS; METABOLISM; METAGENOME; METHODOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; THIN LAYER CHROMATOGRAPHY;

AMINO ACID SEQUENCE; BACTERIA; CHROMATOGRAPHY, THIN LAYER; CLONING, MOLECULAR; DNA, BACTERIAL; FLAVONOIDS; GENOME, BACTERIAL; GENOMIC LIBRARY; METAGENOME; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

EID: 84880651118     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01077-13     Document Type: Article

References (74)

1. Perner M, Ilmberger N, Köhler HU, Chow J, Streit WR. 2011. Emerging fields in functional metagenomics and its industrial relevance: overcoming limitations and redirecting the search for sovel biocatalysts, p 483-498. Inde Bruijn FJ (ed), Handbook of molecular microbial ecology II: metagenomics in different habitats. John Wiley & Sons, Inc., Hoboken, NJ.
2. Schmeisser C, Steele H, Streit WR. 2007. Metagenomics, biotechnology with non-culturable microbes. Appl. Microbiol. Biotechnol. 75:955-962.
3. Iqbal HA, Feng Z, Brady SF. 2012. Biocatalysts and small molecule products from metagenomic studies. Curr. Opin. Chem. Biol. 16:109-116.
4. Simon C, Daniel R. 2011. Metagenomic analyses: past and future trends. Appl. Environ. Microbiol. 77:1153-1161.
5. Daniel R. 2005. The metagenomics of soil. Nat. Rev. Microbiol. 3:470-478.
6. Streit WR, Daniel R, Jaeger K-E. 2004. Prospecting for biocatalysts and drugs in the genomes of non-cultured microorganisms. Curr. Opin. Biotechnol. 15:285-290.
7. Warren RL, Freeman JD, Levesque RC, Smailus DE, Flibotte S, Holt RA. 2008. Transcription of foreign DNA in Escherichia coli. Genome Res. 18:1798-1805.
8. Uchiyama T, Miyazaki K. 2009. Functional metagenomics for enzyme discovery: challenges to efficient screening. Curr. Opin. Biotech. 20:616-622.
9. Ferrer M, Beloqui A, Timmis KN, Golyshin PN. 2009. Metagenomics for mining new genetic resources of microbial communities. J. Mol. Microbiol. Biotechnol. 16:109-123.
10. Tuffin M, Anderson D, Heath C, Cowan DA. 2009. Metagenomic gene discovery: how far have we moved into novel sequence space? Biotechnol. J. 4:1671-1683.
11. Simon C, Daniel R. 2009. Achievements and new knowledge unraveled by metagenomic approaches. Appl. Microbiol. Biotechnol. 85:265-276.
12. Steele HL, Jaeger KE, Daniel R, Streit WR. 2009. Advances in recovery of novel biocatalysts from metagenomes. J. Mol. Microbiol. Biotechnol. 16: 25-37.
13. Taupp M, Mewis K, Hallam SJ. 2011. The art and design of functional metagenomic screens. Curr. Opin. Biotechnol. 22:465-472.
14. Beloqui A, Pita M, Polaina J, Martinez-Arias A, Golyshina OV, Zumarraga M, Yakimov MM, Garcia-Arellano H, Alcalde M, Fernandez VM, Elborough K, Andreu JM, Ballesteros A, Plou FJ, Timmis KN, Ferrer M, Golyshin PN. 2006. Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: biochemical properties, structural analysis, and phylogenetic relationships. J. Biol. Chem. 281:22933-22942.
15. Collier AC, Tingle MD, Keelan JA, Paxton JW, Mitchell MD. 2000. A highly sensitive fluorescent microplate method for the determination of UDP-glucuronosyl transferase activity in tissues and placental cell lines. Drug Metab. Dispos. 28:1184-1186.
16. DeSantis G, Zhu Z, Greenberg WA, Wong K, Chaplin J, Hanson SR, Farwell B, Nicholson LW, Rand CL, Weiner DP, Robertson DE, Burk MJ. 2002. An enzyme library approach to biocatalysis: development of nitrilases for enantioselective production of carboxylic acid derivatives. J. Am. Chem. Soc. 124:9024-9025.
17. Knietsch A, Waschkowitz T, Bowien S, Henne A, Daniel R. 2003. Metagenomes of complex microbial consortia derived from different soils as sources for novel genes conferring formation of carbonyls from shortchain polyols on Escherichia coli. J. Mol. Microbiol. Biotechnol. 5:46-56.
