Cecal microbiota composition differs under normal and high ambient temperatures in genetically distinct chicken lines

Authors: CAMPOS, PHILIP - Orise Fellow; Schreier, Lori; Proszkowiec-Weglarz, Monika; DRIDI, SAMI - University Of Arkansas

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/20/2023
Publication Date: 9/25/2023
Citation: Campos, P.M., Schreier, L.L., Proszkowiec-Wegla, M.K., Dridi, S. 2023. Cecal microbiota composition differs under normal and high ambient temperatures in genetically distinct chicken lines. Scientific Reports. 13:16037. https://doi.org/10.1038/s41598-023-43123-9.
DOI: https://doi.org/10.1038/s41598-023-43123-9

Interpretive Summary: Chickens have been bred over multiple decades for traits such as faster growth and higher breast yield. Changes in genetics come with trade-offs, where positive changes in these traits may have led to negative changes in other traits in modern broiler chickens, such as immunity and gut integrity. As a result, modern broilers are more susceptible to environmental challenges such as heat stress, where increases to the chickens’ core body temperature can negatively affect broiler health and growth rates by harming gut integrity. Heat stress has also been shown to alter the gut microbiota, or the community of bacterial species residing in the gut. The gut microbiota plays a role in broiler health by affecting how nutrients are absorbed and how the immune system responds, therefore we have studied how heat stress may affect the microbiota. Taking in consideration the potential effects from both genetic differences and heat stress, this study investigated the effects of heat stress on the microbiota of chickens from four different genetic lines. Two older, slower-growing lines (Jungle Fowl and Athens Canadian Random Bred) and two more modern, faster-growing lines (1995 Random Bred and 2015 Modern Random Bred) were obtained for this experiment. The microbiota of the cecum was chosen for analysis because of the large numbers and diverse types of bacteria residing in this region. Populations of bacteria that were attached to the gut or were present in the gut contents were analyzed separately. The bacterial sequences analyzed showed that the bacteria present in the gut contents were the most greatly affected by heat stress. The changes in bacterial diversity (number of unique bacteria) differed in the two slower-growing lines compared to the faster-growing lines. The slower-growing lines had a lower starting point of unique bacteria and heat stress resulted in an increase of unique bacteria, while the faster-growing lines had a higher starting point of unique bacteria and heat stress resulted in a decrease of unique bacteria. Percentages of certain bacterial groups also changed in a similar pattern, with increases in percentages common in the slower-growing lines and decreases in percentages common in the faster-growing lines. An analysis was made to predict how the functions of the microbiota were altered by heat stress. The modern 2015 line was predicted to have the most changes in function because of heat stress, supporting that modern lines may be more susceptible to heat stress. Continued research could be important in developing methods to limit negative effects to the microbiota under heat stress and improve the health of modern broiler chickens.

Technical Abstract: Decades of selection for broiler chickens with traits for rapid growth and high metabolic rate have made modern broilers susceptible to environmental stressors such as heat stress (HS). HS has negative effects on poultry performance and gastrointestinal tract (GIT) integrity, and stresses can disrupt intestinal microbiota, which play a role in broiler health by affecting factors such as nutrient exchange and immune system modulation. The aim of this study was to compare bacterial communities in the cecal luminal (CeL) and cecal mucosal (CeM) microbiota between HS and thermoneutral (TN) birds in four broiler lines. Day-old broiler chicks from the Giant Jungle Fowl (JF), Athens Canadian Random Bred (ACRB), 1995 Random Bred (L1995), and Modern Random Bred (L2015) lines were raised under TN conditions until day (d) 28. On d 29, birds were subjected to TN (24 °C) or chronic cyclic HS (8 h/d, 36 °C) condition until d 56. On d 56, two birds per replicate were euthanized to collect cecal luminal content and mucosal scrapings for bacterial DNA isolation. 16S rRNA amplicon sequencing was performed to characterize the microbiota and determine differences in alpha and beta diversity between HS and TN birds for each broiler line. HS primarily affected CeL microbiota, and alpha diversity was affected depending on broiler line, where richness decreased in the older JF and ACRB lines, while increasing in the newer L1995 and L2015 lines. Beta diversity analysis (unweighted UniFrac, PERMANOVA) revealed significant differences between HS and TN conditions in in CeL microbiota of all four lines and in CeM microbiota of L2015. HS resulted in increasing relative abundance of 23 genera and 15 genera in the CeL microbiota of the JF and ACRB lines, respectively, and resulted in decreasing relative abundance of 8 genera and 24 genera in L1995 and L2015, respectively, again demonstrating different patterns depending on line. In comparisons of predicted functional abundance using the MetaCyc database, L2015 and JF showed differential abundance in various predicted pathways in both CeL and CeM microbiota, indicating potential differences in function of CeL and CeM microbiota in a modern line compared to an ancestral line. HS had the most prominent effects on pathways in L2015 in both the CeL and CeM microbiota, suggesting that there may be a greater impact of HS on function in L2015 compared to other lines. Continued research on GIT microbiota and the function of its members is of importance to alleviate the negative effects of HS on modern broiler chickens’ performance and health.