Streptomyces-Derived Bioactive Pigments: Ecofriendly Source of Bioactive Compounds
Abstract
:1. Introduction
2. Results
2.1. General Findings
2.2. Biosynthetic Pathways and Structure of Streptomyces Pigments
2.3. Pigment Purification
2.4. Stability Tests of the Pigments
2.5. Optimization of the Pigment’s Production
Streptomyces Strain | Type/Color of Pigment | Yield Reported (mg/L) | Optimized Variable | Optimization Result | Ref. |
---|---|---|---|---|---|
Streptomyces sp. MVCS13 | Melanin | 239 | Temperature | 50 °C | [66] |
pH | 7.4 | ||||
L-Tyrosine | 0.75 g/L | ||||
Asparagine | 1.5 g/L | ||||
MgSO4 | 0.25 g/L | ||||
NaCl | 0.75 g/L | ||||
FeSO4 | 0.015 g/L | ||||
Trace salt solution | 1.5 mL/L | ||||
Streptomyces sp. F1 Streptomyces sp. F2 Streptomyces sp. F3 | Melanin | 21,130 | Carbon Source | Starch 1% w/v | [60] |
Nitrogen source | Soyabean 0.2% w/v | ||||
Salinity | 15 ppt | ||||
Temperature | 35 °C | ||||
pH | 7 | ||||
Incubation time | 168 h | ||||
Cheaper source | Sugarcane waste | ||||
Streptomyces sp. PM4 | Red pigment | 1874 | Carbon Source | Maltose (4.06 g/L) | [61] |
Nitrogen source | Peptone (7.34 g/L) | ||||
Yeast extract (4.34 g/L) | |||||
Tyrosine (2.89 g/L) | |||||
Streptomyces sp. AQBWWS1 | Carotenoid | N/A 1 | Carbon Source | Glucose | [71] |
Xylose | |||||
Amino acids | Cystine | ||||
Tryptophan | |||||
NaCl Concentration | 2.50% | ||||
Streptomyces sp. D25 | Yellow pigment | 1225 | Carbon Source | Glucose | [62] |
Fructose | |||||
Nitrogen source | Malt Extract | ||||
pH | 7, 9, 11 | ||||
Temperature | 30 °C, 40 °C | ||||
NaCl Concentration | 1%–5% | ||||
Streptomyces sp. S45 | Pinkish-brown pigment | N/A | Carbon Source | Glucose | [63] |
Rhamnose | |||||
Nitrogen source | Soybean meal | ||||
Minerals | CaCl2 | ||||
pH | 7 | ||||
Temperature | 30 °C | ||||
Streptomyces glaucescens NEAE-H | Melanin | 350 | Incubation period | 6 days | [40] |
Nitrogen source | Protease-peptone (5 g/L) | ||||
Ferric ammonium citrate (0.5 g/L) | |||||
Streptomyces sp. ZL- 24 | Melanin | 138 | NiCl2 | 3.05 Mm | [94] |
FeSO4 | 1.33 g/L | ||||
Soy peptone | 20.31 g/L | ||||
pH | 7 | ||||
Temperature | 30 °C | ||||
Inoculation size | 3% (v/v) | ||||
Incubation period | 5 days | ||||
Streptomyces sp. LS-1 | May be actinorhodin-related compounds. | N/A 1 | Carbon Source | Glucose | [97] |
Nitrogen source | KNO3 | ||||
Streptomyces canaries M8 | Carotenoid | N/A | NaCl Concentration | >10% | [105] |
Streptomyces sp. Ac-1 | Yellow pigment | N/A 2 | Agitation | 100 rpm | [65] |
NaCl Concentration | 2% | ||||
pH | 5 | ||||
Streptomyces sp. Ac-2 | Yellow pigment | N/A 2 | Agitation | Steady state | [65] |
NaCl Concentration | 4% | ||||
pH | 9 | ||||
Streptomyces sp. | Red pigment | N/A | Temperature | 37 °C | [68] |
pH (Solid media) | 10.5 or 7 | ||||
pH (Broth culture) | 7 |
2.6. Bioactivity Results
2.6.1. Antimicrobial Activity
