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Current Status and Applications of Adaptive Laboratory Evolution in Industrial Microorganisms

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초록

Adaptive laboratory evolution (ALE) is an evolutionary engineering approach in artificial conditions that improves organisms through the imitation of natural evolution. Due to the development of multi-level omics technologies in recent decades, ALE can be performed for various purposes at the laboratory level. This review delineates the basics of the experimental design of ALE based on several ALE studies of industrial microbial strains and updates current strategies combined with progressed metabolic engineering, in silico modeling and automation to maximize the evolution efficiency. Moreover, the review sheds light on the applicability of ALE as a strain development approach that complies with non-recombinant preferences in various food industries. Overall, recent progress in the utilization of ALE for strain development leading to successful industrialization is discussed.

Abstract

Adaptive laboratory evolution (ALE) is an evolutionary engineering approach in artificial conditions that improves organisms through the imitation of natural evolution. Due to the development of multi-level omics technologies in recent decades, ALE can be performed for various purposes at the laboratory level. This review delineates the basics of the experimental design of ALE based on several ALE studies of industrial microbial strains and updates current strategies combined with progressed metabolic engineering, in silico modeling and automation to maximize the evolution efficiency. Moreover, the review sheds light on the applicability of ALE as a strain development approach that complies with non-recombinant preferences in various food industries. Overall, recent progress in the utilization of ALE for strain development leading to successful industrialization is discussed.

참고문헌 (130)

  1. Phaneuf PV, "ALEdb 1.0: a database of mutations from adaptive laboratory evolution experimentation", Nucleic Acids Res., 47, pp.D1164~D1171 (2019)
  2. Shepelin D, "Selecting the best : evolutionary engineering of chemical production in microbes", Genes(Basel), 9, pp.249~ (2018)
  3. Bennett AF, , Microbial experimental evolution, 297, pp.R17~R25 (2009)
  4. Kering KK, "Application of adaptive evolution to improve the stability of bacteriophages during storage", Viruses, 12, pp.E423~ (2020)
  5. Bailey LA, "Determination of Chinese hamster ovary cell line stability and recombinant antibody expression during long-term culture", Biotechnol. Bioeng, 109, pp.2093~2103 (2012)
  6. Cakar ZP, "Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties", FEMS Yeast Res, 12, pp.171~182 (2012)
  7. Stella RG, "Evolutionary engineering of Corynebacterium glutamicum", Biotechnol. J, 14, pp.e1800444~ (2019)
  8. Zhou S, "Functional replacement of the Escherichia coli D-(-)-lactate dehydrogenase gene(ldhA)with the L-(+)-lactate dehydrogenase gene(ldhL)from Pediococcus acidilactici", Appl. Environ. Microbiol, 69, pp.2237~2244 (2003)
  9. Zhu K, "Modification and evolution of Gluconobacter oxydans for enhanced growth and biotransformation capabilities at low glucose concentration", Mol. Biotechnol, 49, pp.56~64 (2011)
  10. Nielsen J, "Systems biology of metabolism", Annu. Rev. Biochem, 86, pp.245~275 (2017)
  11. Ibarra RU, "Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth", Nature, 420, pp.186~189 (2002)
