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A Multiomic Analysis of Chicken Serum Revealed the Modulation of Host Factors Due to Campylobacter jejuni Colonization and In-Water Supplementation of Eugenol Nanoemulsion

SIMPLE SUMMARY: Campylobacter jejuni, a normal flora in the chicken gut, is one of the most common causes of bacterial gastroenteritis in humans, affecting approximately 95 million people worldwide. Carcass contamination at the processing plant through the leakage of gut contents can lead to foodbor...

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Autores principales: Wagle, Basanta R., Quach, Austin, Yeo, Seungjun, Assumpcao, Anna L. F. V., Arsi, Komala, Donoghue, Annie M., Jesudhasan, Palmy R. R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9951679/
https://www.ncbi.nlm.nih.gov/pubmed/36830346
http://dx.doi.org/10.3390/ani13040559
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author Wagle, Basanta R.
Quach, Austin
Yeo, Seungjun
Assumpcao, Anna L. F. V.
Arsi, Komala
Donoghue, Annie M.
Jesudhasan, Palmy R. R.
author_facet Wagle, Basanta R.
Quach, Austin
Yeo, Seungjun
Assumpcao, Anna L. F. V.
Arsi, Komala
Donoghue, Annie M.
Jesudhasan, Palmy R. R.
author_sort Wagle, Basanta R.
collection PubMed
description SIMPLE SUMMARY: Campylobacter jejuni, a normal flora in the chicken gut, is one of the most common causes of bacterial gastroenteritis in humans, affecting approximately 95 million people worldwide. Carcass contamination at the processing plant through the leakage of gut contents can lead to foodborne illnesses when contaminated poultry or poultry products are consumed or improperly handled. This study focused on identifying host factors modulated by Campylobacter colonization in untreated chickens and those treated with phytochemical eugenol. We used a novel LCMS-based multiomics technology to identify the factors modulating the colonization of C. jejuni in broiler chickens. Three groups of broiler chickens were used: (1) negative control, (2) positive control, and (3) eugenol nanoemulsion (EGNE) treatment–supplemented with 0.125% EGNE in the water. Based on the multiomic analysis (proteins, lipids, and metabolites), we identified a few key host factors that were modulated with the colonization of C. jejuni. ABSTRACT: Campylobacter jejuni is a foodborne pathogen that causes campylobacteriosis globally, affecting ~95 million people worldwide. Most C. jejuni infections involve consuming and/or handling improperly cooked poultry meat. To better understand chicken host factors modulated by Campylobacter colonization, we explored a novel LCMS-based multiomic technology using three experimental groups: (1) negative control, (2) positive control, and (3) eugenol nanoemulsion (EGNE) treatment (supplemented with 0.125% EGNE in the water) of broiler chickens (n = 10 birds/group). Birds in groups two and three were challenged with C. jejuni on day 7, and serum samples were collected from all groups on day 14. Using this multiomic analysis, we identified 1216 analytes (275 compounds, seven inorganics, 407 lipids, and 527 proteins). The colonization of C. jejuni significantly upregulated CREG1, creatinine, and 3-[2-(3-Hydroxyphenyl) ethyl]-5-methoxyphenol and downregulated sphingosine, SP d18:1, high mobility group protein B3, phosphatidylcholines (PC) P-20:0_16:0, PC 11:0_26:1, and PC 13:0_26:2. We found that 5-hydroxyindole-3-acetic acid significantly increased with the EGNE treatment when compared to the positive and negative controls. Additionally, the treatment increased several metabolites when compared to the negative controls. In conclusion, this study revealed several potential targets to control Campylobacter in broiler chickens.