2.6.2. Antioxidant Activity
2.6.3. Cytotoxic Activity
2.7. Applications of Streptomyces Pigments
Streptomyces Pigments with Antibiofilm/Antifouling Potential
2.8. Future Perspectives
3. Materials and Methods
3.1. Databases and Search Strategy
3.2. Selection Procedure
3.3. Data Collection and Tabulation
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Type of Source | Bioactivity | No. Strains | No. Compounds | Ref. |
---|---|---|---|---|
Freshwater (Free-living) | Antimicrobial | 6 | 3 | [64,65] |
Marine (Free-living) | Antimicrobial | 4 | 1 | [60,66] |
Antioxidant | 1 | 1 | [67] | |
Multiple 1 | 1 | N/A 2 | [68] | |
Marine Symbiont | Antimicrobial | 1 | N/A 2 | [69] |
Cytotoxic | 1 | N/A 2 | [61] | |
Multiple 1 | 1 | N/A 2 | [70] | |
N/A 3 | 1 | N/A 2 | [71] | |
Terrestrial Symbiont | N/A 3 | 1 | 3 | [72] |
Soil (Free-living) | Antimicrobial | 11 | 3 | [62,63,73,74,75,76,77,78,79,80,81] |
Antioxidant | 1 | 1 | [82] | |
Cytotoxic | 5 | 2 | [83,84,85,86,87] | |
Multiple 1 | 8 | 6 | [40,88,89,90,91,92,93,94] | |
N/A 3 | 4 | 1 | [95,96,97] | |
N/A 1 | Antimicrobial | 4 | 6 | [98,99,100,101] |
Antioxidant | 1 | 1 | [102] | |
N/A 3 | 15 | 7 | [103,104,105,106,107,108,109,110] |
Streptomyces Strain | Type/Color of Pigment | Yield Reported (mg/L) | Ref. |
---|---|---|---|
Streptomyces sp. MVCS13 | Melanin | 239 | [66] |
Streptomyces sp. F1 | Melanin | 21130 | [60] |
Streptomyces sp. F2 | |||
Streptomyces sp. F3 | |||
Streptomyces sp. | Melanin | 1460 | [67] |
Streptomyces glaucescens NEAE-H | Melanin | 350 | [40] |
Streptomyces sp. ZL-24 | Melanin | 59 to 138 | [94] |
Streptomyces glaucescens KCTC988 | Melanin | 125 1 | [102] |
Streptomyces cavourensis SV 21 | Melanin | 670 | [70] |
Streptomyces parvus BSB49 | Eumelanin | 160 to 240 | [90] |
Streptomyces sp. CWW6 | Streptorubrin A (prodiginine pigment) | 20 | [64] |
Streptomyces sp. WMA-LM31 | Prodigiosin (4) | 30 | [91] |
Streptomyces sp. JS520 | Red pigment | <1 to 139 1 | [88] |
Streptomyces sp. PM4 | Red pigment | 1874 | [61] |
Streptomyces acidiscabies | Naphthoquinone derivatives: Bright yellow compound (5) 2 | 63 | [72] |
Orange compound (6) 3 | 28 | ||
Compound (7) 4 | 2 | ||
Streptomyces sp. D25 | Yellow pigment | 175 to 1225 5 | [62] |
Streptomyces griseoaurantiacus JUACT 01 | Yellow pigment | 4300 | [84] |
Streptomyces aurantiacus AAA5 | Resistomycin (19) (yellow compound) | 52 | [93] |
S. griseus IFO13350 w | Grixazone A (14) | 5 | [98] |
Grixazone B (14) | 2 | ||
Streptomyces sp. A1013Y | Blue pigment | 2 | [82] |
S. coelicolor 100 | Blue pigment | 3000 | [86] |
Streptomyces coelicolor MSIS1 | Red or blue, depending on conditions | 5030 (shake flasks) 9000 (bioreactor) | [92] |
Streptomyces coelescens ATCC 19830 (NP2) | Deep blue | 3000 to 4000 | [96] |
Streptomyces anthocyanicus ATCC 19821 (NP4) | Deep red | 3000 to 4000 | [96] |
Streptomyces Strain | Type/Color of Pigment | Stability Results | Ref. |