  12. Choe D, "Adaptive laboratory evolution of a genome-reduced Escherichia coli", Nat. Commun, 10, pp.935~ (2019)
  13. Si T, "Directed Enzyme Evolution: Advances and Applications", pp.173~200 (2017), Springer International Publishing
  14. Conrad TM, "Microbial laboratory evolution in the era of genome-scale science", Mol. Syst. Biol, 7, pp.509~509 (2011)
  15. Portnoy VA, "Adaptive laboratory evolution-harnessing the power of biology for metabolic engineering", Curr. Opin. Biotechnol, 22, pp.590~594 (2011)
  16. Winkler JD, "Recent advances in the evolutionary engineering of industrial biocatalysts", Genomics, 104, pp.406~411 (2014)
  17. Winkler J, "Adaptive laboratory evolution for strain engineering", Methods Mol. Biol, 985, pp.211~222 (2013)
  18. Elena SF, "Evolution experiments with microorganisms : the dynamics and genetic bases of adaptation", Nat. Rev. Genet, 4, pp.457~469 (2003)
  19. Choi KR, "Systems metabolic engineering strategies : Integrating systems and synthetic biology with metabolic engineering", Trends Biotechnol, 37, pp.817~837 (2019)
  20. Grabar TB, "Methylglyoxal bypass identified as source of chiral contamination in l(+)and d(-)-lactate fermentations by recombinant Escherichia coli", Biotechnol. Lett, 28, pp.1527~1535 (2006)
  21. Royce LA, "Evolution for exogenous octanoic acid tolerance improves carboxylic acid production and membrane integrity", Metab. Eng, 29, pp.180~188 (2015)
  22. Wang Y, "Homofermentative production of D-lactic acid from sucrose by a metabolically engineered Escherichia coli", Biotechnol. Lett, 34, pp.2069~2075 (2012)
  23. Zhao J, "Homofermentative production of optically pure L-lactic acid from xylose by genetically engineered Escherichia coli B", Microb. Cell Fact, 12, pp.57~ (2013)
  24. Zhou S, "Fermentation of 10%(w", v)sugar to D : (-)-lactate by engineered Escherichia coli B, 2005, pp.27, 1891~1896
  25. Kim HJ, "Short-term adaptation modulates anaerobic metabolic flux to succinate by activating ExuT, a novel D-glucose transporter in Escherichia coli", Front. Microbiol, 11, pp.27~ (2020)
  26. Otero JM, "Industrial systems biology of Saccharomyces cerevisiae enables novel succinic acid cell factory", PLoS One, 8, pp.e54144~ (2013)
  27. John M. Leavitt, "Biosensor‐Enabled Directed Evolution to Improve Muconic Acid Production in Saccharomyces cerevisiae", Biotechnology Journal, 12(10), pp.1600687~ (2017), Wiley[DOI]
  28. Jiang LY, "Metabolic evolution of Corynebacterium glutamicum for increased production of Lornithine", BMC Biotechnol, 13, pp.47~ (2013)
  29. Mahr R, "Biosensor-driven adaptive laboratory evolution of L-valine production in Corynebacterium glutamicum", Metab. Eng, 32, pp.184~194 (2015)
  30. Basso TO, "Engineering topology and kinetics of sucrose metabolism in Saccharomyces cerevisiae for improved ethanol yield", Metab. Eng, 13, pp.694~703 (2011)
  31. Vilela Lde F, "Enhanced xylose fermentation and ethanol production by engineered Saccharomyces cerevisiae strain", AMB Express, 5, pp.16~ (2015)
  32. Pontrelli S, "Directed strain evolution restructures metabolism for 1-butanol production in minimal media", Metab. Eng, 49, pp.153~163 (2018)
  33. Smith KM, "An evolutionary strategy for isobutanol production strain development in Escherichia coli", Metab. Eng, 13, pp.674~681 (2011)
  34. Yu S, "Enhancement of lipid production in low-starch mutants Chlamydomonas reinhardtii by adaptive laboratory evolution", Bioresour. Technol, 147, pp.499~507 (2013)
  35. Yoneda A, "Comparative transcriptomics elucidates adaptive phenol tolerance and utilization in lipid-accumulating Rhodococcus opacus PD630", Nucleic Acids Res, 44, pp.2240~2254 (2016)
