Skip to main content
SpringerLink
Log in

Connecting Biology With Biotechnology

Industrial Applications of Adaptive Laboratory Evolution

  • General Article
  • Published:
Resonance Aims and scope Submit manuscript

Abstract

Adaptive laboratory evolution (ALE) has been used as a tool to understand the basic principles of evolution as well as for engineering microorganisms for numerous industrial applications. With recent advances in next-generation sequencing (NGS), ALE has regained its momentum, and it has become possible to identify underlying causal mutations. Thus, ALE can serve as a tool for imparting industrially useful features in the microbes and complement the genetic engineering approaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Suggested Reading

  1. Jee J et al., Rates and mechanisms of bacterial mutagenesis from maximum-depth sequencing, Nature, Vol.534(7609), pp.693, 2016.

    Article  Google Scholar 

  2. LaCroix RA et al., 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., Vol.81(1), pp.17–30, 2015.

    Article  Google Scholar 

  3. Choe D et al., Adaptive laboratory evolution of a genome-reduced Escherichia coli, Nat Commun., Vol.10, pp.1, 2019.

    Article  Google Scholar 

  4. S Perli T et al., S Perli T et al., Adaptive laboratory evolution and reverse engineering of single-vitamin protrotrophies in Saccharomyces cerevisiae, Appl. Environ. Microbiol., Vol.86(12), pp.1–23, 2020.

    Article  Google Scholar 

  5. Bracher JM et al., Laboratory evolution of a biotin-requiring Saccharomyces cerevisiae strain for full biotin prototrophy and identification of causal mutations, Appl. Environ. Microbiol., Vol.83, pp.16, 2017.

    Article  Google Scholar 

  6. Har JRG et al., Adaptive laboratory evolution of methylotrophic Escherichia coli enables synthesis of all amino acids from methanol-derived carbon, Appl. Microbiol. Biotechnol., Vol.105(2), pp.869–76, 2021.

    Article  Google Scholar 

  7. Shui ZX et al., Adaptive laboratory evolution of ethanologenic Zymomonas mobilis strain tolerant to furfural and acetic acid inhibitors, Appl. Microbiol. Biotechnol., Vol.99(13), pp.5739–48, 2015.

    Article  Google Scholar 

  8. Wallace-Salinas V, Gorwa-Grauslund MF. Adaptive evolution of an industrial strain of Saccharomyces cerevisiae for combined tolerance to inhibitors and temperature, Biotechnol Biofuels, Vol.6(1), pp.1–9, 2013.

    Article  Google Scholar 

  9. Wang D, Ju X, Zhou D, Wei G, Efficient production of pullulan using rice hull hydrolysate by adaptive laboratory evolution of Aureobasidium pulluans, Biores. Technol., Vol.164, pp.12–9, 2014.

    Article  Google Scholar 

  10. Moniri M et al., Production and status of bacterial cellulose in biomedical engineering, Nanomaterials, Vol.7(9), pp.1–26, 2017.

    Article  Google Scholar 

  11. Wu ZY, Liang HW, Chen LF, Hu BC, Yu SH, Bacterial cellulose: A robust platform for design of three dimensional carbon-based functional nanomaterials, Acc. Chem. Res., Vol.49(1), pp.96–105, 2016.

    Article  Google Scholar 

  12. Vasconcellos VM, Farinas CS, Ximenes E, Slininger P, Ladisch M, Adaptive laboratory evolution of nanocellulose-producing bacterium, Biotechnol. and Bioeng., Vol.116, pp.1923–1933, 2019.

    Article  Google Scholar 

  13. Wang Z et al., Adaptive laboratory evolution of Yarrowia lipolytica improves ferulic acid tolerance, Appl. Microbiol. Biotechnol., Vol.105(4), pp.1745–58, 2021.

    Article  Google Scholar 

  14. Igeño MI, Macias D, Blasco R, A case of adaptive laboratory evolution (ALE): Biodegradation of furfural by Pseudomonas pseudoalcaligenes CECT 5344, Genes, Vol.10, pp.7, 2019.

    Article  Google Scholar 

  15. Liu Z, Radi M, Mohamed ETT, Feist AM, Dragone G, Mussatto SI, Adaptive laboratory evolution of Rhodosporidium toruloides to inhibitors derived from lignocellulosic biomass and genetic variations behind evolution, Biores. Technol., Vol.333, 2021.

  16. Ju SY, Kim JH, Lee PC, Long-term adaptive evolution of Leuconostoc mesenteroides for enhancement of lactic acid tolerance and production, Biotechnol. Biofuels, Vol.9(1), pp.1–12, 2016.