---|---|---|---|
Streptomyces vietnamensis sp. nov. GIMV4.0001 | Violet–blue pigment | pH-sensitive | [76] |
Stable at high temperature | |||
Stable under UV light | |||
Streptomyces spectabilis L20190601 | Metacycloprodigiosin (1) | pH-sensitive, red at pH 3.0 and yellow or orange at pH 9.0 | [77] |
Streptomyces sp. A1013Y | TDTA (18) | Stable in a wide range of pHs | [82] |
Thermo-stable | |||
Good stability with indoor incandescent and ultraviolet lights, but unstable with sunlight | |||
Stable with most metal ions and vitamins except Fe3+, Cu2+, and Al3+ | |||
Streptomyces coelicolor 100 | λ-Actinorhodin (12) | pH-sensitive; red at pH < 7, amaranth at pH 7–8, blue at pH > 8 | [86] |
Photo-stable | |||
Thermo-stable | |||
Resistant to oxidants and reducers under acid conditions and to reducers under alkaline conditions. | |||
Stable with food additives | |||
Stable with most metal ions except Fe2+ and Pb2+ | |||
Streptomyces coelicolor MSIS1 | May be one of actinorhodinic acid. | pH-sensitive, red at pH < 7, amaranth at pH 7–8, blue at pH > 8 | [92] |
Streptomyces coelescens ATCC 19830 (NP2) | Deep blue | pH-sensitive | [96] |
Streptomyces anthocyanicus ATCC 19821 (NP4) | Deep red | pH-sensitive | [96] |
Streptomyces sp. LS-1 | May be actinorhodin-related compounds. | Sensitive to low pH | [97] |
Relatively photo-stable | |||
Relatively thermo-stable | |||
Streptomyces parvullus M4 | Red | pH-Stable | [105] |
Streptomyces coelicolor M6 | Red | pH-Stable | [105] |
Streptomyces cyaneofuscatus | Actinomycin X2 (10) | Excellent thermal stability | [69] |
Acid and alkali resistance |
Streptomyces Strains | Source | Positive Antimicrobial Tests | Inhibition Zone (mm) | Ref. |
Streptomyces sp. F1 | Pure colonies | E. coli, Lactobacillus vulgaris, Proteus mirabilus, Vibrio cholera, S. aureus, S. typhi, S. paratyphi, and K. oxytoca | N/A | [60] |
Streptomyces sp. F2 | ||||
Streptomyces sp. F3 | ||||
Streptomyces coeruleorubidus NBRC 12844 | Extract | S. aureus ATCC 1112, B. cereus ATCC1015, P. aeruginosa ATCC 1074, C. freundii ATCC 8090, K. pneumoniae ATCC 1053, and S. marcescens ATCC 14756 | N/A | [73] |
Streptomyces sp. D10 | Fraction | MRSA | 15 | [75] |
VRSA | 20 | |||
E. coli | 15 | |||
Klebsiella sp. | 10 | |||
Streptomyces sp. D25 | Extract | MRSA | 22 1 | [62] |
Streptomyces sp. SAG-85 | Extract | MRSA | 23 2 | [78] |
S. marcescens | 47 2 | |||
Streptomyces sp. ZL-24 | Compound 3 (Melanin) | P. aeruginosa ATCC 9027 | 26–32 | [94] |
E. coli ATCC 8379 | 21–29 | |||
S. aureus ATCC6538 | 15–30 | |||
Mycobacterium smegmatis ATCC 10231 | 17–36 | |||
Streptomyces coelicolor A3(2) | Extract | B. subtilis, S. aureus, E. coli, and Pseudomonas fluorescens | N/A | [101] |
Streptomyces cyaneofuscatus | Compound (Actinomycin X2 (10)) | S. aureus ATCC 6538 | 20 | [69] |
Streptomyces sp. Ac-2 | Extract | P. aeruginosa ATCC 27853 | 18 2 | |
