Advertisement

Enhancing Metagenomic Approaches Through Synthetic Biology

  • Luana de Fátima Alves
  • Rafael Silva-Rocha
  • María-Eugenia GuazzaroniEmail author

Abstract

Bioactive compounds and enzymes with tolerance to process-specific parameters or improved catalytic performance play a crucial role in the development of applications in the chemical and pharmaceutical industry or energy production. Metagenomics takes advantage of the wealth of biochemical diversity present in the genomes of microorganisms found in environmental samples and provides a set of new technologies directed toward screening for new genes with potential in biotechnological applications. However, despite the vast number of published successful studies using this approach, metagenomic strategies typically have low rates of target discovery, and a number of issues need to be addressed in order to improve the screening efficiency of metagenomic libraries. Current limitations include biases imposed by expression in foreign host organisms, low vector performance in particular hosts, and the absence of suitable screening strategies for many targets. These restrictions cannot be overcome by using a single approach but rather require the synergetic implementation of multiple methodologies. In this chapter, we review some of the principal constraints regarding the discovery of new genes with potential use in biotechnology in metagenomic libraries and discuss how these might be resolved using synthetic biology methods. In addition, we review the state of art of synthetic biology approaches directed to improve the recovery of target genes in metagenomic screenings.

Keywords

Functional metagenomics Synthetic biology Bioprospecting Biocatalyst discovery 

Notes

Acknowledgments

The study was supported by the National Council of Technological and Scientific Development (CNPq 472893/2013-0 and 441833/2014-4) and by the Sao Paulo State Foundation (FAPESP, grant number 2015/04309-1 and 2012/21922-8). MEG was a beneficiary of a CNPq Young Talent Fellowship (CNPq 370630/2013-0). Authors have no conflict of interest to declare.

References

  1. Ajikumar PK, Tyo K, Carlsen S, Mucha O, Phon TH, Stephanopoulos G (2008) Terpenoids: opportunities for biosynthesis of natural product drugs using engineered microorganisms. Mol Pharm 5(2):167–190. doi: 10.1021/mp700151b PubMedCrossRefGoogle Scholar
  2. Alcaide M, Tornes J, Stogios PJ, Xu X, Gertler C, Di Leo R, Bargiela R, Lafraya A, Guazzaroni ME, Lopez-Cortes N, Chernikova TN, Golyshina OV, Nechitaylo TY, Plumeier I, Pieper DH, Yakimov MM, Savchenko A, Golyshin PN, Ferrer M (2013) Single residues dictate the co-evolution of dual esterases: MCP hydrolases from the alpha/beta hydrolase family. Biochem J 454(1):157–166PubMedCrossRefGoogle Scholar
  3. Angelov A, Mientus M, Liebl S, Liebl W (2009) A two-host fosmid system for functional screening of (meta)genomic libraries from extreme thermophiles. Syst Appl Microbiol 32(3):177–185. doi: 10.1016/j.syapm.2008.01.003 PubMedCrossRefGoogle Scholar
  4. Arkin A (2008) Setting the standard in synthetic biology. Nat Biotechnol 26(7):771–774. doi: 10.1038/nbt0708-771 PubMedCrossRefGoogle Scholar