    Article  Google Scholar 

  17. Ming H, Xu D, Guo Z, Liu Y, Adaptive evolution of Lactobacillus casei under acidic conditions enhances multiple-stress tolerance, Food Sci, Technol. Res., Vol.22(3), pp.331–6, 2016.

    Article  Google Scholar 

  18. Mundhada H et al., Increased production of L-serine in Escherichia coli through adaptive laboratory evolution, Metabol. Eng., Vol.39, pp.141–50, 2017.

    Article  Google Scholar 

  19. Horinouchi T, Sakai A, Kotani H, Tanabe K, Furusawa C, Improvement of isopropanol tolerance of Escherichia coli using adaptive laboratory evolution and omics technologies, J. Biotechnol., Vol.255, pp.47–56, 2017.

    Article  Google Scholar 

  20. da Silveira FA et al., Assessment of ethanol tolerance of Kluyveromyces marxianus CCT 7735 selected by adaptive laboratory evolution, Appl. Microbiol. Biotechnol., Vol.104(17), pp.7483–94, 2020.

    Article  Google Scholar 

  21. Catrileo D, Acuña-Fontecilla A, Godoy L, Adaptive laboratory evolution of native Torulaspora delbrueckii YCPUC10 with enhanced ethanol resistance and evaluation in co-inoculated fermentation, Front Microbiol., vol.11(December), pp.1–13, 2020.

    Google Scholar 

  22. Kusumawardhani H, Furtwängler B, Adaptive laboratory evolution restores solvent tolerance in plasmid-cured Pseudomonas putida S12: A molecular analysis, Appl. and Env. Microbial., Vol.87(9), pp.1–18, 2021.

    Article  Google Scholar 

  23. Jiang LY, Chen SG, Zhang YY, Liu JZ, Metabolic evolution of Corynebacterium glutamicum for increased production of L-ornithine, BMC Biotechnol., Vol.13, 2013.

  24. Han S Il, Kim S, Lee C, Choi YE, Blue-Red LED wavelength shifting strategy for enhancing beta-carotene production from halotolerant microalga, Dunaliella salina, J. Microbiol., Vol.57(2), pp.101–6, 2019.

    Article  Google Scholar 

  25. Kwon YW, Bae JH, Kim SA, Han NS, Development of freeze-thaw tolerant Lactobacillus rhamnosus GG by adaptive laboratory evolution, Front Microbiol., Vol.9(Nov), pp.1–10, 2018.

    Google Scholar 

  26. Bonilla CY, Generally stressed out bacteria: Environmental stress response mechanisms in gram-positive bacteria, Integr Comp Biol., Vol.60(1), pp.126–33, 2020.

    Article  Google Scholar 

  27. Zorraquino V, Kim M, Rai N, Tagkopoulos I, The genetic and transcriptional basis of short and long term adaptation across multiple stresses in Escherichia coli, Mol Biol Evol., Vol.34(3), pp.707–17, 2017.

    Google Scholar 

  28. Oide S et al. Thermal and solvent stress cross-tolerance conferred to Corynebacterium glutamicum by adaptive laboratory evolution, Appl Environ Microbiol., Vol.81(7), pp.2284–98, 2015.

    Article  Google Scholar 

  29. Çakar ZP et al., Isolation of cobalt hyper-resistant mutants of Saccharomyces cerevisiae by in vivo evolutionary engineering approach, J Biotechnol., Vol.143(2), pp.130–8, 2009.

    Article  Google Scholar 

  30. Çakar ZP, Seker UOS, Tamerler C, Sonderegger M, Sauer U, Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae, FEMS Yeast Res., Vol.5(6–7), pp.569–78, 2005.

    Article  Google Scholar 

  31. Strucko T et al., Laboratory evolution reveals regulatory and metabolic tradeoffs of glycerol utilization in Saccharomyces cerevisiae., Metab Eng., Vol.47, pp.73–82, 2018.

    Article  Google Scholar 

  32. Eremina NS et al., Adaptive evolution of Escherichia coli K-12 MG1655 grown on ethanol and glycerol, Appl Biochem Microbiol., Vol.54(8), pp.793–9, 2019.

    Article  Google Scholar 

  33. Hong KK, Vongsangnak W, Vemuri GN, Nielsen J, Unravelling evolutionary strategies of yeast for improving galactose utilization through integrated systems level analysis, Proc. Natl. Acad. Sci. USA., Vol.108(29), pp.12179–84, 2011.