  36. Fu W, "Enhancement of carotenoid biosynthesis in the green microalga Dunaliella salina with light-emitting diodes and adaptive laboratory evolution", Appl. Microbiol. Biotechnol, 97, pp.2395~2403 (2013)
  37. Chou HH, "Programming adaptive control to evolve increased metabolite production", Nat. Commun, 4, pp.2595~ (2013)
  38. Reyes LH, "Improving carotenoids production in yeast via adaptive laboratory evolution", Metab. Eng, 21, pp.26~33 (2014)
  39. Charusanti P, "Exploiting adaptive laboratory evolution of Streptomyces clavuligerus for antibiotic discovery and overproduction", PLoS One, 7, pp.e33727~ (2012)
  40. Rathore SS, "Novel approach of adaptive laboratory evolution:Triggers defense molecules in Streptomyces sp. against targeted pathogen", RSC Adv., 6, pp.96250~96262 (2016)
  41. Jantama K, "Combining metabolic engineering and metabolic evolution to develop nonrecombinant strains of Escherichia coli C that produce succinate and malate", Biotechnol. Bioeng, 99, pp.1140~1153 (2008)
  42. Luo H, "Coupling S-adenosylmethionine-dependent methylation to growth : design and uses", PLoS Biol, 17, pp.e2007050~ (2019)
  43. Choi JW, "Development of a high-copy-number plasmid via adaptive laboratory evolution of Corynebacterium glutamicum", Appl. Microbiol. Biotechnol, 102, pp.873~883 (2018)
  44. Guimaraes PM, "Adaptive evolution of a lactose-consuming Saccharomyces cerevisiae recombinant", Appl. Environ. Microbiol, 74, pp.1748~1756 (2008)
  45. Kuyper M, "Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting Saccharomyces cerevisiae strain", FEMS Yeast Res, 5, pp.925~934 (2005)
  46. Lee SM, "Systematic and evolutionary engineering of a xylose isomerase-based pathway in Saccharomyces cerevisiae for efficient conversion yields", Biotechnol. Biofuels, 7, pp.122~ (2014)
  47. Tuyishime P, "Engineering Corynebacterium glutamicum for methanoldependent growth and glutamate production", Metab. Eng, 49, pp.220~231 (2018)
  48. Lu L, "Combining metabolic engineering and adaptive evolution to enhance the production of dihydroxyacetone from glycerol by Gluconobacter oxydans in a low-cost way", Bioresour. Technol, 117, pp.317~324 (2012)
  49. Fong SS, "Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states", Genome Res, 15, pp.1365~1372 (2005)
  50. Hua Q, "Metabolic characterization of Escherichia coli strains adapted to growth on lactate", Appl. Environ. Microbiol, 73, pp.4639~4647 (2007)
  51. Lee DH, "Adaptive evolution of Escherichia coli K-12 MG1655 during growth on a nonnative carbon source, L-1, 2-propanediol", Appl. Environ. Microbiol, 76, pp.4158~4168 (2010)
  52. Sandberg TE, "The emergence of adaptive laboratory evolution as an efficient tool for biological discovery and industrial biotechnology", Metab. Eng, 56, pp.1~16 (2019)
  53. Dragosits M, "Adaptive laboratory evolution-principles and applications for biotechnology", Microb. Cell Fact, 12, pp.64~ (2013)
  54. Graf M, "Continuous adaptive evolution of a fastgrowing Corynebacterium glutamicum strain independent of protocatechuate", Front. Microbiol, 10, pp.1648~ (2019)
  55. Hoskisson PA, "Continuou culture – making a comeback?", Microbiology, 151, pp.3153~3159 (2005)
  56. Jin T, "Biotechnology for Biofuel Production and Optimization", pp.265~290 (2016), Elsevier
  57. Herbert D, "The continuous culture of bacteria; a theoretical and experimental study", J. Gen. Microbiol, 14, pp.601~622 (1956)
  58. Rao VSH, "Global stability in chemostat models involving time delays and wall growth", Nonlinear Analysis : Real World Applications, 5, pp.141~158 (2004)