  5. Banik JJ, Brady SF (2010) Recent application of metagenomic approaches toward the discovery of antimicrobials and other bioactive small molecules. Curr Opin Microbiol 13(5):603–609. doi: 10.1016/j.mib.2010.08.012 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bharate SB, Sawant SD, Singh PP, Vishwakarma RA (2013) Kinase inhibitors of marine origin. Chem Rev 113(8):6761–6815. doi: 10.1021/cr300410v PubMedCrossRefGoogle Scholar
  7. Bhat MK (2000) Cellulases and related enzymes in biotechnology. Biotechnol Adv 18(5):355–383PubMedCrossRefGoogle Scholar
  8. Bhat A, Riyaz-Ul-Hassan S, Ahmad N, Srivastava N, Johri S (2013) Isolation of cold-active, acidic endocellulase from Ladakh soil by functional metagenomics. Extremophiles 17(2):229–239PubMedCrossRefGoogle Scholar
  9. Bhatnagar I, Kim SK (2010) Immense essence of excellence: marine microbial bioactive compounds. Mar Drugs 8(10):2673–2701. doi: 10.3390/md8102673 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Blunt JW, Copp BR, Keyzers RA, Munro MH, Prinsep MR (2015) Marine natural products. Nat Prod Rep 32(2):116–211. doi: 10.1039/c4np00144c PubMedCrossRefGoogle Scholar
  11. Brady SF, Simmons L, Kim JH, Schmidt EW (2009) Metagenomic approaches to natural products from free-living and symbiotic organisms. Nat Prod Rep 26(11):1488–1503. doi: 10.1039/b817078a PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chen HL, Chen YC, Lu MY, Chang JJ, Wang HT, Ke HM, Wang TY, Ruan SK, Wang TY, Hung KY, Cho HY, Lin WT, Shih MC, Li WH (2012) A highly efficient beta-glucosidase from the buffalo rumen fungus Neocallimastix patriciarum W5. Biotechnol Biofuels 5(1):24PubMedPubMedCentralCrossRefGoogle Scholar
  13. Cieslinski H, Bialkowskaa A, Tkaczuk K, Dlugolecka A, Kur J, Turkiewicz M (2009) Identification and molecular modeling of a novel lipase from an Antarctic soil metagenomic library. Pol J Microbiol 58(3):199–204PubMedGoogle Scholar
  14. Craig JW, Chang FY, Kim JH, Obiajulu SC, Brady SF (2010) Expanding small-molecule functional metagenomics through parallel screening of broad-host-range cosmid environmental DNA libraries in diverse proteobacteria. Appl Environ Microbiol 76(5):1633–1641. doi: 10.1128/AEM.02169-09. [pii].PubMedPubMedCentralCrossRefGoogle Scholar
  15. Daniel R (2005) The metagenomics of soil. Nat Rev Microbiol 3(6):470–478PubMedCrossRefGoogle Scholar
  16. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, Furlan M, Desnues C, Haynes M, Li L, McDaniel L, Moran MA, Nelson KE, Nilsson C, Olson R, Paul J, Brito BR, Ruan Y, Swan BK, Stevens R, Valentine DL, Thurber RV, Wegley L, White BA, Rohwer F (2008) Functional metagenomic profiling of nine biomes. Nature 452(7187):629–632PubMedCrossRefGoogle Scholar
  17. Eggeling L, Bott M, Marienhagen J (2015) Novel screening methods-biosensors. Curr Opin Biotechnol 35C:30–36. doi: 10.1016/j.copbio.2014.12.021 CrossRefGoogle Scholar
  18. Feng Y, Duan CJ, Pang H, Mo XC, Wu CF, Yu Y, Hu YL, Wei J, Tang JL, Feng JX (2007) Cloning and identification of novel cellulase genes from uncultured microorganisms in rabbit cecum and characterization of the expressed cellulases. Appl Microbiol Biotechnol 75(2):319–328PubMedCrossRefGoogle Scholar
  19. 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 U S A 108(31):12629–12634. doi: 10.1073/pnas.1103921108 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Fernandez-Arrojo L, Guazzaroni ME, Lopez-Cortes N, Beloqui A, Ferrer M (2010) Metagenomic era for biocatalyst identification. Curr Opin Biotechnol 21(6):725–733PubMedCrossRefGoogle Scholar
