Abstract
The uptake of exogenous DNA materials through the cell membrane by bacteria, known as transformation, is essential for the genetic manipulation of bacteria and, thus, plays key roles in biotechnological and biological research. The efficiency of natural transformation is very low; therefore, various artificial transformation methods have been developed for simple and efficient bacterial transformation. The basic bacterial transformation method is based on chemical, physical, and electrical processes and other means to permeabilize the bacterial cell membrane to allow plasmid DNA uptake. With the introduction of novel chemicals, materials, and devices and the optimization of protocols, new transformation methods have become simpler, cheaper, and more reproducible for use in diverse bacterial species compared with conventional methods. In this review, artificial transformation methods have been classified according to the membrane-permeabilizing mechanisms employed by them. Their influential factors, transformation efficiency, advantages, disadvantages, and practical applications are briefly illustrated. Finally, physicochemical transformation as a new bacterial transformation technique has also been described.
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References
Berthier F, Zagorec M, ChampomierVerges M, Ehrlich SD, MorelDeville F (1996) Efficient transformation of Lactobacillus sake by electroporation. Microbiol-Uk 142:1273–1279. https://doi.org/10.1099/13500872-142-5-1273
Bozkir A, Saka OM (2004) Chitosan-DNA nanoparticles: effect on DNA integrity, bacterial transformation and transfection efficiency. J Drug Target 12(5):281–288. https://doi.org/10.1080/10611860410001714162
Brito LF, Irla M, Walter T, Wendisch VF (2017) Magnesium aminoclay-based transformation of Paenibacillus riograndensis and Paenibacillus polymyxa and development of tools for gene expression. Appl Microbiol Biotechnol 101(2):735–747. https://doi.org/10.1007/s00253-016-7999-1
Campos-Guillen J, Fernandez F, Pastrana X, Loske AM (2012) Relationship between plasmid size and shock wave-mediated bacterial transformation. Ultrasound Med Biol 38(6):1078–1084. https://doi.org/10.1016/j.ultrasmedbio.2012.02.018
Chan WT, Verma CS, Lane DP, Gan SK (2013) A comparison and optimization of methods and factors affecting the transformation of Escherichia coli. Biosci Rep 33(6). https://doi.org/10.1042/BSR20130098
Chandrasekaran G, Han HK, Kim GJ, Shin HJ (2011) Antimicrobial activity of delaminated aminopropyl functionalized magnesium phyllosilicates. Appl Clay Sci 53(4):729–736. https://doi.org/10.1016/j.clay.2011.07.001
Chang S, Cohen SN (1979) High frequency transformation of Bacillus subtilis protoplasts by plasmid DNA. Mol Gen Genet 168(1):111–115. https://doi.org/10.1007/bf00267940
Choi HA, Lee YC, Lee JY, Shin HJ, Han HK, Kim GJ (2013) A simple bacterial transformation method using magnesium- and calcium-aminoclays. J Microbiol Methods 95(2):97–101. https://doi.org/10.1016/j.mimet.2013.07.018
Chuanchuen R, Narasaki CT, Schweizer HP (2002) Benchtop and microcentrifuge preparation of Pseudomonas aeruginosa competent cells. Biotechniques 33(4):760, 762-3. https://doi.org/10.2144/02334bm08
Chung CT, Niemela SL, Miller RH (1989) One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci U S A 86(7):2172–2175. https://doi.org/10.1073/pnas.86.7.2172
Cohen SN, Chang AC, Hsu L (1972) Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A 69(8):2110–2114. https://doi.org/10.1073/pnas.69.8.2110
Dagert M, Ehrlich SD (1979) Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene 6(1):23–28. https://doi.org/10.1016/0378-1119(79)90082-9
Deshmukh K, Ramanan SR, Kowshik M (2019) Novel one step transformation method for Escherichia coli and Staphylococcus aureus using arginine-glucose functionalized hydroxyapatite nanoparticles. Mater Sci Eng C Mater Biol Appl 96:58–65. https://doi.org/10.1016/j.msec.2018.10.088