  59. Radek A, "Miniaturized and automated adaptive laboratory evolution : evolving Corynebacterium glutamicum towards an improved d-xylose utilization", Bioresour. Technol, 245, pp.1377~1385 (2017)
  60. Wu G, "Metabolic burden : cornerstones in synthetic biology and metabolic engineering applications", Trends Biotechnol, 34, pp.652~664 (2016)
  61. Schwentner A, "Metabolic engineering to guide evolution-creating a novel mode for L-valine production with Corynebacterium glutamicum", Metab. Eng, 47, pp.31~41 (2018)
  62. Lee S-W, "A synthetic suicide riboswitch for the high-throughput screening of metabolite production in Saccharomyces cerevisiae", Metab. Eng, 28, pp.143~150 (2015)
  63. Palsson BO, "Systems Biology: Constraint-based Reconstruction and Analysis", pp.422~437 (2015), Cambridge University Press
  64. Lee DH, "Cumulative number of cell divisions as a meaningful timescale for adaptive laboratory evolution of Escherichia coli", PLoS One, 6, pp.e26172~ (2011)
  65. Pfeifer E, "Adaptive laboratory evolution of Corynebacterium glutamicum towards higher growth rates on glucose minimal medium", Sci. Rep, 7, pp.16780~ (2017)
  66. Larson MH, "CRISPR interference(CRISPRi)for sequence-specific control of gene expression", Nat. Protoc, 8, pp.2180~2196 (2013)
  67. Perez-Pinera P, "RNA-guided gene activation by CRISPRCas9-based transcription factors", Nat. Methods, 10, pp.973~976 (2013)
  68. Anzalone AV, "Search-and-replace genome editing without double-strand breaks or donor DNA", Nature, 576, pp.149~157 (2019)
  69. Bódi Z, "Phenotypic heterogeneity promotes adaptive evolution", PLoS Biol, 15, pp.e2000644~e2000644 (2017)
  70. Sen M, "In vivo evolutionary engineering of a boron-resistant bacterium : Bacillus boroniphilus", Antonie van Leeuwenhoek, 99, pp.825~835 (2011)
  71. Sonderegger M, "Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose", Appl. Environ. Microbiol, 69, pp.1990~1998 (2003)
  72. Camps M, "Targeted gene evolution in Escherichia coli using a highly error-prone DNA polymerase I", 100, pp.9727~9732 (2003)
  73. Ravikumar A, "Scalable, continuous evolution of genes at mutation rates above genomic error thresholds", Cell, 175, pp.1946~1957 (2018)
  74. Moore CL, "A processive protein chimera introduces mutations across defined DNA regions in vivo", J. Am. Chem. Soc, 140, pp.11560~11564 (2018)
  75. Halperin SO, "CRISPR-guided DNA polymerases enable diversification of all nucleotides in a tunable window", Nature, 560, pp.248~252 (2018)
  76. Jakočiūnas T, "CasPER, a method for directed evolution in genomic contexts using mutagenesis and CRISPR", Cas9, 2018, pp.48, 288~296
  77. Garst AD, "Genome-wide mapping of mutations at singlenucleotide resolution for protein, metabolic and genome engineering", Nat. Biotechnol, 35, pp.48~55 (2017)
  78. Zhang Y-X, "Genome shuffling leads to rapid phenotypic improvement in bacteria", Nature, 415, pp.644~646 (2002)
  79. Alper H, "Global transcription machinery engineering : a new approach for improving cellular phenotype", Metab. Eng, 9, pp.258~267 (2007)
  80. Wang HH, "Programming cells by multiplex genome engineering and accelerated evolution", Nature, 460, pp.894~898 (2009)
  81. Sandberg TE, "Evolution of Escherichia coli to 42oC and subsequent genetic engineering reveals adaptive mechanisms and novel mutations", Mol. Biol. Evol, 31, pp.2647~2662 (2014)
  82. Luan G, "Genome replication engineering assisted continuous evolution(GREACE)to improve microbial tolerance for biofuels production", Biotechnol. Biofuels, 6, pp.137~ (2013)
