Gut-Derived Lactic Acid Bacteria from Cotton Bollworm Exhibit Efficient Gossypol Degradation and Probiotic Potential During Solid-State Fermentation of Cottonseed Meal
Abstract
1. Introduction
2. Materials and Methods
2.1. Materials and Reagents
2.2. Isolation of Gossypol-Degrading Bacteria from Helicoverpa Armigera Larval Gut
2.3. Identification of Gossypol-Degrading Bacteria from Helicoverpa armigera Gut
2.4. Determination of the Growth Curve and Free Gossypol Degradation Rate for the Target Strain
2.5. Artificial Gastric Juice and Bile Salt Tolerance
2.6. Temperature Tolerance Assessment
2.7. Evaluation of Cell Surface Properties
2.8. Auto-Aggregation Assessment
2.9. Hemolytic and Antioxidant Assessment
2.10. Assessment of Antibacterial Activity
2.11. Antibiotic Susceptibility Testing
2.12. Solid-State Fermentation of Cottonseed Meal by the Target Strain
2.13. Statistical Analysis
3. Results
3.1. Preliminary Characterisation of Isolated Bacteria
3.2. 16S rDNA Sequencing and Phylogenetic Analysis of Bacterial Strains
3.3. Physiological and Biochemical Characteristics of the Strain
3.4. Growth Curves and Acid Production Curves of Four Strains of Lactic Acid Bacteria
3.5. Tolerance of Four Strains of Lactic Acid Bacteria to Artificial Gastrointestinal Environments
3.6. Thermal Tolerance of the Four Lactic Acid Bacterial Strains
3.7. Auto-Aggregation and Surface Hydrophobicity of Four Lactic Acid Bacterial Strains
3.8. Antibacterial Activity of Four Lactic Acid Bacterial Strains
3.9. Hemolytic Activity and Antioxidant Capacity of Four Lactic Acid Bacterial Strains
3.10. Drug Sensitivity of Four Strains of Lactic Acid Bacteria
3.11. Solid-State Fermentation of Cottonseed Meal and Gossypol Detoxification, as Well as Nutritional Quality Indicators
4. Discussion
4.1. Isolation and Gossypol Degradation Capacity of Lactic Acid Bacteria Strains
4.2. Gastrointestinal Tolerance and Heat Resistance
4.3. Auto-Aggregation and Cell Surface Hydrophobicity
4.4. Antioxidant and Antimicrobial Activities
4.5. Safety Assessment: Antibiotic Susceptibility and Hemolytic Activity
4.6. Solid-State Fermentation and Nutritional Improvement of CSM
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Media | Composition |
---|---|
LB | 1%yeast extract, 2%peptone, 1%NaCl, 2% agar |
MRS | 1%peptone, 0.8%Beef extract, 0.4%Yeast, 2%glucose, 0.2%K2HPO4, 0.2%(NH4)2HC6H5O7, 0.5%CH3COONa, 0.02%MgSO4, 0.004%MgSO4, 0.1%Tween 80 |
MRSA | 1%peptone, 0.8%Beef extract, 0.4%Yeast, 2%glucose, 0.2%K2HPO4, 0.2%(NH4)2HC6H5O7, 0.5%CH3COONa, 0.02%MgSO4, 0.004%MgSO4, 0.1%Tween 80, 2%agar |
GMRS | 0.1%gossypol, 1%peptone, 0.8%Beef extract, 0.4%Yeast, 0.2%K2HPO4, 0.2%(NH4)2HC6H5O7, 0.5%CH3COONa, 0.02%MgSO4, 0.004%MgSO4, 0.1%Tween 80 |
GMRSA | 0.2%gossypol, 1%peptone, 0.8%Beef extract, 0.4%Yeast, 0.2%K2HPO4, 0.2%(NH4)2HC6H5O7, 0.5%CH3COONa, 0.02%MgSO4, 0.004%MgSO4, 0.1%Tween 80, 2% agar |
Strains | Closest Match | GenBank Accession No. | Similarity/% |
---|---|---|---|
GM-NP | Pediococcus acidilactici | NR042057.1 | 99.184% |
GM-P | Pediococcus acidilactici | NR042057.1 | 99.515% |
GM-2 | Weissella confusa | NR040816.1 | 99.861% |
GM-3 | Mammaliicoccus sciuri | NR041327.1 | 99.859% |
GM-4 | Enterococcus innesii | NR181755.1 | 99.718% |
GM-5 | Enterococcus innesii | NR181755.1 | 99.858% |
GM-6 | Enterococcus faecalis | NR115765.1 | 100.000% |
