Heat stress impacts the multi-domain ruminal microbiota and some of the functional features independent of its effect on feed intake in lactating dairy cows

Park et al. Journal of Animal Science and Biotechnology https://doi.org/10.1186/s40104-022-00717-z (2022) 13:71 RESEARCH Open Access Heat stress impacts the multi-domain ruminal microbiota and some of the functional features independent of its effect on feed intake in lactating dairy cows Tansol Park1,2, Lu Ma3, Shengtao Gao3, Dengpan Bu3,4* and Zhongtang Yu1* Abstract Background: Heat stress (HS) affects the ruminal microbiota and decreases the lactation performance of dairy cows. Because HS decreases feed intake, the results of previous studies were confounded by the effect of HS on feed intake. This study examined the direct effect of HS on the ruminal microbiota using lactating Holstein cows that were pair-fed and housed in environmental chambers in a 2 × 2 crossover design. The cows were pair-fed the same amount of identical total mixed ration to eliminate the effect of feed or feed intake. The composition and structure of the microbiota of prokaryotes, fungi, and protozoa were analyzed using metataxonomics and compared between two thermal conditions: pair-fed thermoneutrality (PFTN, thermal humidity index: 65.5) and HS (87.2 for daytime and 81.8 for nighttime). Results: The HS conditions altered the structure of the prokaryotic microbiota and the protozoal microbiota, but not the fungal microbiota. Heat stress significantly increased the relative abundance of Bacteroidetes (primarily Gram-negative bacteria) while decreasing that of Firmicutes (primarily Gram-positive bacteria) and the Firmicutes-toBacteroidetes ratio. Some genera were exclusively found in the heat-stressed cows and thermal control cows. Some co-occurrence and mutual exclusion between some genera were also found exclusively for each thermal condition. Heat stress did not significantly affect the overall functional features predicted using the 16S rRNA gene sequences and ITS1 sequences, but some enzyme-coding genes altered their relative abundance in response to HS. * Correspondence: ; 3 State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, People’s Republic of China 1 Department of Animal Sciences, The Ohio State University, Columbus, OH, USA Full list of author information is available at the end of the article © The Author(s). 2022 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. 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Journal of Animal Science and Biotechnology (2022) 13:71 Page 2 of 15 Conclusions: Overall, HS affected the prokaryotes, fungi, and protozoa of the ruminal microbiota in lactating Holstein cows to a different extent, but the effect on the structure of ruminal microbiota and functional profiles was limited when not confounded by the effect on feed intake. However, some genera and co-occurrence were exclusively found in the rumen of heat-stressed cows. These effects should be attributed to the direct effect of heat stress on the host metabolism, physiology, and behavior. Some of the “heat-stress resistant” microbes may be useful as potential probiotics for cows under heat stress. Keywords: Functional profiles, Heat stress, Microbiome, Multi-kingdom, Network analysis, Ruminal microbiota Background Global warming as a result of the increased release of greenhouse gases (GHG) from different sources, including agriculture and livestock, is of great concern worldwide. Animal production, including dairy production, is impaired considerably by rising environmental temperature. The elevated ambient temperature accompanying global warming has been increasing the frequency and duration of heat stress (HS) episodes in dairy cows, especially in tropical, subtropical, and Mediterranean regions [1]. Dairy cows are more susceptible to HS than other farm animals, and they suffer from HS when the average temperature-humidity index (THI) exceeds 68 (approximately 22 °C at 50% relative humidity) [2]. Heat stress can have profound adverse effects on many aspects of dairy cows, including decreasing feed intake, feed efficiency, nutrient digestibility, milk production, milk quality; creating negative energy balance; and impairing reproductive performance among others [3–6]. Any of these adverse effects can lead to significant economic loss to the producers [7]. Moreover, HS also leads to poor animal welfare [8]. Heat stress in dairy cows is worsening as global warming continues, and HS is now well recognized as an environmental stressor that undermines the sustainable development of the dairy industry [9]. Therefore, HS in dairy cows has attracted tremendous research interest in the past decade. It has been shown that HS can directly impair the normal metabolism, physiology, and immune system in lactating dairy cows, including the metabolism of lipid in bovine primary adipocytes [10], the metabolism of carbohydrate and lipid, and milk protein synthesis in mammary tissues [11, 12], the metabolism of glucose and energy and energy balance [13], and immune system function [14]. Reduced voluntary feed intake is inherently associated with HS, and it aggravates these adverse effects indirectly [15–17]. The complex and diverse ruminal microbiota [18–20] plays a pivotal role in supplying the majority of the energy and nutrients required by dairy cows [21]. This microbiota is also dynamic responding to many internal and external factors [22–24], including HS [25, 26]. Heat stress can affect the ruminal microbiota because it reduces feed intake and impacts the metabolism, physiology, immune system, and behavior of the host. Using 16S rRNA or its gene-based analysis, the earliest studies showed that HS significantly affected the species richness and composition of the ruminal microbiota in dairy heifers with a BW ≥ 430 kg [27] and increased the genus Streptococcus and Clostridium coccoides–Eubacterium rectale group but decreased Fibrobacter in the rumen of dairy heifers [28]. In recent years, metataxonomics and metagenomics have been used to comprehensively exam (...truncated)