18. Schipper C, Hornung C, Bijtenhoorn P, Quitschau M, Grond S, Streit WR. 2009. Metagenome-derived clones encoding two novel lactonase family proteins involved in biofilm inhibition in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 75:224-233.
19. Uchiyama T, Abe T, Ikemura T, Watanabe K. 2005. Substrate-induced gene-expression screening of environmental metagenome libraries for isolation of catabolic genes. Nat. Biotechnol. 23:88-93.
20. Williamson LL, Borlee BR, Schloss PD, Guan C, Allen HK, Handelsman J. 2005. Intracellular screen to identify metagenomic clones that induce or inhibit a quorum-sensing biosensor. Appl. Environ. Microbiol. 71:6335-6344.
21. Ververidis F, Trantas E, Douglas C, Vollmer G, Kretzschmar G, Panopoulos N. 2007. Biotechnology of flavonoids and other phenylpropanoidderived natural products. Part II: reconstruction of multienzyme pathways in plants and microbes. Biotechnol. J. 2:1235-1249.
22. Schütz K, Muks E, Carle R, Schieber A. 2006. Quantitative determination of phenolic compounds in artichoke-based dietary supplements and pharmaceuticals by high-performance liquid chromatography. J. Agric. Food Chem. 54:8812-8817.
23. Leonard E, Yan Y, Fowler ZL, Li Z, Lim CG, Lim KH, Koffas MA. 2008. Strain improvement of recombinant Escherichia colifor efficient production of plant flavonoids. Mol. Pharm. 5:257-265.
24. Wang M, Liang CP, Wu QL, Simon JE, Ho CT (ed.). 2006. Instrumental analysis of popular botanical products in the U.S. market, p. 25-38. InHerbs: challenges in chemistry and biology. American Chemical Society, Washington, DC.
25. Manach C, Scalbert A, Morand C, Remesy C, Jimenez L. 2004. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79:727-747.
26. Das S, Rosazza JP. 2006. Microbial and enzymatic transformations of flavonoids. J. Nat. Prod. 69:499-508.
27. Graefe EU, Wittig J, Mueller S, Riethling AK, Uehleke B, Drewelow B, Pforte H, Jacobasch G, Derendorf H, Veit M. 2001. Pharmacokinetics and bioavailability of quercetin glycosides in humans. J. Clin. Pharmacol. 41:492-499.
28. Kren V, Martinkova L. 2001. Glycosides in medicine: the role of glycosidic residue in biological activity. Curr. Med. Chem. 8:1303-1328.
29. Coutinho PM, Deleury E, Davies GJ, Henrissat B. 2003. An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328: 307-317.
30. Bowles D, Lim EK, Poppenberger B, Vaistij FE. 2006. Glycosyltransferases of lipophilic small molecules. Annu. Rev. Plant Biol. 57:567-597.
31. Mackenzie PI, Owens IS, Burchell B, Bock KW, Bairoch A, Belanger A, Fournel-Gigleux S, Green M, Hum Iyanagi DWT, Lancet D, Louisot P, Magdalou J, Chowdhury JR, Ritter JK, Schachter H, Tephly TR, Tipton KF, Nebert DW. 1997. The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 7:255-269.
32. Lairson LL, Henrissat B, Davies GJ, Withers SG. 2008. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77: 521-555.
33. Osmani SA, Bak S, Møller BL. 2009. Substrate specificity of plant UDPdependent glycosyltransferases predicted from crystal structures and homology modeling. Phytochemistry 70:325-347.
34. Breton C, Snajdrova L, Jeanneau C, Koca J, Imberty A. 2006. Structures and mechanisms of glycosyltransferases. Glycobiology 16:29R-37R.
35. Yang M, Proctor MR, Bolam DN, Errey JC, Field RA, Gilbert HJ, Davis BG. 2005. Probing the breadth of macrolide glycosyltransferases: in vitroremodeling of a polyketide antibiotic creates active bacterial uptake and enhances potency. J. Am. Chem. Soc. 127:9336-9337.
36. Jeon Y, Kim B, Kim J, Cheong Y, Ahn J-H. 2009. Enzymatic glycosylation of phenolic compounds using BsGT-3. J. Korean Soc. Appl. Biol. Chem. 52:98-101.
37. Rao KV, Weisner NT. 1981. Microbial transformation of quercetin by Bacillus cereus. Appl. Environ. Microbiol. 42:450-452.