  83. Wang X, "GREACE-assisted adaptive laboratory evolution in endpoint fermentation broth enhances lysine production by Escherichia coli", Microb. Cell Fact, 18, pp.106~ (2019)
  84. McBryde C, "Generation of Novel Wine Yeast Strains by Adaptive Evolution", Am. J. Enol. Vitic, 57, pp.423~ (2006)
  85. Pérez-Torrado R, "Genetic improvement of non-GMO wine yeasts : strategies, advantages and safety", Trends Food Sci. Technol, 45, pp.1~11 (2015)
  86. Börner RA, "Genome editing of lactic acid bacteria: opportunities for food, feed, pharma and biotech", FEMS Microbiol. Lett., 366, pp.fny291~ (2019)
  87. Lusk JL, "Consumer acceptance of new food technologies : causes and roots of controversies", Annu. Rev. Resour. Econ, 6, pp.381~405 (2014)
  88. Høier E, "The production, application and action of lactic cheese starter cultures", pp.166~192 (2010), Technology of Cheesemaking
  89. Gonzalez R, "Wine Safety, Consumer Preference, and Human Health", pp.71~96 (2016), Springer
  90. Csutak O, "Genetically Engineered Foods", pp.143~175 (2018), Academic Press
  91. Snow R, "Yeast genetics", pp.439~459 (1983), Springer
  92. Walker ME, "Application of the reuseable, KanMX selectable marker to industrial yeast : construction and evaluation of heterothallic wine strains of Saccharomyces cerevisiae, possessing minimal foreign DNA sequences", 4, pp.339~347 (2003)
  93. Bakalinsky AT, "The chromosomal constitution of wine strains of Saccharomyces cerevisiae", Yeast, 6, pp.367~382 (1990)
  94. Querol A, "Adaptive evolution of wine yeast", Int. J. Food Microbiol, 86, pp.3~10 (2003)
  95. Denby CM, "Industrial brewing yeast engineered for the production of primary flavor determinants in hopped beer", Nat. Commun, 9, pp.965~ (2018)
  96. Pardo E, "De novo production of six key grape aroma monoterpenes by a geraniol synthase-engineered Saccharomyces cerevisiae wine strain", Microb. Cell Fact, 14, pp.136~ (2015)
  97. Petzold CJ, "Analytics for metabolic engineering", Front. Bioeng. Biotechnol, 3, pp.135~ (2015)
  98. Bergman A, "Metabolic engineering strategies to convert carbohydrates to aviation range hydrocarbons", pp.151~190 (2016), Biofuels for Aviation
  99. Hansen ASL, "Systems biology solutions for biochemical production challenges", Curr. Opin. Biotechnol, 45, pp.85~91 (2017)
  100. Thiele I, "A protocol for generating a high-quality genome-scale metabolic reconstruction", Nat. Protoc, 5, pp.93~121 (2010)
  101. Edwards JS, "Systems properties of the Haemophilus influenzaeRd metabolic genotype", J. Biol. Chem, 274, pp.17410~17416 (1999)
  102. O’Brien EJ, "Using genome-scale models to predict biological capabilities", Cell, 161, pp.971~987 (2015)
  103. Sandberg TE, "Laboratory evolution to alternating substrate environments yields distinct phenotypic and genetic adaptive strategies", Appl. Environ. Microbiol, 83, pp.e00410~e00417 (2017)
  104. LaCroix RA, "A model for designing adaptive laboratory evolution experiments", Appl. Environ. Microbiol, 83, pp.e03115~e03116 (2017)
  105. LaCroix RA, "Use of adaptive laboratory evolution to discover key mutations enabling rapid growth of Escherichia coli K-12 MG1655 on glucose minimal medium", Appl. Environ. Microbiol, 81, pp.17~30 (2015)
  106. Strucko T, "Laboratory evolution reveals regulatory and metabolic trade-offs of glycerol utilization in Saccharomyces cerevisiae", Metab. Eng, 47, pp.73~82 (2018)
  107. glucose reveals a negligible isotopic influence on metabolism and physiology, "PLoS One", 2016, e0151130~
  108. Horinouchi T, "Development of an automated culture system for laboratory evolution", J. Lab. Autom, 19, pp.478~482 (2014)