  21. Ferrer M, Chernikova TN, Timmis KN, Golyshin PN (2004) Expression of a temperature-sensitive esterase in a novel chaperone-based Escherichia coli strain. Appl Environ Microbiol 70(8):4499–4504. doi: 10.1128/AEM.70.8.4499-4504.2004 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Ferrer M, Golyshina OV, Chernikova TN, Khachane AN, Martins Dos Santos VA, Yakimov MM, Timmis KN, Golyshin PN (2005) Microbial enzymes mined from the Urania deep-sea hypersaline anoxic basin. Chem Biol 12(8):895–904PubMedCrossRefGoogle Scholar
  23. Ferrer M, Beloqui A, Timmis KN, Golyshin PN (2009) Metagenomics for mining new genetic resources of microbial communities. J Mol Microbiol Biotechnol 16(1–2):109–123PubMedCrossRefGoogle Scholar
  24. Gabor EM, Alkema WB, Janssen DB (2004) Quantifying the accessibility of the metagenome by random expression cloning techniques. Environ Microbiol 6(9):879–886. doi: 10.1111/j.1462-2920.2004.00640.x PubMedCrossRefGoogle Scholar
  25. Galvao TC, de Lorenzo V (2006) Transcriptional regulators a la carte: engineering new effector specificities in bacterial regulatory proteins. Curr Opin Biotechnol 17(1):34–42PubMedCrossRefGoogle Scholar
  26. Gardner TS, Cantor CR, Collins JJ (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403(6767):339–342PubMedCrossRefGoogle Scholar
  27. Gloux K, Berteau O, El Oumami H, Beguet F, Leclerc M, Dore J (2010) A metagenomic beta-glucuronidase uncovers a core adaptive function of the human intestinal microbiome. Proc Natl Acad Sci U S A 108(Suppl 1):4539–4546PubMedPubMedCentralGoogle Scholar
  28. Gong JS, Lu ZM, Li H, Zhou ZM, Shi JS, Xu ZH (2013) Metagenomic technology and genome mining: emerging areas for exploring novel nitrilases. Appl Microbiol Biotechnol 97(15):6603–6611PubMedCrossRefGoogle Scholar
  29. Guazzaroni M-E, Golyshin PN, Ferrer M (2010a) Analysis of complex microbial communities through metagenomic survey. In: Marco D (ed) Metagenomics: theory, methods and applications. Caister Academic, Norfolk, pp 55–77Google Scholar
  30. Guazzaroni ME, Beloqui A, Vieites JM, Al-ramahi Y, Cortes NL, Ghazi A, Golyshin PN, Ferrer M (2010b) Metagenomic mining of enzyme diversity. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2911–2927. doi: 10.1007/978-3-540-77587-4_216 CrossRefGoogle Scholar
  31. Guazzaroni ME, Morgante V, Mirete S, Gonzalez-Pastor JE (2013) Novel acid resistance genes from the metagenome of the Tinto River, an extremely acidic environment. Environ Microbiol 15(4):1088–1102PubMedCrossRefGoogle Scholar
  32. Hallin PF, Binnewies TT, Ussery DW (2008) The genome BLASTatlas-a GeneWiz extension for visualization of whole-genome homology. Mol Biosyst 4(5):363–371PubMedCrossRefGoogle Scholar
  33. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68(4):669–685PubMedPubMedCentralCrossRefGoogle Scholar
  34. Heath C, Hu XP, Cary SC, Cowan D (2009) Identification of a novel alkaliphilic esterase active at low temperatures by screening a metagenomic library from Antarctic desert soil. Appl Environ Microbiol 75(13):4657–4659PubMedPubMedCentralCrossRefGoogle Scholar
