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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)

Yeast

 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)

Others

 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)