S. aureus ATCC 25923 | 22 2 | [65] | ||
E. coli ATCC 25922 | 21 2 | |||
Streptomyces sp. | Extract 4 | S. aureus MTCC 3160 | 4 | [68] |
B. subtilis MTCC 736 | 10 | |||
E. coli MTCC 1554 | 6 | |||
Vibrio cholera MTCC 3906 | 5 | |||
Streptomyces sp. NS-05 | Extract 5 | E. coli MTCC 739 | 5 2 | [81] |
Proteus vulgaris MTCC 6380 | 8 2 |
Streptomyces Strain (Source/Compound Name) | Positive Antimicrobial Tests | MIC (μg/mL) | Ref. |
---|---|---|---|
S. spectabilis L20190601 1 (Metacycloprodigiosin (1)) | Staphylococcus aureus | <1 | [77] |
Bacillus subtilis | <1 | ||
Escherichia coli | 4 | ||
Streptococcus pyogenes | <1 | ||
Pseudomonas aeruginosa | <1 | ||
Bacillus typhi | 1 | ||
Candida albicans | 2 | ||
Trichophyton rubrum | 64 | ||
Streptomyces sp. JS520 1 (Undecylprodigiosin (2)) | Micrococcus luteus ATCC 379 | 50 | [88] |
Bacillus subtilis ATCC 6633 | 50 | ||
Candida albicans ATCC 10231 | 100 | ||
Candida albicans ATCC 10259 | 200 | ||
Streptomyces sp. JAR6 1 (Undecylprodigiosin (2)) | Salmonella sp. | 150 | [89] |
Bacillus subtilis | 50 | ||
Proteus mirabilis | 80 | ||
Shigella sp. | 100 | ||
Escherichia coli | 170 | ||
Enterococcus sp. | 120 | ||
Klebsiella pneumoniae | 180 | ||
Streptomyces sp. MVCS13 (Melanin) | Bacillus sp. FPO1 | 23 2 | [66] |
Aeromonas sp. FPO2 | 27 2 | ||
Citrobacter sp. FPO3 | 21 2 | ||
Edwardsiella sp. FPO4 | 20 2 | ||
Vibrio sp. FPO5 | 18 2 | ||
Aeromonas sp. FPO6 | 22 2 | ||
Streptomyces aurantiacus AAA5 (Resistomycin (19)) | S. epidermis | 8 2 | [93] |
Enterococcus faecalis | 5 2 | ||
Bacillus subtilis | 25 2 | ||
Staphylococcus aureus | 13 2 | ||
Klebsiella pneumoniae | 16 2 | ||
Shigella sp. | 45 2 | ||
Proteus vulgaris | 70 2 | ||
Escherichia coli | 42 2 | ||
Pseudomonas aeruginosa | 34 2 | ||
Salmonella typhii | 15 2 | ||
Streptomyces sp. MBT27 1 (Actinomycins L1 (8)) 3 | Staphylococcus aureus MB5393 | 4–8 | [80] |
Staphylococcus aureus ATCC29213 | 2–4 | ||
Vancomycin-sensitive Enterococcus faecium | 4–8 | ||
Vancomycin-resistant Enterococcus faecium | 4–8 | ||
S. epidermidis | 4–8 | ||
Escherichia coli ATCC25922 | >128 | ||
Klebsiella pneumoniae ATCC700603 | >128 | ||
Streptomyces sp. MBT27 1 (Actinomycins L2 (9)) 3 | Staphylococcus aureus MB5393 | 8–16 | |
Vancomycin-sensitive Enterococcus faecium | 8–16 | [80] | |
Vancomycin-resistant Enterococcus faecium | 8–16 | ||
Streptomyces parvulus C5-5Y (Fraction F5) | S. aureus | 125 | [74] |
S. epidermidis | 125 | ||
Enterococcus faecalis | 250 | ||
E. coli | 375 | ||
Pseudomonas sp. | 125 | ||
K. pneumoniae | 125 | ||
S. typhi | 125 | ||
Proteus vulgaris | 500 | ||
Shigella sp. | 125 | ||
Streptococcus mutans | 125 | ||
Streptomyces sp. S45 (Fraction) | S. aureus ATCC 29213 | 2 | [63] |
Streptomyces sp. BSE6.1 (Prodigiosin (4)) | S. aureus MTCC1430 | 400 | [99] |
Streptomyces Strain (Source) | Antioxidant Method Evaluated | IC50 (μg/mL) | Equivalence to Vitamin C (μg) | Ref. |