Ding C, Pan J, Jin M, Yang D, Shen Z, Wang J, Zhang B, Liu W, Fu J, Guo X, Wang D, Chen Z, Yin J, Qiu Z, Li J (2016) Enhanced uptake of antibiotic resistance genes in the presence of nanoalumina. Nanotoxicology 10(8):1051–1060. https://doi.org/10.3109/17435390.2016.1161856
Dower WJ, Miller JF, Ragsdale CW (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16(13):6127–6145. https://doi.org/10.1093/nar/16.13.6127
Duitman EH, Wyczawski D, Boven LG, Venema G, Kuipers OP, Hamoen LW (2007) Novel methods for genetic transformation of natural Bacillus subtilis isolates used to study the regulation of the mycosubtilin and surfactin synthetases. Appl Environ Microbiol 73(11):3490–3496. https://doi.org/10.1128/AEM.02751-06
Dunny GM, Lee LN, LeBlanc DJ (1991) Improved electroporation and cloning vector system for gram-positive bacteria. Appl Environ Microbiol 57(4):1194–1201
Fiedler S, Wirth R (1988) Transformation of bacteria with plasmid DNA by electroporation. Anal Biochem 170(1):38–44. https://doi.org/10.1016/0003-2697(88)90086-3
Fong WK, Hanley TL, Thierry B, Hawley A, Boyd BJ, Landersdorfer CB (2016) External manipulation of nanostructure in photoresponsive lipid depot matrix to control and predict drug release in vivo. J Control Release 228:67–73. https://doi.org/10.1016/j.jconrel.2016.02.042
Garcia PA, Ge Z, Moran JL, Buie CR (2016) Microfluidic screening of electric fields for electroporation. Sci Rep 6:21238. https://doi.org/10.1038/srep21238
Garcia PA, Ge ZF, Kelley LE, Holcomb SJ, Buie CR (2017) High efficiency hydrodynamic bacterial electrotransformation. Lab Chip 17(3):490–500. https://doi.org/10.1039/c6lc01309k
Gokara M, Kimavath GB, Podile AR, Subramanyam R (2015) Differential interactions and structural stability of chitosan oligomers with human serum albumin and alpha-1-glycoprotein. J Biomol Struct Dyn 33(1):196–210. https://doi.org/10.1080/07391102.2013.868321
Hanahan D, Jessee J, Bloom FR (1991) [4] Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol 204. Elsevier:63–113
Hisatsune J, Sato’o Y, Yu LS, Kutsuno S, Hayakawa Y, Sugai M (2016) Efficient transformation of Staphylococcus aureus using multi-pulse electroporation. J Microbiol Methods 130:69–72. https://doi.org/10.1016/j.mimet.2016.08.012
Iwasaki K, Uchiyama H, Yagi O, Kurabayashi T, Ishizuka K, Takamura Y (1994) Transformation of Pseudomonas putida by electroporation. Biosci Biotechnol Biochem 58(5):851–854
Kas HS (1997) Chitosan: properties, preparations and application to microparticulate systems. J Microencapsul 14(6):689–711. https://doi.org/10.3109/02652049709006820
Kumari M, Pandey S, Mishra A, Nautiyal CS (2017) Finding a facile way for the bacterial DNA transformation by biosynthesized gold nanoparticles. FEMS Microbiol Lett 364(12). https://doi.org/10.1093/femsle/fnx081
Lee YC, Choi YS, Choi M, Yang HT, Liu KC, Shin HJ (2013) Dual-end functionalized magnesium organo-(phyllo)silicates via co-condensation and its antimicrobial activity. Appl Clay Sci 83-84:474–485. https://doi.org/10.1016/j.clay.2012.10.007
Leong KW, Mao HQ, Truong-Le VL, Roy K, Walsh SM, August JT (1998) DNA-polycation nanospheres as non-viral gene delivery vehicles. J Control Release 53(1-3):183–193. https://doi.org/10.1016/S0168-3659(97)00252-6
Li J, Li JJ, Zhang J, Wang X, Kawazoe N, Chen G (2016) Gold nanoparticle size and shape influence on osteogenesis of mesenchymal stem cells. Nanoscale 8(15):7992–8007. https://doi.org/10.1039/c5nr08808a
Liu X, Liu L, Wang Y, Wang X, Ma Y, Li Y (2014) The study on the factors affecting transformation efficiency of E. coli competent cells. Pak J Pharm Sci 27(3 Suppl):679–684
Lu YP, Zhang C, Lv FX, Bie XM, Lu ZX (2012) Study on the electro-transformation conditions of improving transformation efficiency for Bacillus subtilis. Lett Appl Microbiol 55(1):9–14. https://doi.org/10.1111/j.1472-765X.2012.03249.x
