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Randomized Controlled Trial
. 2024 Feb 23;19(2):e0296350.
doi: 10.1371/journal.pone.0296350. eCollection 2024.

Host transcriptome response to heat stress and Eimeria maxima infection in meat-type chickens

Ahmed F A Ghareeb  1 , James C Foutz  1 , Gustavo H Schneiders  1 , Jennifer N Richter  1 , Marie C Milfort  1 , Alberta L Fuller  1 , Romdhane Rekaya  2 , Samuel E Aggrey  1
Affiliations
Randomized Controlled Trial

Host transcriptome response to heat stress and Eimeria maxima infection in meat-type chickens

Ahmed F A Ghareeb et al. PLoS One. .

Abstract

Eimeria (E.) maxima parasite infects chickens' midgut disrupting the jejunal and ileal mucosa causing high morbidity and mortality. Heat stress (HS) is a seasonal stressor that impacts biological functions leading to poor performance. This study elucidates how HS, E. maxima infection, and their combination affect the ileum transcriptome. Two-hundred and forty 2-week-old males Ross708 chickens were randomly allocated into four treatment groups: thermoneutral-control (TNc), thermoneutral-infected (TNi), heat-stress control (HSc), and heat stress-infected (HSi), with 6 replicates each of 10 birds. Infected groups received 200x103 sporulated E. maxima oocysts/bird, and heat-treated groups were raised at 35°C. At 6-day post-treatment, ileums of five randomly selected chickens per group were sampled, RNA was extracted and sequenced. A total of 413, 3377, 1908, and 2304 DEGs were identified when applying the comparisons: TNc vs HSc, TNc vs TNi, HSi vs HSc, and TNi vs HSi, respectively, at cutoff ≥1.2-fold change (FDR: q<0.05). HSc vs TNc showed upregulation of lipid metabolic pathways and degradation/metabolism of multiple amino acids; and downregulation of most immune-related and protein synthesis pathways. TNc vs TNi displayed upregulation of most of immune-associated pathways and eukaryotic mRNA maturation pathways; and downregulation of fatty acid metabolism and multiple amino acid metabolism pathways including tryptophan. Comparing HSi versus HSc and TNi revealed that combining the two stressors restored the expression of some cellular functions, e.g., oxidative phosphorylation and protein synthesis; and downregulate immune response pathways associated with E. maxima infection. During E. maxima infection under HS the calcium signaling pathway was downregulated, including genes responsible for increasing the cytoplasmic calcium concentration; and tryptophan metabolism was upregulated, including genes that contribute to catabolizing tryptophan through serotonin and indole pathways; which might result in reducing the cytoplasmic pool of nutrients and calcium available for the parasite to scavenge and consequently might affect the parasite's reproductive ability.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Number of DEGs of each pairwise comparison at 6 dpi of chickens infected with Eimeria maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected.
Fig 2
Fig 2
A. Heatmap of the top ~60 DEGs of TNc vs. HSc, calculated as Log 2 relative hit counts of the comparison between the chickens exposed to HS (HSc) and their thermoneutral control (TNc) at 6 day-post-treatment. B. The top KEGG pathways of TNc vs. HSc, based on the pathway term significance (α≤0.1) of the comparison between the chickens exposed to HS (HSc) and their thermoneutral control (TNc) at 6 day-post-treatment. The green squares and arrowheads depict the downregulated pathways and genes, respectively. The red circles and arrowheads depict the upregulated pathways and genes, respectively. The bigger size squares and circles denote the lower p-value. An increase in the color transparency (lighter color) of the squares and circles indicates an increase in the percentage of the included genes with expression that counter the regulation direction of the pathway. C. The top significant KEGG pathways of TNc vs. HSc, the comparison between the chickens exposed to HS (HSc) and their thermoneutral control (TNc) at 6 day-post-treatment. D. The top significant Gene Ontology terms of TNc vs. HSc, the comparison between the chickens exposed to HS (HSc) and their thermoneutral control (TNc) at 6 day-post-treatment.