  35. Herrera S (2004) Industrial biotechnology-a chance at redemption. Nat Biotechnol 22(6):671–675PubMedCrossRefGoogle Scholar
  36. Homann MJ, Vail RB, Previte E, Tamarez M, Morgan B, Dodds DR, Zaks A (2004) Rapid identification of enantioselective ketone reductions using targeted microbial libraries, vol 60. Elsevier. First publishedGoogle Scholar
  37. Houssen WE, Jaspars M (2012) Isolation of marine natural products. Methods Mol Biol 864:367–392. doi: 10.1007/978-1-61779-624-1_14 PubMedCrossRefGoogle Scholar
  38. Hu XP, Heath C, Taylor MP, Tuffin M, Cowan D (2012) A novel, extremely alkaliphilic and cold-active esterase from Antarctic desert soil. Extremophiles 16(1):79–86PubMedCrossRefGoogle Scholar
  39. Jackson SA, Borchert E, O’Gara F, Dobson AD (2015) Metagenomics for the discovery of novel biosurfactants of environmental interest from marine ecosystems. Curr Opin Biotechnol 33:176–182. doi: 10.1016/j.copbio.2015.03.004 PubMedCrossRefGoogle Scholar
  40. Jiang C, Ma G, Li S, Hu T, Che Z, Shen P, Yan B, Wu B (2009) Characterization of a novel beta-glucosidase-like activity from a soil metagenome. J Microbiol 47(5):542–548PubMedCrossRefGoogle Scholar
  41. Jiang C, Yin B, Tang M, Zhao G, He J, Shen P, Wu B (2013) Identification of a metagenome-derived prephenate dehydrogenase gene from an alkaline-polluted soil microorganism. Antonie Van Leeuwenhoek 103(6):1209–1219PubMedCrossRefGoogle Scholar
  42. Kirk O, Borchert TV, Fuglsang CC (2002) Industrial enzyme applications. Curr Opin Biotechnol 13(4):345–351PubMedCrossRefGoogle Scholar
  43. Ko KC, Han Y, Cheong DE, Choi JH, Song JJ (2013) Strategy for screening metagenomic resources for exocellulase activity using a robotic, high-throughput screening system. J Microbiol Methods 94(3):311–316PubMedCrossRefGoogle Scholar
  44. Koide T, Pang WL, Baliga NS (2009) The role of predictive modelling in rationally re-engineering biological systems. Nat Rev Microbiol 7(4):297–305. doi: 10.1038/nrmicro2107 PubMedPubMedCentralGoogle Scholar
  45. Krogh KB, Harris PV, Olsen CL, Johansen KS, Hojer-Pedersen J, Borjesson J, Olsson L (2010) Characterization and kinetic analysis of a thermostable GH3 beta-glucosidase from Penicillium brasilianum. Appl Microbiol Biotechnol 86(1):143–154PubMedCrossRefGoogle Scholar
  46. Leis B, Angelov A, Li H, Liebl W (2014) Genetic analysis of lipolytic activities in Thermus thermophilus HB27. J Biotechnol 191:150–157. doi: 10.1016/j.jbiotec.2014.07.448 PubMedCrossRefGoogle Scholar
  47. Leis B, Angelov A, Mientus M, Li H, Pham VT, Lauinger B, Bongen P, Pietruszka J, Goncalves LG, Santos H, Liebl W (2015) Identification of novel esterase-active enzymes from hot environments by use of the host bacterium Thermus thermophilus. Front Microbiol 6:275. doi: 10.3389/fmicb.2015.00275 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Lorenz P, Eck J (2005) Metagenomics and industrial applications. Nat Rev Microbiol 3(6):510–516PubMedCrossRefGoogle Scholar
  49. Lorenz P, Liebeton K, Niehaus F, Eck J (2002) Screening for novel enzymes for biocatalytic processes: accessing the metagenome as a resource of novel functional sequence space. Curr Opin Biotechnol 13(6):572–577PubMedCrossRefGoogle Scholar
  50. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66(3):506–577PubMedPubMedCentralCrossRefGoogle Scholar
