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Table 1 Achievements of ARTP mutagenesis in biotechnology (2010–2018)

From: Microbial mutagenesis by atmospheric and room-temperature plasma (ARTP): the latest development

Microorganism Compound/property Improvement Final results Refs
Gram-negative bacteria
 Acetobacter pasteurianus Acetic acid, ethanol tolerance Increased ethanol tolerance, 385.7% acetic acid increase 32.83 g l−1 acetic acid titer at 11% ethanol Wu et al. (2015)
 Corynebacterium glutamicum l-Arginine 43.79% production increase Final titer 45.36 g l−1 (24 h), 0.571 g l−1 h−1 Cheng et al. (2016)
 Enterobacter aerogenes Hydrogen 26.4% increase (yield per mole glucose) 4.901 l hydrogen per g dry cell weight Lu et al. (2011)
 Enterobacter cloacae NaCl tolerance Increased NaCl tolerance and increased TPH degradation Tolerance to 7.5% NaCl while 3.17% to 7.94% TPH degradation increase Hua et al. (2010)
Cadmium tolerance Increased cadmium tolerance Normal growth at 0.25 g l−1 cadmium Xu et al. (2017a)
 Escherichia coli Succinic acid 3.12-fold growth increase, 2.5-fold productivity increase 27.9 g l−1 succinic acid, with a rate of 0.38 g l−1 h−1) Ma et al. (2016a)
Trans-4-hydroxy-l-proline Enhanced production from glycerol by a recombinant E. coli BSL21 strain 1.24 g l−1 from 20 g l−1 glycerol (12 h, batch culture) Wang et al. (2016a)
Anaerobic growth, succinic acid Anaerobic growth without yeast extract and tryptone Conversion of 35 g l−1 glucose to 25.2 g l−1 succinic acid Liu et al. (2013)
l-Lysine 21% increase 136.51 g l−1 Wang et al. (2016c)
l-Lysine Resistance to rifampicin, s-2-aminoethyl-l-cysteine and l-threonine auxothropic Strain for study was obtained by ARTP Xu et al. (2016)
Hemicellulose usage, succinic acid Simultaneous usage of glucose and xylose under anaerobic conditions 23.1 g l−1, yield 0.85 g g−1 sugar mixture Bao et al. (2014)
Succinic acid 1.33-fold increase in ATP during xylose fermentation 21.1 g l−1, 76% yield Jiang et al. (2014)
 Methylosinus trichosporium Growth rate, methane monooxygenase > twofold growth rate/methane monooxygenase activity ~ 38 U g−1 dry cell weight Li et al. (2012)
 Pseudomonas sp. Esterase Original strain for study was obtained by ARTP Dong et al. (2015)
Esterase 4.45-fold increased production 39.84 U ml−1 Dong et al. (2017a)
 Pseudomonas putida Nicotinic acid 42% increase 189 g l−1 Dong et al. (2017b)
 Sphingomonas sp. High temperature-tolerant production of Welan gum High temperature-tolerant production 26.8 g  l−1 Zhu et al. (2014b)
Gram-positive bacteria
 Actinomyces Acarbose 62.5% increase 2.974 g l−1 Ren et al. (2017)
 Arthrobacter Dextranase 19 and 30% increase in activity, slight change of pH and temp optima   Wang et al. (2014b)
 Bacillus amyloliquefaciens Menaquinone-7 4.25-fold increase 30.2 mg l−1 Xu and Zhang (2017)
 Bacillus coagulans l-Lactic acid Strain for this study was obtained by ARTP Zheng et al. (2014)
l-Lactic acid Two mutants with 42.75 and 46.1% increase, respectively 3.84 and 3.93 g l−1 Lv et al. (2016)