    Article  Google Scholar 

  34. Karhumaa K, Wiedemann B, Hahn-Hägerdal B, Boles E, Gorwa-Grausland MF, Co-utilization of L-arabinose and D-xylose by laboratory and industrial Saccharomyces cerevisiae strains, Microb. Cell Fact., Vol.5, pp.1–11, 2006.

    Article  Google Scholar 

  35. Sarkar P, Mukherjee M, Goswami G, Das D, Adaptive laboratory evolution induced novel mutations in Zymomonas mobilis ATCC ZW658: A potential platform for co-utilization of glucose and xylose, J. Ind. Microbiol. Biotechnol., Vol.47(3), pp.329–41, 2020.

    Article  Google Scholar 

  36. Zhang B, Li N, Wang Z, Tang YJ, Chen T, Zhao X, Inverse metabolic engineering of Bacillus subtilis for xylose utilization based on adaptive evolution and whole-genome sequencing, Appl. Microbiol. Biotechnol., Vol.99, pp.885–96, 2015.

    Article  Google Scholar 

  37. Radek A et al., Miniaturized and automated adaptive laboratory evolution: Evolving Corynebacterium glutamicum towards an improved D-xylose utilization, Biores. Technol., Vol.245, pp.1377–85, 2017.

    Article  Google Scholar 

  38. Tuyishime P et al., Engineering Corynebacterium glutamicum for methanol-dependent growth and glutamate production, Metabol. Eng., Vol.49, pp.220–231, 2018.

    Article  Google Scholar 

  39. Wang Y et al., Adaptive laboratory evolution enhances methanol tolerance and conversion in engineered Corynebacterium glutamicum, Commun Biol., Vol.3, pp.1, 2020.

    Article  Google Scholar 

  40. Espinosa MI et al., Adaptive laboratory evolution of native methanol assimilation in Saccharomyces cerevisiae, Nat. Comm., Vol.11, pp.1, 2020.

    Article  Google Scholar 

  41. Bennett RK et al., Improving the methanol tolerance of an Escherichia coli methylotroph via adaptive laboratory evolution enhances synthetic methanol utilization, Front Microbiol., Vol.12, pp.1–11, 2021.

    Article  Google Scholar 

  42. Reyes LH, Gomez JM, Kao KC, Improving carotenoids production in yeast via adaptive laboratory evolution, Metabol. Eng., Vol.21, pp.26–33, 2014.

    Article  Google Scholar 

  43. Mahr R, Gätgens C, Gätgens J, Polen T, Kalinowski J, Frunzke J. Biosensor-driven adaptive laboratory evolution of l-valine production in Corynebacterium glutamicum, Metabol. Eng., Vol.32, pp.184–94, 2015.

    Article  Google Scholar 

  44. Charusanti P et al., Exploiting adaptive laboratory evolution of Streptomyces clavuligerus for antibiotic discovery and overproduction, PLoS One, Vol.7, pp.3, 2012.

    Article  Google Scholar 

  45. Song P et al., Enhancement of pneumocandin B0 production in Glarea lozoyensis by low-temperature adaptive laboratory evolution, Front Microbiol., Vol.9(Nov), pp.1–12, 2018.

    Google Scholar 

  46. Lenski RE, Travisano M. Dynamics of adaptation and diversification: A 10,000- generation experiment with bacterial populations, Proc. Natl. Acad. Sci. USA, Vol.91(15), pp.6808–14, 1994.

    Article  Google Scholar 

  47. Blount ZD, Borland CZ, Lenski RE, Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli, Proc. Natl. Acad. Sci. USA, Vol.105(23), pp.7899–906, 2008.

    Article  Google Scholar 

  48. Kim S, Lieberman TD, Kishony R, Alternating antibiotic treatments constrain evolutionary paths to multidrug resistance, Proc. Natl. Acad. Sci. USA, Vol.111(40), pp.14494–9, 2014.

    Article  Google Scholar 

  49. Dong Y, Zhang F, Wang B, Gao J, Zhang J, Shao Y, Laboratory evolution assays and whole-genome sequencing for the development and safety evaluation of Lactobacillus plantarum with stable resistance to gentamicin, Front Microbiol., Vol.10(Jun), 2019.

  50. Bachmann H et al., Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution, Genome Res., Vol.22(1), pp.115–24, 2012.

    Article  Google Scholar 

  51. Dragosits M, Mattanovich D, Adaptive laboratory evolution—Principles and applications for biotechnology, Microb Cell Fact., Vol.12(1), pp.1–17, 2013.

