Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome
ABSTRACT: Climate change is one of the most significant challenges facing the sustainability of global poultry production. Stress resulting from extreme temperature swings, including cold snaps, is a major concern for food production birds. Despite being well-documented in mammals, the effect of env...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2024-03-01
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| Series: | Poultry Science |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0032579123009136 |
| _version_ | 1797291812938842112 |
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| author | Joshua M. Lyte Julia Eckenberger James Keane Kelsy Robinson Tyler Bacon Anna Luiza Facchetti V Assumpcao Annie M. Donoghue Rohana Liyanage Karrie M. Daniels Valentina Caputi Mark Lyte |
| author_facet | Joshua M. Lyte Julia Eckenberger James Keane Kelsy Robinson Tyler Bacon Anna Luiza Facchetti V Assumpcao Annie M. Donoghue Rohana Liyanage Karrie M. Daniels Valentina Caputi Mark Lyte |
| author_sort | Joshua M. Lyte |
| collection | DOAJ |
| description | ABSTRACT: Climate change is one of the most significant challenges facing the sustainability of global poultry production. Stress resulting from extreme temperature swings, including cold snaps, is a major concern for food production birds. Despite being well-documented in mammals, the effect of environmental stress on enteric neurophysiology and concomitant impact on host-microbiome interactions remains poorly understood in birds. As early life stressors may imprint long-term adaptive changes in the host, the present study sought to determine whether cold temperature stress, a prominent form of early life stress in chickens, elicits changes in enteric stress-related neurochemical concentrations that coincide with compositional and functional changes in the microbiome that persist into the later life of the bird. Chicks were, or were not, subjected to cold ambient temperature stress during the first week post-hatch and then remained at normal temperature for the remainder of the study. 16S rRNA gene and shallow shotgun metagenomic analyses demonstrated taxonomic and functional divergence between the cecal microbiomes of control and cold stressed chickens that persisted for weeks following cessation of the stressor. Enteric concentrations of serotonin, norepinephrine, and other monoamine neurochemicals were elevated (P < 0.05) in both cecal tissue and luminal content of cold stressed chickens. Significant (P < 0.05) associations were identified between cecal neurochemical concentrations and microbial taxa, suggesting host enteric neurochemical responses to environmental stress may shape the cecal microbiome. These findings demonstrate for the first time that early life exposure to environmental temperature stress can change the developmental trajectory of both the chicken cecal microbiome and host neuroendocrine enteric physiology. As many neurochemicals serve as interkingdom signaling molecules, the relationships identified here could be exploited to control the impact of climate change-driven stress on avian enteric host-microbe interactions. |
| first_indexed | 2024-03-07T19:43:09Z |
| format | Article |
| id | doaj.art-1afcbbc3ee6746e18bac190d24997609 |
| institution | Directory Open Access Journal |
| issn | 0032-5791 |
| language | English |
| last_indexed | 2024-03-07T19:43:09Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Poultry Science |
| spelling | doaj.art-1afcbbc3ee6746e18bac190d249976092024-02-29T05:17:12ZengElsevierPoultry Science0032-57912024-03-011033103393Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiomeJoshua M. Lyte0Julia Eckenberger1James Keane2Kelsy Robinson3Tyler Bacon4Anna Luiza Facchetti V Assumpcao5Annie M. Donoghue6Rohana Liyanage7Karrie M. Daniels8Valentina Caputi9Mark Lyte10Poultry Production and Product Safety Research Unit, Agricultural Research Service, United States Department of Agriculture, Fayetteville, AR 72701, USA; Corresponding author:APC Microbiome Ireland, University College Cork, Cork, Ireland; School of Microbiology, University College Cork, Cork, IrelandEIRNA Bio Ltd, Cork, IrelandPoultry Research Unit, Agricultural Research Service, United States Department of Agriculture Mississippi State, MS 39762, USAPoultry Production and Product Safety Research Unit, Agricultural Research Service, United States Department of Agriculture, Fayetteville, AR 72701, USAPoultry Production and Product Safety Research Unit, Agricultural Research Service, United States Department of Agriculture, Fayetteville, AR 72701, USA; APC Microbiome Ireland, University College Cork, Cork, Ireland; School of Microbiology, University College Cork, Cork, Ireland; EIRNA Bio Ltd, Cork, Ireland; Poultry Research Unit, Agricultural Research Service, United States Department of Agriculture Mississippi State, MS 39762, USA; Department of Poultry Science, University of Arkansas, Fayetteville, AR 72701, USA; Statewide Mass Spectrometry Lab, University of Arkansas, Fayetteville, AR 72701, USA; Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USAPoultry Production and Product Safety Research Unit, Agricultural Research Service, United States Department of Agriculture, Fayetteville, AR 72701, USAStatewide Mass Spectrometry Lab, University of Arkansas, Fayetteville, AR 72701, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USAPoultry Production and Product Safety Research Unit, Agricultural Research Service, United States Department of Agriculture, Fayetteville, AR 72701, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USAABSTRACT: Climate change is one of the most significant challenges facing the sustainability of global poultry production. Stress resulting from extreme temperature swings, including cold snaps, is a major concern for food production birds. Despite being well-documented in mammals, the effect of environmental stress on enteric neurophysiology and concomitant impact on host-microbiome interactions remains poorly understood in birds. As early life stressors may imprint long-term adaptive changes in the host, the present study sought to determine whether cold temperature stress, a prominent form of early life stress in chickens, elicits changes in enteric stress-related neurochemical concentrations that coincide with compositional and functional changes in the microbiome that persist into the later life of the bird. Chicks were, or were not, subjected to cold ambient temperature stress during the first week post-hatch and then remained at normal temperature for the remainder of the study. 16S rRNA gene and shallow shotgun metagenomic analyses demonstrated taxonomic and functional divergence between the cecal microbiomes of control and cold stressed chickens that persisted for weeks following cessation of the stressor. Enteric concentrations of serotonin, norepinephrine, and other monoamine neurochemicals were elevated (P < 0.05) in both cecal tissue and luminal content of cold stressed chickens. Significant (P < 0.05) associations were identified between cecal neurochemical concentrations and microbial taxa, suggesting host enteric neurochemical responses to environmental stress may shape the cecal microbiome. These findings demonstrate for the first time that early life exposure to environmental temperature stress can change the developmental trajectory of both the chicken cecal microbiome and host neuroendocrine enteric physiology. As many neurochemicals serve as interkingdom signaling molecules, the relationships identified here could be exploited to control the impact of climate change-driven stress on avian enteric host-microbe interactions.http://www.sciencedirect.com/science/article/pii/S0032579123009136stressmicrobiomeavianneurochemicalgut |
| spellingShingle | Joshua M. Lyte Julia Eckenberger James Keane Kelsy Robinson Tyler Bacon Anna Luiza Facchetti V Assumpcao Annie M. Donoghue Rohana Liyanage Karrie M. Daniels Valentina Caputi Mark Lyte Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome Poultry Science stress microbiome avian neurochemical gut |
| title | Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome |
| title_full | Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome |
| title_fullStr | Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome |
| title_full_unstemmed | Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome |
| title_short | Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome |
| title_sort | cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome |
| topic | stress microbiome avian neurochemical gut |
| url | http://www.sciencedirect.com/science/article/pii/S0032579123009136 |
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