  51. Martinez-Garcia E, Nikel PI, Chavarria M, de Lorenzo V (2014) The metabolic cost of flagellar motion in Pseudomonas putida KT2440. Environ Microbiol 16(1):291–303. doi: 10.1111/1462-2920.12309 PubMedCrossRefGoogle Scholar
  52. Martinez-Martinez M, Alcaide M, Tchigvintsev A, Reva O, Polaina J, Bargiela R, Guazzaroni ME, Chicote A, Canet A, Valero F, Rico Eguizabal E, Guerrero Mdel C, Yakunin AF, Ferrer M (2013) Biochemical diversity of carboxyl esterases and lipases from Lake Arreo (Spain): a metagenomic approach. Appl Environ Microbiol 79(12):3553–3562PubMedPubMedCentralCrossRefGoogle Scholar
  53. Martinez-Martinez M, Lores I, Pena-Garcia C, Bargiela R, Reyes-Duarte D, Guazzaroni ME, Pelaez AI, Sanchez J, Ferrer M (2014) Biochemical studies on a versatile esterase that is most catalytically active with polyaromatic esters. Microb Biotechnol 7(2):184–191PubMedPubMedCentralCrossRefGoogle Scholar
  54. Maurer KH (2004) Detergent proteases. Curr Opin Biotechnol 15(4):330–334PubMedCrossRefGoogle Scholar
  55. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R (2005) The microbial pan-genome. Curr Opin Genet Dev 15(6):589–594. doi: 10.1016/j.gde.2005.09.006 PubMedCrossRefGoogle Scholar
  56. Mohn WW, Garmendia J, Galvao TC, de Lorenzo V (2006) Surveying biotransformations with a la carte genetic traps: translating dehydrochlorination of lindane (gamma-hexachlorocyclohexane) into lacZ-based phenotypes. Environ Microbiol 8(3):546–555. doi: 10.1111/j.1462-2920.2006.00983.x PubMedCrossRefGoogle Scholar
  57. Moon TS, Clarke EJ, Groban ES, Tamsir A, Clark RM, Eames M, Kortemme T, Voigt CA (2011) Construction of a genetic multiplexer to toggle between chemosensory pathways in Escherichia coli. J Mol Biol 406(2):215–227. doi: 10.1016/j.jmb.2010.12.019 PubMedCrossRefGoogle Scholar
  58. Morimoto S, Fujii T (2009) A new approach to retrieve full lengths of functional genes from soil by PCR-DGGE and metagenome walking. Appl Microbiol Biotechnol 83(2):389–396PubMedCrossRefGoogle Scholar
  59. Nasuno E, Kimura N, Fujita MJ, Nakatsu CH, Kamagata Y, Hanada S (2012) Phylogenetically novel LuxI/LuxR-type quorum sensing systems isolated using a metagenomic approach. Appl Environ Microbiol 78(22):8067–8074PubMedPubMedCentralCrossRefGoogle Scholar
  60. Nikel PI, de Lorenzo V (2013) Implantation of unmarked regulatory and metabolic modules in Gram-negative bacteria with specialised mini-transposon delivery vectors. J Biotechnol 163(2):143–154. doi: 10.1016/j.jbiotec.2012.05.002 PubMedCrossRefGoogle Scholar
  61. Osterberg S, del Peso-Santos T, Shingler V (2011) Regulation of alternative sigma factor use. Annu Rev Microbiol 65:37–55. doi: 10.1146/annurev.micro.112408.134219 PubMedCrossRefGoogle Scholar
  62. Otte KB, Hauer B (2015) Enzyme engineering in the context of novel pathways and products. Curr Opin Biotechnol 35C:16–22. doi: 10.1016/j.copbio.2014.12.011 CrossRefGoogle Scholar
  63. Percival Zhang YH, Himmel ME, Mielenz JR (2006) Outlook for cellulase improvement: screening and selection strategies. Biotechnol Adv 24(5):452–481PubMedCrossRefGoogle Scholar
  64. Posfai G, Plunkett G 3rd, Feher T, Frisch D, Keil GM, Umenhoffer K, Kolisnychenko V, Stahl B, Sharma SS, de Arruda M, Burland V, Harcum SW, Blattner FR (2006) Emergent properties of reduced-genome Escherichia coli. Science 312(5776):1044–1046. doi: 10.1126/science.1126439 PubMedCrossRefGoogle Scholar
