Can Probiotics Improve the Environmental Microbiome and Resistome of Commercial Poultry Production?
Abstract
:1. Introduction
2. Material and Methods
2.1. Housing, Litter and Treatments for Birds Raised on Commercial Poultry Farms
House | Flock 1 | Flock 2 | Flock 3 | Flock 4 | Flock 5 |
---|---|---|---|---|---|
A and B | No AGP | No AGP | No AGP | No AGP | No AGP |
C and D | |||||
Starter- | Flavomycin | Flavomycin | Flavomycin | Flavomycin | Flavomycin |
Grower- | Flavomycin | Flavomycin | Flavomycin | Flavomycin | Flavomycin |
Finisher- | Flavomycin | Virginiamycin | Virginiamycin | Virginiamycin | Flavomycin |
2.2. Housing, Litter and Treatments for Birds Raised in Research Facilities
Product (Manufacturer) | Composition | Dosage and administration |
---|---|---|
All-Lac (Alltech Inc., Lexington, KY, USA) | Lactobacillus, Enterococcus, and Pediococcus | 5 g in 600 mL water for 2,000 birds |
All-Lac + BioMos (Alltech Inc., Lexington, KY, USA) | All-Lac plus a mannan oligosaccharide derived from the cell wall of Saccharomyces cerevisiae | All-Lac: 5 g in 600 mL water for 2,000 birds, BioMos: 2 kg/T of starter feed for 10 days, 1 kg/T of grower feed to 21 days, 0.5 kg/T of finisher feed to 35 days |
Aviguard (Microbial Developments Ltd, Malvern, UK) | Undefined bacteria collected and cultured from chicken cecum contents | 1 pack in 1,000 mL water for 2,000 birds |
Primalac (Star-Labs, Clarksdale, MO, USA) | Lactobacillus species, Enterococcus faecium, and Bifidobacterium thermophilum | 1 kg/T of starter to 10 days, 1 kg /T of grower to 21 days, 0.5 kg/T of finisher to 35 days |
2.3. Quantifying Tetracycline-Resistant Coliforms in Litter and Fecal Samples
2.4. Collection of the Bacterial Pellet
2.5. DNA Extraction
2.6. PCR Detection of Antibiotic Resistance Genes and Salmonella
2.7. Microbial Community Structure as Defined by Terminal Restriction Fragment Length Polymorphism (T-RFLP) of 16S rRNA PCR Amplicons
2.8. PCR Amplification of 16S rRNA for Pyrosequencing
2.9. Statistical and Sequence Analysis
3. Results and Discussion
3.1. Effects of Antibiotic Usage Changes on Microbial Community Structure of Commercial Poultry Litter
3.2. Effects of Antibiotic Usage Changes on the Prevalence of Antibiotic Resistance Genes within the Bacterial Community of Commercial Poultry Litter
No antibiotic | AGP | |||
---|---|---|---|---|
Shannon Diversity Index | Richness | Shannon Diversity Index | Richness | |
Flock 1 | 3.94 ± 0.57 | 22.25 ± 4.6 | 4.11 ± 0.99 | 26.75 ± 13.1 |
Flock 2 | 3.68 ± 0.76 | 17.5 ± 8.3 | 3.76 ± 0.94 | 19.75 ± 13.3 |
Flock 3 | 3.85 ± 0.37 | 22.5 ± 6.4 | 3.66 ± 0.46 | 18.5 ± 3 |
Flock 4 | 3.42 ± 0.42 | 18 ± 5.6 | 3.38 ± 0.06 | 12.25 ± 8.73 |
Flock 5 | 3.27 ± 0.77 | 13.75 ± 6.2 | 3.83 ± 0.12 | 21.75 ± 6.8 |
Bacterial genus predicted by T-RFLP peak | No antibiotic * | AGP * | ||
---|---|---|---|---|
Farm 1 | Farm 2 | Farm 1 | Farm 2 | |
Aerococcus, Bacteroides, Streptococcus | 7.79% | 1.76% | 8.58% | 1.45% |
Clostridia, Ruminococcus, Eubacterium, Fecalobacterium | 10.98% | 13.70% | 10.49% | 11.62% |
Corynebacterium, Lactobacillus | 16.99% | 31.00% | 17.53% | 35.16% |