Fig 3
Fig 3
A. Heatmap of the top ~60 DEGs of TNc vs. TNi, as Log 2 relative hit counts of the comparison between the chickens infected with Eimeria maxima (TNi) and their uninfected thermoneutral control (TNc) at 6 day-post-treatment. B. The top KEGG pathways of TNc vs. TNi, based on the pathway term significance (α≤0.1) of the comparison between the chickens infected with Eimeria maxima (TNi) and their uninfected thermoneutral control (TNc) at 6 day-post-treatment. The green squares and arrowheads depict the downregulated pathways and genes, respectively. The red circles and arrowheads depict the upregulated pathways and genes, respectively. The bigger size squares and circles denote the lower p-value. An increase in the color transparency (lighter color) of the squares and circles indicates an increase in the percentage of the included genes with expression that counter the regulation direction of the pathway. C. The top significant KEGG pathways of TNc vs. TNi, the comparison between the chickens infected with Eimeria maxima (TNi) and their uninfected thermoneutral control (TNc) at 6 day-post-treatment. D. The top significant Gene Ontology terms of TNc vs. TNi, the comparison between the chickens infected with Eimeria maxima (TNi) and their uninfected thermoneutral control (TNc) at 6 day-post-treatment.
Fig 4
Fig 4
A. Heatmap of the top ~60 DEGs of HSc vs. HSi, as Log 2 relative hit counts of the comparison between the chickens infected with Eimeria maxima raised under HS (HSi) their uninfected HS control (HSc) at 6 day-post-treatment. B. The top KEGG pathways of HSc vs. HSi, based on the pathway term significance (α≤0.1) of the comparison between the chickens infected with Eimeria maxima raised under HS (HSi) and their uninfected HS control (HSc) at 6 day-post-treatment. The green squares and arrowheads depict the downregulated pathways and genes, respectively. The red circles and arrowheads depict the upregulated pathways and genes, respectively. The bigger size squares and circles denote the lower p-value. An increase in the color transparency (lighter color) of the squares and circles indicates an increase in the percentage of the included genes with expression that counter the regulation direction of the pathway. C. The top significant KEGG pathways of HSc vs. HSi, the comparison between the chickens infected with Eimeria maxima raised under HS (HSi) and their uninfected HS control (HSc) at 6 day-post-treatment. D. The top significant Gene Ontology terms of HSc vs. HSi, the comparison between the chickens infected with Eimeria maxima raised under HS (HSi) and their uninfected HS control (HSc) at 6 day-post-treatment.
Fig 5
Fig 5
A. Heatmap of the top ~60 DEGs of TNi vs. HSi, as Log 2 relative hit counts of the comparison between the chickens infected with Eimeria maxima raised either under HS (HSi) or thermoneutral condition (TNi) at 6-day-post-treatmen. B. The top KEGG pathways TNi vs. HSi, based on the pathway term significance (α≤0.05) of the comparison between the chickens infected with Eimeria maxima raised either under HS (HSi) or thermoneutral condition (TNi) at 6 day-post-treatment. The green squares and arrowheads depict the downregulated pathways and genes, respectively. The red circles and arrowheads depict the upregulated pathways and genes, respectively. The bigger size squares and circles denote the lower p-value. An increase in the color transparency (lighter color) of the squares and circles indicates an increase in the percentage of the included genes with expression that counter the regulation direction of the pathway. C. The top significant KEGG pathways of TNi vs. HSi, the comparison between the chickens infected with Eimeria maxima raised either under HS (HSi) or thermoneutral condition (TNi) at 6 day-post-treatment. D. The top significant Gene Ontology terms of TNi vs. HSi, the comparison between the chickens infected with Eimeria maxima raised either under HS (HSi) or thermoneutral condition (TNi) at 6 day-post-treatment.
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