---|---|---|---|---|
Streptomyces sp. A1013Y (TDTA (18)) | DPPH | 41 | <1 | [82] |
ABTS | 14 | 1 | ||
Streptomyces glaucescens KCTC988 (Melanin) | ABTS | 25,080 | N/A | [102] |
ABTS (In presence of copper ions) | 7890 | N/A |
Streptomyces Strain (Source) | Antioxidant Method Evaluated | Concentration Evaluated (μg/mL) | Percentage of Activity | Ref. |
---|---|---|---|---|
Streptomyces sp. (Melanin) | Hydroxyl radical scavenging activity | 500 | 70% | [67] |
Streptomyces glaucescens NEAE-H (Melanin) | ABTS | 100 | 57% | [40] |
Streptomyces parvus BSB49 (Eumelanin) | DPPH | 250 | 88% | [90] |
ABTS | 250 | 75% | ||
Streptomyces sp. WMA-LM31 (Prodigiosin) | DPPH | 10 | 60% | [91] |
Lipid peroxidation inhibition assay | 10 | 25% | ||
In vitro protein oxidation inhibition assay | 10 | 55% | ||
Streptomyces sp. ZL-24 (Melanin) | DPPH | 5 | 65% | [94] |
Hydroxyl radical scavenging activity | 50 | 96% | ||
Superoxide scavenging activity | 10 | 43% | ||
50 | 60% |
Streptomyces Strain (Source) | Antioxidant Method Evaluated | Results of Antioxidant Activity | Ref. |
---|---|---|---|
Streptomyces sp. (Melanin) | Superoxide radical scavenging activity | Moderate scavenger of superoxide radical in vitro and exhibited a strong dose–effect relationship. | [67] |
Reducing power assay | Antioxidant activity of melanin might be due to redox reactions. | ||
Streptomyces sp. JS520 (Undecylprodigiosin (2)) | Ferric thiocyanate method | Undecylprodigiosin (2) did not perform as well as commercially available antioxidant α-tocopherol; however, it was effective in delaying lipid peroxidation. | [88] |
Hydrogen peroxide disc-diffusion assay | Undecylprodigiosin (2) acted as a scavenger of H2O2 that is released through the process of peroxidation. | ||
Streptomyces sp. JAR6 (Undecylprodigiosin (2)) | DPPH | Strain JAR6 was able to reduce compounds to pale yellow hydrazine as a DPPH radical. | [89] |
Streptomyces coelicolor MSIS1 (Extract) | Reducing Power Assay | The pigment had positive results for all the concentrations: 10 mg/mL, 50 mg/mL, and 100 mg/mL. | [92] |
Streptomyces cavourensis SV 21 (Melanin) | DPPH | Acid-treated forms of melanin showed much stronger radical scavenging ability than the intact melanin derivatives. | [70] |
Hydroxyl radical scavenging activity | Rapid oxidation and bleaching of the melanin pigment and thus its capacity to scavenge H2O2 out of the environment. | ||
Streptomyces sp. (Extract) | Free radical scavenging activity | The pigment showed increasing free radical scavenging activity and total antioxidant activity with increased concentrations. | [68] |
Ferric Reducing Antioxidant Power | |||
Hydroxyl Radical Scavenging Activity |
Streptomyces Strain | Pigment | Concentration (μg/mL) | Cell Line | Cell Density (Cells/Well) | Time | IC50 (μg/mL) | Ref. |
---|---|---|---|---|---|---|---|