Corynebacterium, Brachybacterium, Joetgalibacillus/Salinicoccus | 13.48% | 6.35% | 11.91% | 8.16% |
Lactobacillus | 18.90% | 3.87% | 19.86% | 3.63% |
Staphylococcus sp. | 7.20% | 4.75% | 7.26% | 3.62% |
Unknown | 11.65% | 27.32% | 12.11% | 24.80% |
Yania, Clostridia | 9.21% | 12.37% | 10.45% | 11.49% |
TREATMENT * | ermA | ermB | ermC | tetM | tetO | vatA | vatB | vatD | vatE | vgaB | intI1 | ||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Farm | Farm | Farm | Farm | Farm | Farm | Farm | Farm | Farm | Farm | Farm | |||||||||||||||||||||||
1 | 2 | 3 | 1 | 2 | 3 | 1 | 2 | 3 | 1 | 2 | 3 | 1 | 2 | 3 | 1 | 2 | 3 | 1 | 2 | 3 | 1 | 2 | 1 | 2 | 3 | 1 | 2 | 3 | 1 | 2 | 3 | ||
Flock 1 | Flavomycin | + | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | + | + | - | - | - | - | - | + | - | - | + | + | + | + |
+ | + | + | + | + | + | - | - | - | - | + | + | - | - | + | - | - | + | - | + | - | - | - | - | - | + | - | - | + | + | + | + | ||
NONE | + | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | + | + | - | - | - | - | + | + | - | - | + | + | + | + | |
+ | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | + | - | - | - | - | + | + | - | - | + | + | + | + | ||
Flock 2 | Flavomycin + Virginiamycin | - | + | + | + | + | + | - | - | - | + | - | + | - | - | + | - | - | + | + | + | - | - | - | - | + | + | - | - | - | + | + | + |
+ | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | + | - | - | - | - | - | + | - | - | + | + | + | + | ||
NONE | + | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | + | + | - | - | - | - | + | + | - | - | + | + | + | + | |
+ | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | + | - | - | - | - | - | + | - | - | + | + | + | + | ||
Flock 3 | Flavomycin + Virginiamycin | + | + | + | + | + | - | - | - | - | + | + | + | - | - | + | + | - | + | - | + | - | - | - | - | + | + | - | - | + | + | + | + |
+ | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | - | - | - | - | - | + | + | - | - | + | + | + | + | ||
NONE | + | + | + | + | + | - | - | - | - | + | - | + | - | - | + | - | - | + | - | - | - | - | - | - | - | + | - | - | + | + | + | + | |
+ | + | + | + | + | + | - | - | - | + | - | + | - | - | + | - | - | + | - | - | - | - | - | - | - | + | - | - | + | + | + | + | ||
Flock 4 | Flavomycin + Virginiamycin | + | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | - | - | - | - | - | - | + | - | - | + | - | + | + |
+ | + | + | + | + | + | - | - | - | + | - | + | - | - | + | - | - | + | - | - | - | - | - | - | - | + | - | - | + | + | + | + | ||
NONE | + | - | + | + | + | + | - | - | - | - | - | + | - | - | + | - | - | + | - | - | - | - | - | - | + | + | - | - | + | + | + | + | |
- | - | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | + | - | - | - | - | - | + | - | - | + | + | + | + | ||
Flock 5 | Flavomycin | - | + | + | - | + | + | - | - | - | + | + | + | - | - | + | - | - | + | + | + | - | - | - | - | - | - | - | - | + | + | + | + |
- | + | + | - | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | + | - | - | - | - | + | + | - | - | + | + | + | + | ||