    Article  Google Scholar 

  52. Pfeifer E, Gätgens C, Polen T, Frunzke J, Adaptive laboratory evolution of Corynebacterium glutamicum towards higher growth rates on glucose minimal medium, Sci. Rep., Vol.7(1), pp.1–14, 2017.

    Article  Google Scholar 

  53. González-Ramos D et al., A new laboratory evolution approach to select for constitutive acetic acid tolerance in Saccharomyces cerevisiae and identification of causal mutations, Biotechnol. for Biof., Vol.9, 2016.

  54. Xu C, Sun T, Li S, Chen L, Zhang W, Adaptive laboratory evolution of cadmium tolerance in Synechocystis sp. PCC 6803, Biotechnol. for Biof., Vol.11(1), pp.1–15, 2018.

    Google Scholar 

  55. Papapetridis I et al., Laboratory evolution for forced glucose-xylose co-consumption enables identification of mutations that improve mixed-sugar fermentation by xylose-fermenting Saccharomyces cerevisiae, FEMS Yeast Res., Vol.18(6), pp.1–17, 2018.

    Article  Google Scholar 

  56. Xu X et al., Evolutionary engineering in Saccharomyces cerevisiae reveals a TRK1-dependent potassium influx mechanism for propionic acid tolerance, Biotechnol. for Biof., Vol.12(1), pp.1–14, 2019.

    Google Scholar 

  57. Lee JK et al., Efficient production of d-lactate from methane in a lactate-tolerant strain of Methylomonas sp. DH-1 generated by adaptive laboratory evolution, Biotechnol for Biof., Vol.12(1), pp.1–11, 2019.

    Google Scholar 

  58. Lim HG et al., Generation of ionic liquid tolerant Pseudomonas putida KT2440 strains via adaptive laboratory evolution, Green Chem., Vol.22(17), pp.5677–90, 2020.

    Article  Google Scholar 

  59. Conrad TM et al., RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media, Proc. Natl. Acad. Sci. USA, Vol.107(47), pp.20500–5, 2010.

    Article  Google Scholar 

  60. Rajaraman E et al., Transcriptional analysis and adaptive evolution of Escherichia coli strains growing on acetate, Appl. Microbiol. Biotechnol., Vol.100(17), pp.7777–85, 2016.

    Article  Google Scholar 

  61. Guzmán GI et al., Enzyme promiscuity shapes adaptation to novel growth substrates, Mol. Syst. Biol., Vol.15(4), pp.1–14, 2019.

    Article  Google Scholar 

  62. Matsusako T, Toya Y, Yoshikawa K, Shimizu H, Identification of alcohol stress tolerance genes of Synechocystis sp. PCC 6803 using adaptive laboratory evolution, Biotechnol. for Biof., Vol.54(8), pp.1–9, 2017.

    Google Scholar 

  63. Lang GI, Desai MM, The spectrum of adaptive mutations in experimental evolution, Genomics, Vol.104(6), pp.412–6, 2014.

    Article  Google Scholar 

  64. Wouter Wisselink H et al., Novel evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains, Appl. Environ. Microbiol., Vol.75(4), pp.907–14, 2009.

    Article  Google Scholar 

Download references

Acknowledgement

We are grateful to the Symbiosis Centre for Research and Innovation (SCRI), Symbiosis International (Deemed University) for financial support. The academic activities related to antimicrobial resistance at the host institute are supported through ERASMUS+ grant 598515-EPP-1-2018-1-IN-EPPKA2-CBHE-JP. Komal Kadam acknowledges Senior Research Fellowship from the Indian Council of Medical Research.

Author information

Authors and Affiliations

  1. Symbiosis School of Biological Sciences, Symbiosis International (Deemed University), Lavale, Pune, 412 115, India

    Komal Kadam & Ram Kulkarni

Authors
  1. Komal Kadam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ram Kulkarni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ram Kulkarni.

Additional information

Komal Kadam is ICMR-Senior Research Fellow at Symbiosis International (Deemed University), Pune. Her doctoral research dissects metabolic regulation in lactic acid bacteria through stress adaptation.

Ram Kulkarni is Associate Professor at Symbiosis International (Deemed University). His current research interests include biochemical and molecular characterization of the useful properties of lactic acid bacteria and their evolutionary and metabolic engineering.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kadam, K., Kulkarni, R. Connecting Biology With Biotechnology. Reson 27, 1741–1759 (2022). https://doi.org/10.1007/s12045-022-1469-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12045-022-1469-0

Keywords

Search

Navigation