Exposure to heat-stress environment affects the physiology, circulation levels of cytokines, and microbiome in dairy cows

Abstract

The microbiome has emerged as a new player on behavior, physiology and stress because of its significant effects on the brain-gut axis. The aim of this study was to increase our understanding of brain-gut function in dairy cows. We investigated the effects of a heat-stress (HS) environment and individual differences of heat sensitivity (IH) on bovine physiological characteristics and microbial composition. Results indicate that both HS and IH increased rectal temperature (RT) (P < 0.05). An HS environment increased plasma, as well as milk cortisol and cytokines in plasma; however, it decreased plasma, and milk oxytocin, triiodothyronine, and thyroxine (P < 0.05) levels. Exposure to an HS environment reduced the diversity of the fecal microbial population, and resulted in a higher expression of diseases, the environmental adaptation pathway, and the immune related pathway, whereas it lowered the expression of metabolic pathways (P < 0.05). High heat sensitive cows have upregulated metabolisms, environmental adaptation and cellular process pathways, and a downregulated neurodegenerative disease pathway (P < 0.05). Thus, we conclude that exposure to an HS environment modulates physiological characteristics, which may interplay with microbial activity, and in turn, alter the circulation levels of cytokines, implicating the role of the brain-gut axis in dairy cows. The HS environment affected physiological characteristics, cytokine levels, and microbial composition, but IH influenced RT and fecal microbial functions.

Figure 1

(A) Shows the temperature-humidity index (THI). (B) Shows rectal temperature of the four groups. Solid line represents the THI of 24 h data (144 values), and dotted line represents THI data based three hours (18 values) during 10:00 to 12:00 am. Data 2016/8/1 and 2016/9/21 represent the blood samplings days. HS means heat stress environment, IH means individual difference of heat sensitivity. *Means significant difference between High heat sensitivity cows under HS environment and low heat sensitivity cows under HS environment cows (P < 0.05). Values with different small letter (a,b) superscripts mean statistically different between HS and none/slight HS environment s (P < 0.05). n = 15 in each group.

Figure 2

Plasma cortisol (A), oxytocin (B), triiodothyronine (C) and thyroxine (D) concentration of cows in the four groups. HS means heat stress environment, IH means individual difference of heat sensitivity. Values with different small letters (a,b) mean statistically different (P < 0.05). n = 15 in each group.

Figure 3

Milk cortisol (A), oxytocin (B), triiodothyronine (C) and thyroxine (D) concentration of cows in the four groups. HS means heat stress environment IH means individual difference of heat sensitivity. Values with different small letters (a,b) mean statistically different (P < 0.05). n = 15 in each group.

Figure 4

Plasma circulation levels of interleukin-1ß (A), interleukin–6 (B), interferon-γ (C), and tumor necrosis factor-α (D) of cows in four groups. HS means heat stress environment, IH means individual difference of heat sensitivity. Values with different small letters (a,b) mean statistically different (P < 0.05). n = 15 in each group.

Figure 5

Feces microbial composition in the four groups. (A) Shows the heat map of the top 35 microbiome at genus level. (B) Shows the richness of feces microbial composition by observed species (richness of microbial composition: H-nHS > L-nHS, H-nHS > H-HS). (C) Shows the top 10 microbiome at phylum level. H-HS = high heat sensitivity cows under heat stress (HS) environment, L-HS = low heat sensitivity cows under HS environment (L-HS), H-nHS = high heat sensitivity cows under none/slight-HS environment, L-nHS = low heat sensitivity cows under non/slight-HS environment. n = 15 in each group.

Figure 6

Feces microbiome functions between comparisons. (A) H-HS vs H-nHS; (B) L-HS vs L-nHS; (C) H-HS vs L-HS; (D) H-nHS vs L-nHS. H-HS = high heat sensitivity cows under heat stress (HS) environment, L-HS = low heat sensitivity cows under HS environment (L-HS), H-nHS = high heat sensitivity cows under none/slight-HS environment, L-nHS = low heat sensitivity cows under non/slight-HS environment. n = 15 in each group.

Figure 7

The relationship of feces microbial composition to plasma cortisol (A) and oxytocin (B) by Shannon analysis; and relationship of feces microbial composition to plasma cortisol (C) and triiodothyonine (D) by Simpson analysis. n = 60. Red circles represent high heat sensitivity cows under heat stress (HS) environment (H-HS), black circles represent low heat sensitivity cows under HS environment (L-HS), gray circles represent high heat sensitivity cows under none/slight-HS environment (H-nHS), and blue circles represent low heat sensitivity cows under non/slight-HS environment (L-nHS).

Figure 8

The relationship of feces microbial composition to milk oxytocin (A) and plasma interleukin-1β (B) by Simpson analysis; and relationship of feces microbial composition to plasma tumor necrosis factor-α by Simpson (C) and Shannon (D) analysis. n = 60. Red circles represent high heat sensitivity cows under heat stress (HS) environment (H-HS), black circles represent low heat sensitivity cows under HS environment (L-HS), gray circles represent high heat sensitivity cows under none/slight-HS environment (H-nHS), and blue circles represent low heat sensitivity cows under non/slight-HS environment (L-nHS).