Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickens

ABSTRACT: We recently reported a stable Bacillus subtilis-carrying chicken NK-lysin peptide (B. subtilis-cNK-2) as an effective oral delivery system of an antimicrobial peptide to the gut with therapeutic effect against Eimeria parasites in broiler chickens. To further investigate the effects of a h...

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Main Authors: Samiru S. Wickramasuriya, Inkyung Park, Youngsub Lee, Luciana M. Richer, Chris Przybyszewski, Cyril G. Gay, Jolieke G. van Oosterwijk, Hyun S. Lillehoj
Format: Article
Language:English
Published: Elsevier 2023-05-01
Series:Poultry Science
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Online Access:http://www.sciencedirect.com/science/article/pii/S0032579123001141
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author Samiru S. Wickramasuriya
Inkyung Park
Youngsub Lee
Luciana M. Richer
Chris Przybyszewski
Cyril G. Gay
Jolieke G. van Oosterwijk
Hyun S. Lillehoj
author_facet Samiru S. Wickramasuriya
Inkyung Park
Youngsub Lee
Luciana M. Richer
Chris Przybyszewski
Cyril G. Gay
Jolieke G. van Oosterwijk
Hyun S. Lillehoj
author_sort Samiru S. Wickramasuriya
collection DOAJ
description ABSTRACT: We recently reported a stable Bacillus subtilis-carrying chicken NK-lysin peptide (B. subtilis-cNK-2) as an effective oral delivery system of an antimicrobial peptide to the gut with therapeutic effect against Eimeria parasites in broiler chickens. To further investigate the effects of a higher dose of an oral B. subtilis-cNK-2 treatment on coccidiosis, intestinal health, and gut microbiota composition, 100 (14-day-old) broiler chickens were allocated into 4 treatment groups in a randomized design: 1) uninfected control (CON), 2) infected control without B. subtilis (NC), 3) B. subtilis with empty vector (EV), and 4) B. subtilis with cNK-2 (NK). All chickens, except the CON group, were infected with 5,000 sporulated Eimeria acervulina (E. acervulina) oocysts on d 15. Chickens given B. subtilis (EV and NK) were orally gavaged (1 × 1012 cfu/mL) daily from d 14 to 18. Growth performances were measured on d 6, 9, and 13 postinfection (dpi). Spleen and duodenal samples were collected on 6 dpi to assess the gut microbiota, and gene expressions of gut integrity and local inflammation makers. Fecal samples were collected from 6 to 9 dpi to enumerate oocyst shedding. Blood samples were collected on 13 dpi to measure the serum 3–1E antibody levels. Chickens in the NK group showed significantly improved (P < 0.05) growth performance, gut integrity, reduced fecal oocyst shedding and mucosal immunity compared to NC. Interestingly, there was a distinct shift in the gut microbiota profile in the NK group compared to that of NC and EV chickens. Upon challenge with E. acervulina, the percentage of Firmicutes was reduced and that of Cyanobacteria increased. In NK chickens, however, the ratio between Firmicutes and Cyanobacteria was not affected and was similar to that of CON chickens. Taken together, NK treatment restored dysbiosis incurred by E. acervulina infection and showed the general protective effects of orally delivered B. subtilis-cNK-2 on coccidiosis infection. This includes reduction of fecal oocyst shedding, enhancement of local protective immunity, and maintenance of gut microbiota homeostasis in broiler chickens.
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spelling doaj.art-d4328b1e216c45de9bc2bd7b7c1f8cca2023-04-29T14:45:36ZengElsevierPoultry Science0032-57912023-05-011025102590Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickensSamiru S. Wickramasuriya0Inkyung Park1Youngsub Lee2Luciana M. Richer3Chris Przybyszewski4Cyril G. Gay5Jolieke G. van Oosterwijk6Hyun S. Lillehoj7Animal Bioscience and Biotechnology Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USAAnimal Bioscience and Biotechnology Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USAAnimal Bioscience and Biotechnology Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USAUS Biologic, Inc., Memphis, TN 38103, USAUS Biologic, Inc., Memphis, TN 38103, USAOffice of National Program-Animal Health, US Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USAUS Biologic, Inc., Memphis, TN 38103, USAAnimal Bioscience and Biotechnology Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USA; Corresponding author:ABSTRACT: We recently reported a stable Bacillus subtilis-carrying chicken NK-lysin peptide (B. subtilis-cNK-2) as an effective oral delivery system of an antimicrobial peptide to the gut with therapeutic effect against Eimeria parasites in broiler chickens. To further investigate the effects of a higher dose of an oral B. subtilis-cNK-2 treatment on coccidiosis, intestinal health, and gut microbiota composition, 100 (14-day-old) broiler chickens were allocated into 4 treatment groups in a randomized design: 1) uninfected control (CON), 2) infected control without B. subtilis (NC), 3) B. subtilis with empty vector (EV), and 4) B. subtilis with cNK-2 (NK). All chickens, except the CON group, were infected with 5,000 sporulated Eimeria acervulina (E. acervulina) oocysts on d 15. Chickens given B. subtilis (EV and NK) were orally gavaged (1 × 1012 cfu/mL) daily from d 14 to 18. Growth performances were measured on d 6, 9, and 13 postinfection (dpi). Spleen and duodenal samples were collected on 6 dpi to assess the gut microbiota, and gene expressions of gut integrity and local inflammation makers. Fecal samples were collected from 6 to 9 dpi to enumerate oocyst shedding. Blood samples were collected on 13 dpi to measure the serum 3–1E antibody levels. Chickens in the NK group showed significantly improved (P < 0.05) growth performance, gut integrity, reduced fecal oocyst shedding and mucosal immunity compared to NC. Interestingly, there was a distinct shift in the gut microbiota profile in the NK group compared to that of NC and EV chickens. Upon challenge with E. acervulina, the percentage of Firmicutes was reduced and that of Cyanobacteria increased. In NK chickens, however, the ratio between Firmicutes and Cyanobacteria was not affected and was similar to that of CON chickens. Taken together, NK treatment restored dysbiosis incurred by E. acervulina infection and showed the general protective effects of orally delivered B. subtilis-cNK-2 on coccidiosis infection. This includes reduction of fecal oocyst shedding, enhancement of local protective immunity, and maintenance of gut microbiota homeostasis in broiler chickens.http://www.sciencedirect.com/science/article/pii/S0032579123001141NK-lysinchickenBacillus subtiliscoccidiosisantimicrobial peptide
spellingShingle Samiru S. Wickramasuriya
Inkyung Park
Youngsub Lee
Luciana M. Richer
Chris Przybyszewski
Cyril G. Gay
Jolieke G. van Oosterwijk
Hyun S. Lillehoj
Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickens
Poultry Science
NK-lysin
chicken
Bacillus subtilis
coccidiosis
antimicrobial peptide
title Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickens
title_full Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickens
title_fullStr Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickens
title_full_unstemmed Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickens
title_short Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickens
title_sort orally delivered bacillus subtilis expressing chicken nk 2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis infected broiler chickens
topic NK-lysin
chicken
Bacillus subtilis
coccidiosis
antimicrobial peptide
url http://www.sciencedirect.com/science/article/pii/S0032579123001141
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