Inhibitor tolerance, l-lactic acid Increase of inhibitor tolerance Up to 45.39 g l−1 depending on the substrate Jiang et al. (2016)
 Bacillus subtilis Amylase, recombinant protein secretion 35% yield increase, 8.8% productivity increase, 37.9% extracellular protein concentration increase 196.35 U ml−1, 1.23 U mg−1 h−1, 0.4 g l−1 Ma et al. (2015)
Amylase 1.34-fold activity increase 1.57 U mg−1 h−1 production rate Ma et al. (2016b)
Surfactin 5.4-fold increase 0.4736 g l−1 Zhu et al. (2014a)
Surfactin Strain for this study was obtained by ARTP Liu et al. (2014)
Uridine 4.4- and 8.7-fold increase in shake flask (30 h shake flask/48 h fed batch) 5.7 and 30.3 g l−1 Fan et al. (2017)
 Clostridium beijerinckii Electricity production (microbial fuel cell) 2.38-fold increase in voltage, 1.39-fold output power increase 68.98 mW m−2 and 0.19 V Liu et al. (2015c)
ABE, butanol tolerance 33% higher ABE production, 25% higher butanol production, butanol tolerance 13.71 g l−1 butanol, 4.9 g l−1 acetone, and 0.19 g l−1 ethanol Kong et al. (2016)
Butanol 32% butanol titer increase 3.1 g l−1 acetone, 10.4 g l−1 butanol, 0.2 g l−1 ethanol in 72 h Guo et al. (2011)
Ferulic acid tolerance Ferulic acid tolerance up to 0.9 g l−1   Liu et al. (2016)
 Clostridium acetobutylicum Acetone, butanol, ethanol 31% increased butanol production 11.3 g l−1 Li et al. (2014)
 Mycobacterium neoaurum 4-Androstene-3,17-dione 30% increase, increase from 48.3% to 60.3% molar yield 6.28 g  l−1 Liu et al. (2015b)
 Sporolactobacillus sp. d-Lactic acid 41.84% increase 1.39 g l−1 h−1 Sun et al. (2015)
 Streptomyces avermitilis Avermectins Total avermectin increase by 18%, avermectin B1a increase by 40% 6.7–8.3 g l−1 total and 3.3–3.9 g l−1 avermectin B1a Wang et al. (2010)
Avermectins 18.9% increase 4.378 g l−1 Cao et al. (2018)
 Streptomyces albulus ε-Poly-l-lysine Fourfold increase 1.59 g l−1 Zong et al. (2012)
ε-Poly-l-lysine Up to 9.5% increase after initial ARTP Up to 2.52 g l−1 Wang et al. (2016b)
 Streptomyces bingchenggensis 5-Oxomilbemycins A3/A4 2.9-fold increase 3.89 g l−1 Wang et al. (2014a)
 Streptomyces sp. ε-Poly-l-lysine 66.3% increase 2.91 g l−1 Wang et al. (2015)
 Streptomyces fungicidicus Enduracidin 1.65-fold increase 1.58 g l−1 Zhang et al. (2015a)
 Streptomyces mobaraensis Transglutaminase 27% increase 5.85 U ml−1 Jiang et al. (2017)
Filamentous fungi
 Aspergillus niger Gluconate 12.1, 15.5 and 32.8% production rate increase in 3 mutants 0.067, 0.065 and 0.077 mol l−1 h−1, respectively Shi et al. (2015)
Glucoamylase 70% higher enzyme yield 2.2 × 103 U ml−1 Zhu et al. (2017)
 Aspergillus terreus Itaconic acid, inhibitor tolerance Growth in hydrolysate 19.3 g l−1 with a 36.01% sugar conversion Li et al. (2016b)
 Blakeslea trispora Lycopene 55% increase 26.4 mg g−1 dry biomass Qiang et al. (2014)
 Glarea lozoyensis Pneumocandin B0 1.39-fold increase 1134 mg l−1 Qin et al. (2016)
 Mortierella alpina Arachidonic acid 40.61% concentration increase 5.09 g l−1, increase of ARA from 38.99 to 45.61% of total fatty acids Li et al. (2015)