NONE | - | + | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | + | - | - | - | - | + | + | - | - | + | + | + | + | |
+ | - | + | + | + | + | - | - | - | + | + | + | - | - | + | - | - | + | - | + | - | - | - | - | + | - | - | - | + | + | + | + | ||
Total prevalence | AGP | 90% | 90% | 0% | 90% | 33% | 33% | 33% | 0% | 43% | 30% | 97% | |||||||||||||||||||||
NONE | 83% | 97% | 0% | 87% | 33% | 33% | 30% | 0% | 50% | 33% | 100% |
3.3. Composition of Poultry Litter in Research Facilities Housing Birds Treated with Prebiotics or Probiotics
Genera | Control | All-Lac | All-Lac + BioMos | Aviguard | Primalac |
---|---|---|---|---|---|
Total sequences | 19,806 | 39,357 | 91,219 | 48,226 | 76,363 |
Number of genera | 85 | 135 | 154 | 119 | 211 |
Staphylococcus * | 5,605 (28.3) | 9,603 (24.4) | 32,171 (35.3) | 14,648 (30.4) | 19,138 (25.1) |
Corynebacterium ** | 4,222 (21.3) | 9,483 (24.1) | 16,872 (18.5) | 7,839 (16.3) | 13,259 (17.4) |
Lactobacillus * | 1,955 (9.9) | 3,925 (10.0) | 9,424 (10.3) | 4,767 (9.9) | 7,775 (10.2) |
Salinicoccus * | 1,851 (9.3) | 3,412 (8.7) | 8,407 (9.2) | 5,802 (12.0) | 5,274 (6.9) |
Yaniella * | 1,272 (6.4) | 1,796 (4.6) | 5,610 (6.2) | 2,467 (5.1) | 4,793 (6.3) |
Brachybacterium ** | 1,077 (5.4) | 1,796 (4.6) | 3,534 (3.9) | 2,698 (5.6) | 3,066 (4.0) |
Brevibacterium ** | 948 (4.8) | 1,371 (3.5) | 2,666 (2.9) | 2,758 (5.7) | 2,660 (3.5) |
Facklamia * | 337 (1.7) | 1,291 (3.3) | 1,640 (1.8) | 796 (1.7) | 1,498 (2.0) |
Clostridium XI * | 295 (1.5) | 424 (1.1) | 0 (0.0) | 556 (1.2) | 1,091 (1.4) |
Enterococcus * | 0 (0.0) | 548 (1.4) | 0 (0.0) | 623 (1.3) | 974 (1.3) |
Atopostipes * | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1,345 (1.8) |
Streptococcus * | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1,260 (1.7) |
Treatment | Sample | Number of sequences | Number of genera | Shannon Diversity Index | Firmicutes (%) | Actinobacteria (%) | Proteobacteria (%) | Most abundant genus |
---|---|---|---|---|---|---|---|---|
Control | First | 3181 | 40 | 2.43 (±0.05) | 78.2 | 21.8 | 0.00 | Staphylococcus (37.6%) |
Last | 3068 | 43 | 2.72 (±0.05) | 61 | 38.9 | 0.00 | Corynebacterium (24.7%) | |
All-Lac | First | 2244 | 57 | 3.10 (±0.14) | 68.6 | 25.4 | 4.50 | Salinicoccus (24.4%) |
Last | 2888 | 25 | 2.36 (±0.05) | 68.7 | 30.8 | 0.00 | Staphylococcus (30.4%) | |
All-Lac + BioMos | First | 8949 | 72 | 2.59 (±0.03) | 78.1 | 21.8 | 0.05 | Staphylococcus (30.7%) |
Last | 587 | 24 | 1.89 (±0.13) | 47.4 | 52.6 | 0.00 | Corynebacterium (48%) | |
Aviguard | First | 4480 | 42 | 2.56 (±0.03) | 88.4 | 11.5 | 0.04 | Salinicoccus (49.9%) |
Last | 4468 | 42 | 2.40 (±0.03) | 64.1 | 35.1 | 0.72 | Corynebacterium (30%) | |
Primalac | First | 2938 | 37 | 2.75 (±0.05) | 66.4 | 32.5 | 0.27 | Salinicoccus (32%) |
Last | 2660 | 34 | 2.58 (±0.04) | 70.8 | 28 | 0.56 | Staphylococcus (30%) |
3.4. Effect of Time and Probiotic or Prebiotic Treatments on Pathogen Abundance in Litter
Flock | Control | All-Lac | All-Lac + BioMos | Aviguard | Primalac |
---|---|---|---|---|---|
1 | + | - | - | + | - |
2 | + | + | - | - | - |
3 | - | + | - | + | - |
4 | - | + | + | + | - |