  65. Purnick PE, Weiss R (2009) The second wave of synthetic biology: from modules to systems. Nat Rev Mol Cell Biol 10(6):410–422PubMedCrossRefGoogle Scholar
  66. Regot S, Macia J, Conde N, Furukawa K, Kjellen J, Peeters T, Hohmann S, de Nadal E, Posas F, Sole R (2011) Distributed biological computation with multicellular engineered networks. Nature 469(7329):207–211. doi: 10.1038/nature09679 PubMedCrossRefGoogle Scholar
  67. Rhee JK, Ahn DG, Kim YG, Oh JW (2005) New thermophilic and thermostable esterase with sequence similarity to the hormone-sensitive lipase family, cloned from a metagenomic library. Appl Environ Microbiol 71(2):817–825PubMedPubMedCentralCrossRefGoogle Scholar
  68. Rhodius VA, Segall-Shapiro TH, Sharon BD, Ghodasara A, Orlova E, Tabakh H, Burkhardt DH, Clancy K, Peterson TC, Gross CA, Voigt CA (2013) Design of orthogonal genetic switches based on a crosstalk map of sigmas, anti-sigmas, and promoters. Mol Syst Biol 9:702. doi: 10.1038/msb.2013.58 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Robertson DE, Chaplin JA, DeSantis G, Podar M, Madden M, Chi E, Richardson T, Milan A, Miller M, Weiner DP, Wong K, McQuaid J, Farwell B, Preston LA, Tan X, Snead MA, Keller M, Mathur E, Kretz PL, Burk MJ, Short JM (2004) Exploring nitrilase sequence space for enantioselective catalysis. Appl Environ Microbiol 70(4):2429–2436PubMedPubMedCentralCrossRefGoogle Scholar
  70. Rocha-Martin J, Harrington C, Dobson AD, O’Gara F (2014) Emerging strategies and integrated systems microbiology technologies for biodiscovery of marine bioactive compounds. Mar Drugs 12(6):3516–3559. doi: 10.3390/md12063516 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Schloss PD, Handelsman J (2003) Biotechnological prospects from metagenomics. Curr Opin Biotechnol 14(3):303–310PubMedCrossRefGoogle Scholar
  72. Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2(7):e92PubMedPubMedCentralCrossRefGoogle Scholar
  73. Schmidt M, de Lorenzo V (2012) Synthetic constructs in/for the environment: managing the interplay between natural and engineered Biology. FEBS Lett 586(15):2199–2206. doi: 10.1016/j.febslet.2012.02.022 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Schnoes AM, Brown SD, Dodevski I, Babbitt PC (2009) Annotation error in public databases: misannotation of molecular function in enzyme superfamilies. PLoS Comput Biol 5(12):e1000605PubMedPubMedCentralCrossRefGoogle Scholar
  75. Shetty RP, Endy D, Knight TF Jr (2008) Engineering BioBrick vectors from BioBrick parts. J Biol Eng 2:5. doi: 10.1186/1754-1611-2-5 PubMedPubMedCentralCrossRefGoogle Scholar
  76. Silva-Rocha R, de Lorenzo V (2011) Implementing an OR-NOT (ORN) logic gate with components of the SOS regulatory network of Escherichia coli. Mol Biosyst 7(8):2389–2396. doi: 10.1039/c1mb05094j PubMedCrossRefGoogle Scholar
  77. Silva-Rocha R, Martinez-Garcia E, Calles B, Chavarria M, Arce-Rodriguez A, de Las Heras A, Paez-Espino AD, Durante-Rodriguez G, Kim J, Nikel PI, Platero R, de Lorenzo V (2013) The Standard European Vector Architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes. Nucleic Acids Res 41(Database issue):D666–D675. doi: 10.1093/nar/gks1119 PubMedCrossRefGoogle Scholar