Streptomyces sp. PM4 | Red pigment | 10, 20, 30, 40, 50 | HT1080 | 2 × 104 | 24 h | 18.5 | [61] |
Hep2 | 15.3 | ||||||
HeLa | 9.6 | ||||||
MCF7 | 8.5 | ||||||
Streptomyces griseoaurantiacus JUACT 01 | Yellow Pigment | 2.5, 5, 10, 20 | HeLa | N/A | 24 h | 5.31 | [84] |
48 h | 2 | ||||||
72 h | 1.8 | ||||||
HepG2 | 24 h | 26.33 | |||||
48 h | 1.75 | ||||||
72 h | 1.41 | ||||||
Human lymphocytes | 24 h, 48 h, 72 h | Any cytotoxicity | |||||
Streptomyces sp. A 16-1 | Red pigment (Fr 5, Fr6, and Fr7) | 0–8 | KB cells | 5 × 104 | 48 h | 0.04 ± 0.005 (Fr 5) | [85] |
0.20 ± 0.02 (Fr 6) | |||||||
0.55 ± 0.05 (Fr 7) | |||||||
PBMCs | Low Cytotoxicity | ||||||
Streptomyces sp. JAR6 | Red pigment (Undecylprodigiosin (2)) | 18.75, 37.5, 75, 150, 300 | HeLa | 1 × 104 | 48 h | 145 | [89] |
Streptomyces glaucescens NEAE-H | Melanin | 1.56, 3.125, 6.25, 12.5, 25, 50, 100 | HFB4 | 1 × 104 | 24 h | 16.34 ± 1.31 | [40] |
WI-38 | 37.05 ± 2.40 | ||||||
WISH | 48.07 ± 2.76 | ||||||
Streptomyces sp. WMA-LM31 | Prodigiosin (4) | 5, 10, 15, 20 | HepG2 | 1 × 104 | 24 h | 12.66 | [91] |
HeLa | 14.83 | ||||||
Streptomyces parvus BSB49 | Eumelanin | 2.72 × 106–1.09 × 107 1 | HeLa | 3 × 104 | 24 h | 5.45 × 106 1 | [90] |
Streptomyces sp. NP4 | Prodigiosin (4) | N/A 2 | HaCat | 1 × 104 | 48 h | No significant cytotoxic effect | [83] |
MRC-5 | |||||||
Streptomyces sp. | N/A | N/A | HT-1080 | N/A | N/A | 202.13 | [68] |
HeLa | 253.86 |
Streptomyces Strain | Pigment Evaluated | Concentration (μg/mL) | Cell Line | Time of Treatment | GI50 (μg/mL) | LC50 (μg/mL) | Ref. |
---|---|---|---|---|---|---|---|
Streptomyces aurantiacus AAA5 | Resistomycin (19) | 5, 0.5, 0.05, 0.005, 0.0005 | HepG2 | N/A | 5 × 10−3 | 1 × 10−2 | [93] |
HeLa | 6 × 10−3 | 1 × 10−2 |
Streptomyces Strain | Type of Assay | N° | Doses (mg/kg) | General Results | LD50 (mg/kg) | Ref. |
---|---|---|---|---|---|---|
S. coelicolor 100 (λ-Actinorhodin (12)) | Mouse acute toxicity trial | First Assay | 1500 and 15,000 | Mouse death resulted from taking an overdose pigment once by oral gavages. | >15,000 | [86] |
Second Assay | 0, 464, 1000, 2155, 4633, 10,000, and 15,000 | Nontoxic substance |
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Sarmiento-Tovar, A.A.; Silva, L.; Sánchez-Suárez, J.; Diaz, L. Streptomyces-Derived Bioactive Pigments: Ecofriendly Source of Bioactive Compounds. Coatings 2022, 12, 1858. https://doi.org/10.3390/coatings12121858
Sarmiento-Tovar AA, Silva L, Sánchez-Suárez J, Diaz L. Streptomyces-Derived Bioactive Pigments: Ecofriendly Source of Bioactive Compounds. Coatings. 2022; 12(12):1858. https://doi.org/10.3390/coatings12121858
Chicago/Turabian StyleSarmiento-Tovar, Aixa A., Laura Silva, Jeysson Sánchez-Suárez, and Luis Diaz. 2022. "Streptomyces-Derived Bioactive Pigments: Ecofriendly Source of Bioactive Compounds" Coatings 12, no. 12: 1858. https://doi.org/10.3390/coatings12121858