  109. Toprak E, "Evolutionary paths to antibiotic resistance under dynamically sustained drug selection", Nat. Genet, 44, pp.101~105 (2011)
  110. Toprak E, "Building a morbidostat : An automated continuous-culture device for studying bacterial drug resistance under dynamically sustained drug inhibition", Nat. Protoc, 8, pp.555~567 (2013)
  111. Takahashi CN, "A low cost, customizable turbidostat for use in Synthetic circuit characterization", ACS Synth. Biol, 4, pp.32~38 (2015)
  112. Heins ZJ, "Designing automated, high-throughput, continuous cell growth experiments using eVOLVER", J. Vis. Exp, 147, pp.10~ (2019)
  113. Wong BG, "Precise, automated control of conditions for high-throughput growth of yeast and bacteria with eVOLVER", Nat. Biotechnol, 36, pp.614~623 (2018)
  114. Curran KA, "Metabolic engineering of muconic acid production in Saccharomyces cerevisiae", Metab. Eng, 15, pp.55~66 (2013)
  115. Kao KC, "Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae", Nat. Genet, 40, pp.1499~1504 (2008)
  116. Baba T, "Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants : the Keio collection", Mol. Syst. Biol, 2 (2006)
  117. Domingues L, "Construction of a flocculent Saccharomyces cerevisiae fermenting lactose", Appl. Microbiol. Biotechnol, 51, pp.621~626 (1999)
  118. Kuyper M, "Metabolic engineering of a xyloseisomerase-expressing Saccharomyces cerevisiae strain for rapid anaerobic xylose fermentation", FEMS Yeast Res, 5, pp.399~409 (2005)
  119. Herring CD, "Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale", Nat. Genet, 38, pp.1406~1412 (2006)
  120. Monk JM, "iML1515, a knowledgebase that computes Escherichia coli traits", Nat. Biotechnol, 35, pp.904~908 (2017)
  121. Lu H, "A consensus Saccharomyces cerevisiae metabolic model Yeast8 and its ecosystem for comprehensively probing cellular metabolism", Nat. Commun, 10, pp.3586~ (2019)
  122. Zhang Y, "A new genome-scale metabolic model of Corynebacterium glutamicum and its application", Biotechnol. Biofuels, 10, pp.169~ (2017)
  123. Kocabaş P, "Analyses of extracellular protein production in Bacillus subtilis – II : genome-scale metabolic model reconstruction based on updated gene-enzyme-reaction data", Biochem. Eng. J, 127, pp.229~241 (2017)
  124. Lu Y, "Genomic sequencing, genome-scale metabolic network reconstruction, and in silico flux analysis of the grape endophytic fungus Alternaria sp. MG1", Microb. Cell Fact, 18, pp.13~ (2019)
  125. Kumelj T, "Predicting strain engineering strategies using iKS1317 : A genome-scale metabolic model of Streptomyces coelicolor", Biotechnol. J, 14, pp.e1800180~ (2019)
  126. Zuniga C, "Predicting dynamic metabolic demands in the photosynthetic eukaryote Chlorella vulgaris", Plant Physiol, 176, pp.450~462 (2018)
  127. Ozcan E, "A genome-scale metabolic network of the aroma bacterium Leuconostoc mesenteroides subsp. cremoris", Appl. Microbiol. Biotechnol., 103, pp.3153~3165 (2019)
  128. Kristjansdottir T, "A metabolic reconstruction of Lactobacillus reuteri JCM 1112 and analysis of its potential as a cell factory", Microb. Cell Fact, 18, pp.186~ (2019)
  129. Loira N, "Reconstruction of the microalga Nannochloropsis salina genome-scale metabolic model with applications to lipid production", BMC Syst. Biol, 11, pp.66~ (2017)
  130. Mora Salguero DA, "Development of a chlamydomonas reinhardtii metabolic network dynamic model to describe distinct phenotypes occurring at different CO2 levels", PeerJ, 6, pp.e5528~ (2018)

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