  78. Simon C, Herath J, Rockstroh S, Daniel R (2009) Rapid identification of genes encoding DNA polymerases by function-based screening of metagenomic libraries derived from glacial ice. Appl Environ Microbiol 75(9):2964–2968PubMedPubMedCentralCrossRefGoogle Scholar
  79. Singhania RR, Patel AK, Sukumaran RK, Larroche C, Pandey A (2013) Role and significance of beta-glucosidases in the hydrolysis of cellulose for bioethanol production. Bioresour Technol 127:500–507PubMedCrossRefGoogle Scholar
  80. Siuti P, Yazbek J, Lu TK (2013) Synthetic circuits integrating logic and memory in living cells. Nat Biotechnol 31(5):448–452. doi: 10.1038/nbt.2510 PubMedCrossRefGoogle Scholar
  81. Sleator RD, Shortall C, Hill C (2008) Metagenomics. Lett Appl Microbiol 47(5):361–366PubMedCrossRefGoogle Scholar
  82. Steele HL, Jaeger KE, Daniel R, Streit WR (2009) Advances in recovery of novel biocatalysts from metagenomes. J Mol Microbiol Biotechnol 16(1–2):25–37PubMedCrossRefGoogle Scholar
  83. Strachan CR, Singh R, VanInsberghe D, Ievdokymenko K, Budwill K, Mohn WW, Eltis LD, Hallam SJ (2014) Metagenomic scaffolds enable combinatorial lignin transformation. Proc Natl Acad Sci U S A 111(28):10143–10148. doi: 10.1073/pnas.1401631111 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Sul WJ, Park J, Quensen JF 3rd, Rodrigues JL, Seliger L, Tsoi TV, Zylstra GJ, Tiedje JM (2009) DNA-stable isotope probing integrated with metagenomics for retrieval of biphenyl dioxygenase genes from polychlorinated biphenyl-contaminated river sediment. Appl Environ Microbiol 75(17):5501–5506PubMedPubMedCentralCrossRefGoogle Scholar
  85. Tabor S (2001) Expression using the T7 RNA polymerase/promoter system. In: Current protocols in molecular biology. Wiley. doi: 10.1002/0471142727.mb1602s11
  86. Tang SY, Cirino PC (2011) Design and application of a mevalonate-responsive regulatory protein. Angew Chem Int Ed Engl 50(5):1084–1086. doi: 10.1002/anie.201006083 PubMedCrossRefGoogle Scholar
  87. Terron-Gonzalez L, Medina C, Limon-Mortes MC, Santero E (2013) Heterologous viral expression systems in fosmid vectors increase the functional analysis potential of metagenomic libraries. Sci Rep 3:1107. doi: 10.1038/srep01107 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Trincone A (2011) Marine biocatalysts: enzymatic features and applications. Mar Drugs 9(4):478–499. doi: 10.3390/md9040478 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Uchiyama T, Miyazaki K (2009) Functional metagenomics for enzyme discovery: challenges to efficient screening. Curr Opin Biotechnol 20(6):616–622. doi: 10.1016/j.copbio.2009.09.010 PubMedCrossRefGoogle Scholar
  90. Uchiyama T, Miyazaki K (2010) Product-induced gene expression, a product-responsive reporter assay used to screen metagenomic libraries for enzyme-encoding genes. Appl Environ Microbiol 76(21):7029–7035PubMedPubMedCentralCrossRefGoogle Scholar
  91. Uchiyama T, Watanabe K (2008) Substrate-induced gene expression (SIGEX) screening of metagenome libraries. Nat Protoc 3(7):1202–1212PubMedCrossRefGoogle Scholar
  92. 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(1):88–93PubMedCrossRefGoogle Scholar