 Trichoderma viride Cellulase 1.97-fold activity improvement 4.17 U g−1 dry weight Xu et al. (2012)
Cellulase Increase of filter paper activity (2.38-fold), carboxymethyl cellulase (2.61-fold), β-glucosidase (2.18-fold), cellobiohydrolase (2.27-fold) 106.60, 2261.54, 29.22 and 60.90 U mg−1, respectively Xu et al. (2011)
 Auerobasidium pullulans Polymalic acid 13.8% titer enhancement 128.2 g l−1 Li et al. (2016a)
 Candida glabrata Pyruvate 32.2% higher production using a cheap nitrogen source 42.3 g l−1 Luo et al. (2017b)
Overproduction of polysaccharides was found Luo et al. (2017a)
 Cryptococcus spec. Ionic liquid tolerance Ionic liquid tolerance (imidazolium-based) Xu et al. (2017b)
 Pichia anomala Sugar alcohol 32.3% higher concentration 47.1 g l−1 from 100 g l−1 glucose Zhang et al. (2015b)
 Rhodosporidium toruloides Inhibitor tolerance Exploration of inhibitor tolerance by omics Qi et al. (2017)
Inhibitor tolerance, lipids Inhibitors resistance, 14–31% higher lipid content Accumulation of up to 60% intracellular lipids of dry cell weight Kitahara et al. (2014)
Inhibitor tolerance Growth in hydrolysate possible Qi et al. (2014)
Carotenoids, lipids   0.23 g lipid × g−1 and 0.75 mg carotenoid × g−1 (per cell dry weight) Zhang et al. (2016)
 Rhodotorula mucilaginosa Carotenoids 67% higher concentration 14.47 mg l−1 Wang et al. (2017)
 Saccharomyces cerevisiae Methanol reduction 72.54% decreased methanol concentration in wine 30.7 mg l−1 methanol Liang et al. (2014)
Glutathione 56.76% production increase   Xu et al. (2017c)
 Yarrowia lipolytica α-ketoglutaric acid Strains for omics study were obtained by ARTP Zeng et al. (2016)
α-ketoglutaric acid 51.8% titer increase 11.83 g l−1 Zeng et al. (2015)
Erythritol 34% increase 64.8 g l−1 from 100 g l−1 glycerol, yield 0.65 g g−1, productivity 1.05 g l−1 h−1 Liu et al. (2017b)
 Chlorella pyrenoidosa (Plant) Biomass 32.08% growth increase, 22.07% dry weight increase, 16.85% lipid productivity increase OD680 = 1.62; 0.52 g l−1 dry weight Cao et al. (2017)
 Crypthecodinium cohnii (Dinoflagellate) Extracellular polysaccharides 33.85% volumetric yield increase, 85.35% EPS yield on biomass increase, 57.17% EPS yield on glucose increase 1.02 g l−1 EPS volumetric yield, 0.39 g g−1 EPS yield on biomass, 94 mg g−1 EPS yield on glucose Liu et al. (2015a)
Growth rate, lipid content 24.32% higher growth rate, 7.05% higher lipid content   Liu et al. (2017a)
 Spirulina platensis (Cyanobacterium) Biomass Enhancement in growth rate, carbohydrate content, chlorophyll content and CO2 fixation in 3 mutants Growth rate (0.118 g l−1 day−1 in 3-A10), carbohydrate content (30.7% in 3-B2), chlorophyll content (3.82 mg g−1) and CO2 fixation (0.120 g CO2 g−1 day−1 in 3-B2) Tan et al. (2015)
Growth, carbohydrate content 78% carbohydrate content increase 0.331 g−1 g−1 Fang et al. (2013)
Astaxanthin 196% increase 45.88 µg g−1 An et al. (2017)
 Microbial community Butanol 34% titer increase 15.63 g l−1 Gu et al. (2017)