3.5. Effects of Probiotics and Prebiotics on the Prevalence of Antibiotic Resistance within the Bacterial Community of Poultry Litter
Treatment | # intI1 copies * ± SD | # eubacterial genomes * ± SD | intI1: eubacterial genome ratio * | Mean Ratio ± SD |
---|---|---|---|---|
Control Flock 1 | 6.30 × 107 ± 9.69 × 106 | 1.15 × 109 ± 1.23 × 107 | 0.0547 | |
Flock 2 | 2.69 × 107 ± 2.90 × 106 | 1.26 × 109 ± 3.03 × 108 | 0.0214 | |
Flock 3 | 3.11 × 106 ± 1.77 × 105 | 5.25 × 108 ± 1.05 × 107 | 0.0059 | |
Flock 4 | 2.97 × 107 ± 8.46 × 106 | 1.04 × 109 ± 5.30 × 107 | 0.0286 | 0.0277 ± 0.0204 |
All-Lac Flock 1 | 3.30 × 107 ± 5.87 × 105 | 1.10 × 109 ± 2.54 × 108 | 0.0300 | |
Flock 2 | 1.59 × 107 ± 9.31 × 106 | 5.23 × 108 ± 2.74 × 107 | 0.0304 | |
Flock 3 | 3.15 × 107 ± 6.79 × 106 | 1.29 × 109 ± 2.25 × 108 | 0.0244 | |
Flock 4 | 4.41 × 107 ± 7.29 × 106 | 2.07 × 109 ± 1.06 × 109 | 0.0213 | 0.0265 ± 0.0044 |
All-Lac + BioMos Flock 1 | 2.31 × 107 ± 4.12 × 106 | 7.26 × 108 ± 3.76 × 107 | 0.0318 | |
Flock 2 | 3.38 × 107 ± 1.44 × 106 | 1.28 × 109 ± 1.29 × 108 | 0.0263 | |
Flock 3 | 2.81 × 107 ± 2.09 × 106 | 1.10 × 109 ± 3.63 × 107 | 0.0254 | |
Flock 4 | 2.37 × 107 ± 4.03 × 106 | 1.05 × 109 ± 4.58 × 107 | 0.0224 | 0.0265 ± 0.0039 |
Aviguard Flock 1 | 3.25 × 107 ± 1.06 × 106 | 1.14 × 109 ± 2. 06 × 108 | 0.0286 | |
Flock 2 | 3.56 × 106 ± 2.02 × 105 | 7.80 × 107 ± 4.63 × 106 | 0.0456 | |
Flock 3 | 5.98 × 107 ± 3.42 × 106 | 8.17 × 108 ± 2.67 × 107 | 0.0732 | |
Flock 4 | 4.18 × 107 ± 2.91 × 106 | 1.06 × 109 ± 2.16 × 108 | 0.0393 | 0.0467 ± 0.0190 |
Primalac Flock 1 | 5.69 × 107 ± 2.06 × 107 | 7.06 × 108 ± 6.80 × 107 | 0.0806 | |
Flock 2 | 6.94 × 107 ± 2.61 × 107 | 1.33 × 109 ± 4.24 × 105 | 0.0520 | |
Flock 3 | 2.76 × 107 ± 3.54 × 105 | 8.64 × 108 ± 6.04 × 107 | 0.0320 | |
Flock 4 | 1.12 × 107 ± 7.07 × 103 | 4.27 × 108 ± 5.83 × 107 | 0.0263 | 0.0477 ± 0.0245 |
4. Conclusions
Acknowledgments
Conflicts of Interest
References
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Pedroso, A.A.; Hurley-Bacon, A.L.; Zedek, A.S.; Kwan, T.W.; Jordan, A.P.O.; Avellaneda, G.; Hofacre, C.L.; Oakley, B.B.; Collett, S.R.; Maurer, J.J.; et al. Can Probiotics Improve the Environmental Microbiome and Resistome of Commercial Poultry Production? Int. J. Environ. Res. Public Health 2013, 10, 4534-4559. https://doi.org/10.3390/ijerph10104534
Pedroso AA, Hurley-Bacon AL, Zedek AS, Kwan TW, Jordan APO, Avellaneda G, Hofacre CL, Oakley BB, Collett SR, Maurer JJ, et al. Can Probiotics Improve the Environmental Microbiome and Resistome of Commercial Poultry Production? International Journal of Environmental Research and Public Health. 2013; 10(10):4534-4559. https://doi.org/10.3390/ijerph10104534
Chicago/Turabian StylePedroso, Adriana A., Anne L. Hurley-Bacon, Andrea S. Zedek, Tiffany W. Kwan, Andrea P. O. Jordan, Gloria Avellaneda, Charles L. Hofacre, Brian B. Oakley, Stephen R. Collett, John J. Maurer, and et al. 2013. "Can Probiotics Improve the Environmental Microbiome and Resistome of Commercial Poultry Production?" International Journal of Environmental Research and Public Health 10, no. 10: 4534-4559. https://doi.org/10.3390/ijerph10104534