Macaluso A, Mettus AM (1991) Efficient transformation of Bacillus thuringiensis requires nonmethylated plasmid DNA. J Bacteriol 173(3):1353–1356. https://doi.org/10.1128/jb.173.3.1353-1356.1991
Macneil DJ (1987) Introduction of plasmid DNA into Streptomyces lividans by electroporation. FEMS Microbiol Lett 42(2-3):239–244
Mandel M, Higa A (1970) Calcium-dependent bacteriophage DNA infection. J Mol Biol 53(1):159–162. https://doi.org/10.1016/0022-2836(70)90051-3
Mao HQ, Roy K, Troung-Le VL, Janes KA, Lin KY, Wang Y, August JT, Leong KW (2001) Chitosan-DNA nanoparticles as gene carriers: synthesis, characterization and transfection efficiency. J Control Release 70(3):399–421
Mcintyre DA, Harlander SK (1989) Genetic transformation of intact Lactococcus lactis subsp. lactis by high-voltage electroporation. Appl Environ Microbiol 55(3):604–610
Mendes GP, Vieira PS, Lanceros-Mendez S, Kluskens LD, Mota M (2015) Transformation of Escherichia coli JM109 using pUC19 by the Yoshida effect. J Microbiol Methods 115:1–5. https://doi.org/10.1016/j.mimet.2015.05.012
Mera A, Araki J, Ohtsuki T, Shimosaka M, Yoshida NJJBB (2011) Chitin nanowhiskers mediate transformation of Escherichia coli by exogenous plasmid DNA. J Biotechnol Biomaterials 1:114
Miller JF, Dower WJ, Tompkins LS (1988) High-voltage electroporation of bacteria: genetic transformation of Campylobacter jejuni with plasmid DNA. Proc Natl Acad Sci U S A 85(3):856–860. https://doi.org/10.1073/pnas.85.3.856
Mitsudome Y, Takahama M, Hirose J, Yoshida N (2014) The use of nano-sized acicular material, sliding friction, and antisense DNA oligonucleotides to silence bacterial genes. AMB Express 4:70. https://doi.org/10.1186/s13568-014-0070-7
Papagianni M, Avramidis N, Filioussis G (2007) High efficiency electrotransformation of Lactococcus lactis spp. lactis cells pretreated with lithium acetate and dithiothreitol. BMC Biotechnol 7:15. https://doi.org/10.1186/1472-6750-7-15
Park MJ, Park MS, Ji GE (2019) Improvement of electroporation-mediated transformation efficiency for a Bifidobacterium strain to a reproducibly high level. J Microbiol Methods 159:112–119. https://doi.org/10.1016/j.mimet.2018.11.019
Prakash GD, Anish RV, Jagadeesh G, Chakravortty D (2011) Bacterial transformation using micro-shock waves. Anal Biochem 419(2):292–301. https://doi.org/10.1016/j.ab.2011.08.038
Qin S, Lin H, Jiang P (2012) Advances in genetic engineering of marine algae. Biotechnol Adv 30(6):1602–1613. https://doi.org/10.1016/j.biotechadv.2012.05.004
Ren J, Lee H, Yoo SM, Yu MS, Park H, Na D (2017) Combined chemical and physical transformation method with RbCl and sepiolite for the transformation of various bacterial species. J Microbiol Methods 135:48–51. https://doi.org/10.1016/j.mimet.2017.02.001
Ren J, Na D, Yoo SM (2018) Optimization of chemico-physical transformation methods for various bacterial species using diverse chemical compounds and nanomaterials. J Biotechnol 288:55–60. https://doi.org/10.1016/j.jbiotec.2018.11.003
Rojas-Chapana JA, Correa-Duarte MA, Ren ZF, Kempa K, Giersig M (2004) Enhanced introduction of gold nanoparticles into vital Acidothiobacillus ferrooxidans by carbon nanotube-based microwave electroporation. Nano Lett 4(5):985–988. https://doi.org/10.1021/nl049699n
Rojas-Chapana J, Troszczynska J, Firkowska I, Morsczeck C, Giersig MJ (2005) Multi-walled carbon nanotubes for plasmid delivery into Escherichia coli cells. Lob Chip 5(5):536–539
Roychoudhury A, Basu S, Sengupta DN (2009) Analysis of comparative efficiencies of different transformation methods of E. coli using two common plasmid vectors. Indian J Biochem Biophys 46(5):395–400
Schenk S, Laddaga RA (1992) Improved method for electroporation of Staphylococcus aureus. FEMS Microbiol Lett 73(1-2):133–138. https://doi.org/10.1016/0378-1097(92)90596-g