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spelling pubmed-99516792023-02-25 A Multiomic Analysis of Chicken Serum Revealed the Modulation of Host Factors Due to Campylobacter jejuni Colonization and In-Water Supplementation of Eugenol Nanoemulsion Wagle, Basanta R. Quach, Austin Yeo, Seungjun Assumpcao, Anna L. F. V. Arsi, Komala Donoghue, Annie M. Jesudhasan, Palmy R. R. Animals (Basel) Communication SIMPLE SUMMARY: Campylobacter jejuni, a normal flora in the chicken gut, is one of the most common causes of bacterial gastroenteritis in humans, affecting approximately 95 million people worldwide. Carcass contamination at the processing plant through the leakage of gut contents can lead to foodborne illnesses when contaminated poultry or poultry products are consumed or improperly handled. This study focused on identifying host factors modulated by Campylobacter colonization in untreated chickens and those treated with phytochemical eugenol. We used a novel LCMS-based multiomics technology to identify the factors modulating the colonization of C. jejuni in broiler chickens. Three groups of broiler chickens were used: (1) negative control, (2) positive control, and (3) eugenol nanoemulsion (EGNE) treatment–supplemented with 0.125% EGNE in the water. Based on the multiomic analysis (proteins, lipids, and metabolites), we identified a few key host factors that were modulated with the colonization of C. jejuni. ABSTRACT: Campylobacter jejuni is a foodborne pathogen that causes campylobacteriosis globally, affecting ~95 million people worldwide. Most C. jejuni infections involve consuming and/or handling improperly cooked poultry meat. To better understand chicken host factors modulated by Campylobacter colonization, we explored a novel LCMS-based multiomic technology using three experimental groups: (1) negative control, (2) positive control, and (3) eugenol nanoemulsion (EGNE) treatment (supplemented with 0.125% EGNE in the water) of broiler chickens (n = 10 birds/group). Birds in groups two and three were challenged with C. jejuni on day 7, and serum samples were collected from all groups on day 14. Using this multiomic analysis, we identified 1216 analytes (275 compounds, seven inorganics, 407 lipids, and 527 proteins). The colonization of C. jejuni significantly upregulated CREG1, creatinine, and 3-[2-(3-Hydroxyphenyl) ethyl]-5-methoxyphenol and downregulated sphingosine, SP d18:1, high mobility group protein B3, phosphatidylcholines (PC) P-20:0_16:0, PC 11:0_26:1, and PC 13:0_26:2. We found that 5-hydroxyindole-3-acetic acid significantly increased with the EGNE treatment when compared to the positive and negative controls. Additionally, the treatment increased several metabolites when compared to the negative controls. In conclusion, this study revealed several potential targets to control Campylobacter in broiler chickens. MDPI 2023-02-05 /pmc/articles/PMC9951679/ /pubmed/36830346 http://dx.doi.org/10.3390/ani13040559 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Communication
Wagle, Basanta R.
Quach, Austin
Yeo, Seungjun
Assumpcao, Anna L. F. V.
Arsi, Komala
Donoghue, Annie M.
Jesudhasan, Palmy R. R.
A Multiomic Analysis of Chicken Serum Revealed the Modulation of Host Factors Due to Campylobacter jejuni Colonization and In-Water Supplementation of Eugenol Nanoemulsion
title A Multiomic Analysis of Chicken Serum Revealed the Modulation of Host Factors Due to Campylobacter jejuni Colonization and In-Water Supplementation of Eugenol Nanoemulsion
title_full A Multiomic Analysis of Chicken Serum Revealed the Modulation of Host Factors Due to Campylobacter jejuni Colonization and In-Water Supplementation of Eugenol Nanoemulsion
title_fullStr A Multiomic Analysis of Chicken Serum Revealed the Modulation of Host Factors Due to Campylobacter jejuni Colonization and In-Water Supplementation of Eugenol Nanoemulsion
title_full_unstemmed A Multiomic Analysis of Chicken Serum Revealed the Modulation of Host Factors Due to Campylobacter jejuni Colonization and In-Water Supplementation of Eugenol Nanoemulsion
title_short A Multiomic Analysis of Chicken Serum Revealed the Modulation of Host Factors Due to Campylobacter jejuni Colonization and In-Water Supplementation of Eugenol Nanoemulsion
title_sort multiomic analysis of chicken serum revealed the modulation of host factors due to campylobacter jejuni colonization and in-water supplementation of eugenol nanoemulsion
topic Communication
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9951679/
https://www.ncbi.nlm.nih.gov/pubmed/36830346
http://dx.doi.org/10.3390/ani13040559
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