GM-7 | Klebsiella oxytoca | NR118853.1 | 99.861% |
GM-8 | Klebsiella oxytoca | NR118853.1 | 99.645% |
GM-9 | Klebsiella oxytoca | NR118853.1 | 99.363% |
GM-10 | Klebsiella oxytoca | NR118853.1 | 99.153% |
Item | P. acidilactici GM-NP | P. acidilactici GM-P | E. faecalis GM-6 | W. confusa GM-2 |
---|---|---|---|---|
Aesculin | + | + | + | − |
1%Sodium Hippurat | + | + | + | + |
Cellobiose | − | − | + | + |
Maltose | − | − | + | + |
Mannose | − | − | + | + |
Salicin | − | − | + | + |
Sorbitol | − | − | + | + |
Sucrose | − | − | + | + |
Raffinose | − | − | + | + |
Inulin | − | − | − | + |
Lactose | − | − | + | + |
Items | Cell Numbers (Log CFU/mL) | |||
---|---|---|---|---|
P. acidilactici GM-NP | P. acidilactici GM-P | E. faecalis GM-6 | W. confusa GM-2 | |
Artificial gastric juice tolerance | ||||
Initial cell number | 9.71 ± 0.03 | 9.36 ± 0.02 | 8.28 ± 0.05 | 8.52 ± 0.05 |
pH2.5, 0.3% pepsin, 1.5 h | 6.98 ± 0.10 | 6.95 ± 0.09 | 5.91 ± 0.20 | 5.82 ± 0.17 |
Survival rate (%) | 71.83 a ± 1.10 | 74.28 a ± 1.06 | 71.35 a ± 2.40 | 68.31 b ± 2.07 |
Artificial intestinal fluid tolerance | ||||
Initial cell number | 9.43 ± 0.02 | 9.40 ± 0.07 | 8.62 ± 0.02 | 8.37 ± 0.01 |
pH6.8, 1% trypsin, three h | 8.48 ± 0.16 | 8.52 ± 0.07 | 7.68 ± 0.07 | 7.48 ± 0.07 |
Survival rate (%) | 89.93 a ± 1.50 | 90.64 a ± 0.86 | 89.10 a ± 0.86 | 85.98 b ± 0.53 |
Artificial bile salt tolerance | ||||
Initial cell number | 8.66 ± 0.03 | 8.69 ± 0.02 | 8.56 ± 0.03 | 8.53 ± 0.02 |
0.3% Ox Gall, four h | 6.78 ± 0.13 | 7.36 ± 0.20 | 5.87 ± 0.05 | 6.26 ± 0.15 |
Survival rate (%) | 78.11 b ± 1.32 | 84.76 a ± 2.16 | 68.54 d ± 0.78 | 73.46 c ± 1.79 |
Items | Survival Rate (%) | |||
---|---|---|---|---|
P. acidilactici GM-NP | P. acidilactici GM-P | E. faecalis GM-6 | W. confusa GM-2 | |
Heat treatment time/min | ||||
60 °C, 5 min | 67.23 b ± 0.54 | 66.36 bc ± 0.64 | 72.20 a ± 0.47 | 60.94 c ± 0.40 |
60 °C, 10 min | 60.29 b ± 0.9 | 57.44 c ± 0.97 | 63.06 a ± 0.87 | 52.51 d ± 0.42 |
60 °C, 15 min | 48.56 c ± 0.86 | 46.72 c ± 0.81 | 53.83 a ± 1.26 | 43.96 d ± 0.35 |
70 °C, 5 min | 57.74 b ± 0.46 | 52.53 c ± 0.74 | 60.86 a ± 0.58 | 51.64 c ± 0.48 |
70 °C, 10 min | 52.14 c ± 0.69 | 49.01 d ± 0.99 | 56.91 a ± 1.45 | 44.69 e ± 0.32 |
70 °C, 15 min | 33.56 b ± 1.14 | 32.79 b ± 0.72 | 39.04 a ± 0.41 | 31.31 b ± 0.38 |
80 °C, 5 min | 34.81 b ± 0.38 | 31.87 c ± 1.00 | 37.97 a ± 0.91 | 25.75 d ± 0.64 |
80 °C, 10 min | 6.68 bc ± 0.40 | 5.17 c ± 0.22 | 9.04 a ± 0.87 | 7.10 bc ± 0.82 |
80 °C, 15 min | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 |
90 °C, 5 min | 17.72 b ± 0.69 | 15.87 bc ± 0.33 | 21.49 a ± 1.14 | 15.32 c ± 0.53 |
90 °C, 10 min | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 |
90 °C, 15 min | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 |
Items | Strains | |||
---|---|---|---|---|
P. acidilactici GM-NP | P. acidilactici GM-P | E. faecalis GM-6 | W. confusa GM-2 | |
Assessment of auto-aggregation ability (%) | ||||
8 h | 48.60 a ± 1.01 | 46.77 a ± 0.55 | 37.21 c ± 1.11 | 43.39 b ± 1.27 |
24 h | 82.96 a ± 0.95 | 81.10 a ± 1.80 | 72.89 b ± 1.76 | 74.34 b ± 0.73 |
Cell surface properties (%) | 54.45 b ± 1.62 | 51.63 bc ± 1.95 | 47.92 c ± 1.91 | 41.60 d ± 2.29 |
Pathogens | Antimicrobial Activities | |||
---|---|---|---|---|
P. acidilactici GM-NP | P. acidilactici GM-P | E. faecalis GM-6 | W. confusa GM-2 | |