Song Y, Hahn T, Thompson IP, Mason TJ, Preston GM, Li G, Paniwnyk L, Huang WE (2007) Ultrasound-mediated DNA transfer for bacteria. Nucleic Acids Res 35(19):e129. https://doi.org/10.1093/nar/gkm710
Tachibana K, Uchida T, Ogawa K, Yamashita N, Tamura K (1999) Induction of cell-membrane porosity by ultrasound. Lancet 353(9162):1409. https://doi.org/10.1016/S0140-6736(99)01244-1
Tan HD, Fu L, Seno M (2010) Optimization of bacterial plasmid transformation using nanomaterials based on the Yoshida effect. Int J Mol Sci 11(12):4962–4973. https://doi.org/10.3390/ijms11124962
Tang X, Nakata Y, Li HO, Zhang M, Gao H, Fujita A, Sakatsume O, Ohta T, Yokoyama K (1994) The optimization of preparations of competent cells for transformation of E. coli. Nucleic Acids Res 22(14):2857–2858. https://doi.org/10.1093/nar/22.14.2857
Tripp VT, Maza JC, Young DD (2013) Development of rapid microwave-mediated and low-temperature bacterial transformations. J Chem Biol 6(3):135–140. https://doi.org/10.1007/s12154-013-0095-4
van der Rest ME, Lange C, Molenaar D (1999) A heat shock following electroporation induces highly efficient transformation of Corynebacterium glutamicum with xenogeneic plasmid DNA. Appl Microbiol Biotechnol 52(4):541–545
Wilharm G, Lepka D, Faber F, Hofmann J, Kerrinnes T, Skiebe E (2010) A simple and rapid method of bacterial transformation. J Microbiol Methods 80(2):215–216. https://doi.org/10.1016/j.mimet.2009.12.002
Wirth R, Friesenegger A, Fiedler S (1989) Transformation of various species of Gram-negative bacteria belonging to 11 different genera by electroporation. Mol Gen Genet 216(1):175–177. https://doi.org/10.1007/Bf00332248
Xue GP, Johnson JS, Dalrymple BP (1999) High osmolarity improves the electro-transformation efficiency of the gram-positive bacteria Bacillus subtilis and Bacillus licheniformis. J Microbiol Methods 34(3):183–191. https://doi.org/10.1016/S0167-7012(98)00087-6
Yi Y, Kuipers OP (2017) Development of an efficient electroporation method for rhizobacterial Bacillus mycoides strains. J Microbiol Methods 133:82–86. https://doi.org/10.1016/j.mimet.2016.12.022
Yoshida N, Sato M (2009) Plasmid uptake by bacteria: a comparison of methods and efficiencies. Appl Microbiol Biotechnol 83(5):791–798. https://doi.org/10.1007/s00253-009-2042-4
Yoshida N, Ikeda T, Yoshida T, Sengoku T, Ogawa K (2001) Chrysotile asbestos fibers mediate transformation of Escherichia coli by exogenous plasmid DNA. FEMS Microbiol Lett 195(2):133–137. https://doi.org/10.1111/j.1574-6968.2001.tb10510.x
Yoshida N, Kodama K, Nakata K, Yamashita M, Miwa T (2002) Escherichia coli cells penetrated by chrysotile fibers are transformed to antibiotic resistance by incorporation of exogenous plasmid DNA. Appl Microbiol Biotechnol 60(4):461–468. https://doi.org/10.1007/s00253-002-1148-8
Yuan L, Wang HW, Yu QA, Wu ZQ, Brash JL, Chen H (2011) “Nano-catalyst” for DNA transformation. J Mater Chem 21(17):6148–6151. https://doi.org/10.1039/c1jm10734h
Yun CH, Bae CS, Ahn T (2016) Transformation of Escherichia coli and protein expression using lipoplex mimicry. Protein Expr Purif 127:68–72. https://doi.org/10.1016/j.pep.2016.07.006
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This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. NRF-2018R1A5A1025077). This work was also supported by an NRF grant funded by the Ministry of Science and ICT (2017R1A2B4004447).
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Ren, J., Karna, S., Lee, HM. et al. Artificial transformation methodologies for improving the efficiency of plasmid DNA transformation and simplifying its use. Appl Microbiol Biotechnol 103, 9205–9215 (2019). https://doi.org/10.1007/s00253-019-10173-x
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DOI: https://doi.org/10.1007/s00253-019-10173-x