38. Kim HJ, Kim BG, Kim JA, Park Y, Lee YJ, Lim Y, Ahn JH. 2007. Glycosylation of flavonoids with E. coliexpressing glycosyltransferase from Xanthomonas campestris. J. Microbiol. Biotechnol. 17:539-542.
39. Zhou J, Bruns MA, Tiedje JM. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62:316-322.
40. Ilmberger N, Meske D, Juergensen J, Schulte M, Barthen P, Rabausch U, Angelov A, Mientus M, Liebl W, Schmitz RA, Streit WR. 2012. Metagenomic cellulases highly tolerant towards the presence of ionic liquids-linking thermostability and halotolerance. Appl. Microbiol. Biotechnol. 95:135-146.
41. Wagner H, Bladt S, Zgainski EM. 1983. Drogenanalyse, Dünnschichtchromatographische Analyse von Arzneidrogen. Springer, Berlin, Germany.
42. Neu R. 1957. Chelate von Diarylborsäuren mit aliphatischen Oxyalkylaminen als Reagenzien für den Nachweis von Oxyphenyl-benzo-ãpyronen. Naturwissenschaften 44:181-182.
43. Tourasse NJ, Helgason E, Oslash OA, Hegna IK, Kolstø AB. 2006. The Bacillus cereusgroup: novel aspects of population structure and genome dynamics. J. Appl. Microbiol. 101:579-593.
44. Tamura K, Peterson PDN, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
45. Li L, Modolo LV, Escamilla-Trevino LL, Achnine L, Dixon RA, Wang X. 2007. Crystal structure of Medicago truncatulaUGT85H2-insights into the structural basis of a multifunctional (iso)flavonoid glycosyltransferase. J. Mol. Biol. 370:951-963.
46. Jones P, Messner B, Nakajima J, Schäffner AR, Saito K. 2003. UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. J. Biol. Chem. 278:43910-43918.
47. Hyung Ko JH, Gyu Kim B, Joong-Hoon A. 2006. Glycosylation of flavonoids with a glycosyltransferase from Bacillus cereus. FEMS Microbiol. Lett. 258:263-268.
48. Jung NR, Joe EJ, Kim BG, Ahn BC, Park JC, Chong Y, Ahn JH. 2010. Change of Bacillus cereusflavonoid O-triglucosyltransferase into flavonoid O-monoglucosyltransferase by error-prone polymerase chain reaction. J. Microbiol. Biotechnol. 20:1393-1396.
49. Ahn BC, Kim BG, Jeon YM, Lee EJ, Lim Y, Ahn JH. 2009. Formation of flavone di-O-glucosides using a glycosyltransferase from Bacillus cereus. J. Microbiol. Biotechnol. 19:387-390.
50. Choi SH, Ryu M, Yoon YJ, Kim DM, Lee EY. 2012. Glycosylation of various flavonoids by recombinant oleandomycin glycosyltransferase from Streptomyces antibioticusin batch and repeated batch modes. Biotechnol. Lett. 34:499-505.
51. Williams GJ, Zhang C, Thorson JS. 2007. Expanding the promiscuity of a natural-product glycosyltransferase by directed evolution. Nat. Chem. Biol. 3:657-662.
52. Hu Y, Walker S. 2002. Remarkable structural similarities between diverse glycosyltransferases. Chem. Biol. 9:1287-1296.
53. Hughes J, Hughes MA. 1994. Multiple secondary plant product UDPglucose glucosyltransferase genes expressed in cassava (Manihot esculentaCrantz) cotyledons. DNA Seq. 5:41-49.
54. Paquette S, Moller BL, Bak S. 2003. On the origin of family 1 plant glycosyltransferases. Phytochemistry 62:399-413.
55. Bolam DN, Roberts S, Proctor MR, Turkenburg JP, Dodson EJ, Martinez-Fleites C, Yang M, Davis BG, Davies GJ, Gilbert HJ. 2007. The crystal structure of two macrolide glycosyltransferases provides a blueprint for host cell antibiotic immunity. Proc. Natl. Acad. Sci. U. S. A. 104:5336-5341.
56. Offen W, Martinez-Fleites C, Yang M, Kiat-Lim E, Davis BG, Tarling CA, Ford CM, Bowles DJ, Davies GJ. 2006. Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J. 25:1396-1405.
57. Mulichak AM, Lu W, Losey HC, Walsh CT, Garavito RM. 2004. Crystal structure of vancosaminyltransferase GtfD from the vancomycin biosynthetic pathway: interactions with acceptor and nucleotide ligands. Biochemistry 43:5170-5180.