E. coli ATCC25922 | ★★★ | ★★★★ | ★★ | ★ |
S. aureus ATCC6538 | ★★★ | ★★★ | ★★ | ★ |
Salmonella ATCC14028 | ★★★★ | ★★★★ | ★★ | - |
P. aeruginosa ATCC9027 | ★★★ | ★★★ | ★★ | ★ |
Items | Strains | |||
---|---|---|---|---|
P. acidilactici GM-NP | P. acidilactici GM-P | E. faecalis GM-6 | W. confusa GM-2 | |
Hemolytic activity | γ | γ | γ | γ |
Free radical scavenging rate (%) (DPPH) | 43.81 a ± 1.11 | 45.29 a ± 1.26 | 28.73 c ± 1.32 | 37.62 b ± 0.50 |
Antibiotic Susceptibility | Strains | |||
---|---|---|---|---|
P. acidilactici GM-NP | P. acidilactici GM-P | E. faecalis GM-6 | W. confusa GM-2 | |
Cefalotin | S | S | I | S |
Clindamycin | S | S | R | S |
Chloramphenicol | I | S | I | S |
Penicillin | R | R | S | S |
Rifampicin | S | S | S | S |
Erythromycin | S | S | I | S |
Ampicillin | S | S | I | S |
Tetracycline | S | S | I | S |
Levofloxacin | R | R | I | S |
Gentamicin | R | R | I | S |
Streptomycin | R | R | I | R |
Polymyxin B | R | R | R | R |
Enrofloxacin | R | R | S | I |
Ciprofloxacin | R | R | I | R |
Ofloxacin | R | R | I | I |
Items | CON | P. acidilactici GM-NP | P. acidilactici GM-P | E. faecalis GM-6 | W. confusa GM-2 |
---|---|---|---|---|---|
CP (%) | 49.77 b ± 0.16 | 53.43 a ± 1.05 | 53.39 a ± 0.77 | 54.35 a ± 0.56 | 52.83 a ± 0.65 |
ASP (%) | 3.49 b ± 0.21 | 6.17 a ± 0.13 | 6.10 a ± 0.06 | 6.08 a ± 0.07 | 6.48 a ± 0.72 |
NDF (%) | 36.76 a ± 1.52 | 28.94 cd ± 0.71 | 30.01 cd ± 1.29 | 29.40 cd ± 1.13 | 31.97 bc ± 0.59 |
ADF (%) | 27.53 a ± 0.73 | 19.87 d ± 1.44 | 18.83 cd ± 0.27 | 22.31 bc ± 0.75 | 23.28 b ± 0.78 |
Crude fat (%) | 1.30 a ± 0.06 | 0.71 b ± 0.04 | 0.51 b ± 0.13 | 0.44 b ± 0.03 | 0.59 b ± 0.10 |
Ash (%) | 6.72 ± 0.58 | 7.26 ± 0.49 | 6.41 ± 0.11 | 6.99 ± 0.32 | 7.17 ± 0.14 |
Ca (%) | 0.32 ± 0.02 | 0.37 ± 0.03 | 0.36 ± 0.03 | 0.34 ± 0.04 | 0.30 ± 0.08 |
P (%) | 0.70 ± 0.05 | 0.68 ± 0.04 | 0.79 ± 0.07 | 0.70 ± 0.01 | 0.72 ± 0.09 |
pH | 6.39 a ± 0.03 | 5.99 b ± 0.22 | 5.58 C ± 0.02 | 5.92 b ± 0.04 | 6.11 b ± 0.05 |
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Li, S.; Deng, S.; Zhang, P.; Lu, Q.; Pu, W.; Ma, M.; Li, S.; Zhang, W.; Chen, C. Gut-Derived Lactic Acid Bacteria from Cotton Bollworm Exhibit Efficient Gossypol Degradation and Probiotic Potential During Solid-State Fermentation of Cottonseed Meal. Fermentation 2025, 11, 598. https://doi.org/10.3390/fermentation11100598
Li S, Deng S, Zhang P, Lu Q, Pu W, Ma M, Li S, Zhang W, Chen C. Gut-Derived Lactic Acid Bacteria from Cotton Bollworm Exhibit Efficient Gossypol Degradation and Probiotic Potential During Solid-State Fermentation of Cottonseed Meal. Fermentation. 2025; 11(10):598. https://doi.org/10.3390/fermentation11100598
Chicago/Turabian StyleLi, Sijin, Shangya Deng, Peng Zhang, Qicheng Lu, Wei Pu, Mingyu Ma, Shu Li, Wenju Zhang, and Cheng Chen. 2025. "Gut-Derived Lactic Acid Bacteria from Cotton Bollworm Exhibit Efficient Gossypol Degradation and Probiotic Potential During Solid-State Fermentation of Cottonseed Meal" Fermentation 11, no. 10: 598. https://doi.org/10.3390/fermentation11100598
APA StyleLi, S., Deng, S., Zhang, P., Lu, Q., Pu, W., Ma, M., Li, S., Zhang, W., & Chen, C. (2025). Gut-Derived Lactic Acid Bacteria from Cotton Bollworm Exhibit Efficient Gossypol Degradation and Probiotic Potential During Solid-State Fermentation of Cottonseed Meal. Fermentation, 11(10), 598. https://doi.org/10.3390/fermentation11100598