  93. Varaljay VA, Howard EC, Sun S, Moran MA (2010) Deep sequencing of a dimethylsulfoniopropionate-degrading gene (dmdA) by using PCR primer pairs designed on the basis of marine metagenomic data. Appl Environ Microbiol 76(2):609–617PubMedCrossRefGoogle Scholar
  94. Vieites JM, Guazzaroni ME, Beloqui A, Golyshin PN, Ferrer M (2009) Metagenomics approaches in systems microbiology. FEMS Microbiol Rev 33(1):236–255PubMedCrossRefGoogle Scholar
  95. Voigt CA (2006) Genetic parts to program bacteria. Curr Opin Biotechnol 17(5):548–557. doi: 10.1016/j.copbio.2006.09.001 PubMedCrossRefGoogle Scholar
  96. Wang GY, 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(16):2401–2404PubMedCrossRefGoogle Scholar
  97. Ward R (2011) Cellulase engineering for biomass saccharification. In: Buckeridge MS, Goldman GH (eds) Routes to cellulosic ethanol. Springer, New York, pp 135–151. doi: 10.1007/978-0-387-92740-4_9 CrossRefGoogle Scholar
  98. Warnecke F, Hess M (2009) A perspective: metatranscriptomics as a tool for the discovery of novel biocatalysts. J Biotechnol 142(1):91–95PubMedCrossRefGoogle Scholar
  99. Weber W, Fussenegger M (2010) Synthetic gene networks in mammalian cells. Curr Opin Biotechnol 21(5):690–696PubMedCrossRefGoogle Scholar
  100. Wexler M, Bond PL, Richardson DJ, Johnston AW (2005) A wide host-range metagenomic library from a waste water treatment plant yields a novel alcohol/aldehyde dehydrogenase. Environ Microbiol 7(12):1917–1926PubMedCrossRefGoogle Scholar
  101. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 95(12):6578–6583PubMedPubMedCentralCrossRefGoogle Scholar
  102. 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(10):6335–6344PubMedPubMedCentralCrossRefGoogle Scholar
  103. Yan X, Geng A, Zhang J, Wei Y, Zhang L, Qian C, Wang Q, Wang S, Zhou Z (2013) Discovery of (hemi-) cellulase genes in a metagenomic library from a biogas digester using 454 pyrosequencing. Appl Microbiol Biotechnol 97(18):8173–8182PubMedCrossRefGoogle Scholar
  104. Yuhong Z, Shi P, Liu W, Meng K, Bai Y, Wang G, Zhan Z, Yao B (2009) Lipase diversity in glacier soil based on analysis of metagenomic DNA fragments and cell culture. J Microbiol Biotechnol 19(9):888–897PubMedCrossRefGoogle Scholar
  105. Zaprasis A, Liu YJ, Liu SJ, Drake HL, Horn MA (2010) Abundance of novel and diverse tfdA-like genes, encoding putative phenoxyalkanoic acid herbicide-degrading dioxygenases, in soil. Appl Environ Microbiol 76(1):119–128PubMedCrossRefGoogle Scholar
  106. Zelcbuch L, Antonovsky N, Bar-Even A, Levin-Karp A, Barenholz U, Dayagi M, Liebermeister W, Flamholz A, Noor E, Amram S, Brandis A, Bareia T, Yofe I, Jubran H, Milo R (2013) Spanning high-dimensional expression space using ribosome-binding site combinatorics. Nucleic Acids Res 41(9):e98PubMedPubMedCentralCrossRefGoogle Scholar
  107. Zhan J, Ding B, Ma R, Ma X, Su X, Zhao Y, Liu Z, Wu J, Liu H (2010) Develop reusable and combinable designs for transcriptional logic gates. Mol Syst Biol 6:388. doi: 10.1038/msb.2010.42 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Luana de Fátima Alves
    • 1
  • Rafael Silva-Rocha
    • 2
  • María-Eugenia Guazzaroni
    • 1
    Email author
  1. 1.Departamento de BioquimicaFMRP-University of São PauloRibeirão PretoBrazil
  2. 2.Departamento de Biologia CelularFMRP—University of São PauloRibeirão PretoBrazil

Personalised recommendations