58. Lim E-K, Ashford DA, Bowles DJ. 2006. The synthesis of small-molecule rhamnosides through the rational design of a whole-cell biocatalysis system. ChemBioChem 7:1181-1185.
59. Mabry TJ, Markham KR, Thomas MB. 1970. The systematic identification of flavonoids. Springer-Verlag, New York, NY.
60. Gantt RW, GoffRD, Williams GJ, Thorson JS. 2008. Probing the aglycon promiscuity of an engineered glycosyltransferase. Angew. Chem. Int. Ed. Engl. 47:8889-8892.
61. Vogt T, Jones P. 2000. Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci. 5:380-386.
62. Williams GJ, Gantt RW, Thorson JS. 2008. The impact of enzyme engineering upon natural product glycodiversification. Curr. Opin. Chem. Biol. 12:556-564.
63. Yoon JA, Kim BG, Lee WJ, Lim Y, Chong Y, Ahn JH. 2012. Production of a novel quercetin glycoside through metabolic engineering of Escherichia coli. Appl. Environ. Microbiol. 78:4256-4262.
64. Filippini M, Kaech A, Ziegler U, Bagheri HC. 2011. Fibrisoma limigen. nov., sp. nov., a filamentous bacterium isolated from tidal flats. Int. J. Syst. Evol. Microbiol. 61:1418-1424.
65. Lail K, Sikorski J, Saunders E, Lapidus A, Glavina Del Rio T, Copeland A, Tice H, Cheng JF, Lucas S, Nolan M, Bruce D, Goodwin L, Pitluck S, Ivanova N, Mavromatis K, Ovchinnikova G, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Chain P, Brettin T, Detter JC, Schutze A, Rohde M, Tindall BJ, Goker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Chen F. 2010. Complete genome sequence of Spirosoma lingualetype strain (1). Stand. Genomic Sci. 2:176-185.
66. Lang E, Lapidus A, Chertkov O, Brettin T, Detter JC, Han C, Copeland A, Glavina Del Rio T, Nolan M, Chen F, Lucas S, Tice H, Cheng JF, Land M, Hauser L, Chang YJ, Jeffries CD, Kopitz M, Bruce D, Goodwin L, Pitluck S, Ovchinnikova G, Pati A, Ivanova N, Mavrommatis K, Chen A, Palaniappan K, Chain P, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Goker M, Rohde M, Kyrpides NC, Klenk HP. 2009. Complete genome sequence of Dyadobacter fermentanstype strain (NS114). Stand. Genomic Sci. 1:133-140.
67. Chelius MK, Triplett EW. 2000. Dyadobacter fermentansgen. nov., sp. nov., a novel gram-negative bacterium isolated from surface-sterilized Zea maysstems. Int. J. Syst. Evol. Microbiol. 50:751-758.
68. Finster KW, Herbert RA, Lomstein BA. 2009. Spirosoma spitsbergensesp. nov. and Spirosoma luteumsp. nov., isolated from a high Arctic permafrost soil, and emended description of the genus Spirosoma. Int. J. Syst. Evol. Microbiol. 59:839-844.
69. Filippini M, Svercel M, Laczko E, Kaech A, Ziegler U, Bagheri HC. 2008. 2011. Fibrella aestuarinagen. nov., sp. nov., a filamentous bacterium of the family Cytophagaceaeisolated from a tidal flat, and emended description of the genus Rudanella Weon et al. 2008. Int. J. Syst. Evol. Microbiol. 61:184-189.
70. Ha S, Gross B, Walker S. 2001. E. coliMurG: a paradigm for a superfamily of glycosyltransferases. Curr. Drug Targets Infect. Disord. 1:201-213.
71. Samuel G, Reeves P. 2003. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr. Res. 338:2503-2519.
72. Giraud MF, Naismith JH. 2000. The rhamnose pathway. Curr. Opin. Struct. Biol. 10:687-696.
73. Modolo LV, Li L, Pan H, Blount JW, Dixon RA, Wang X. 2009. Crystal structures of glycosyltransferase UGT78G1 reveal the molecular basis for glycosylation and deglycosylation of (iso)flavonoids. J. Mol. Biol. 392: 1292-1302.
74. Shao H, He X, Achnine L, Blount JW, Dixon RA, Wang X. 2005. Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell 17:3141-3154.