Low rumen degradable starch reduces diarrhea and colonic inflammation by influencing the whole gastrointestinal microbiota and metabolite flow in dairy goats

doi:10.1016/j.jia.2024.04.015

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Chunjia Jin^{1, 2}, Ziqi Liang^{1, 2}, Xiaodong Su^{1, 2}, Peiyue Wang^{1, 2}, Xiaodong Chen^{1, 2}, Yue Wang^{1, 2}, Xinjian Lei^{1, 2}, Junhu Yao^{1, 2#}, Shengru Wu¹^,²^#

1 College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China

2 Key Laboratory of Livestock Biology, Northwest A&F University, Yangling 712100, China

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摘要淀粉是反刍动物重要的能量来源，反刍动物采食高淀粉日粮提高了瘤胃可降解淀粉（RDS）水平，导致瘤胃酸中毒和后肠炎症。目前高淀粉日粮引起反刍动物后肠功能障碍的机制尚不明确，有关后肠道微生物如何调控后肠道健康的研究较为深入，但仍缺乏基于消化道层面的整体性考虑。本研究整合了瘤胃、空肠、回肠和结肠微生物、代谢物和宿主转录组数据，探究基于消化道微生物和代谢物流转的前肠对后肠基因表达的影响。试验选取40只体重相近、健康的3月龄青年奶山羊，随机均分两组，分别饲喂低RDS日粮（LRDS，整粒玉米，RDS=13.85%，n=20）和高RDS日粮（HRDS，粉碎玉米，RDS=20.74%，n=20）日粮，饲喂90 d后发现与HRDS组相比，LRDS组腹泻率明显降低。根据粪便评分每组挑选6只羊进行屠宰取样，发现LRDS可显著降低腹泻率和结肠病理评分。转录组学结果显示，LRDS降低了空肠、回肠和结肠的炎症相关基因的表达。16S rRNA测序结果显示，LRDS组小肠和后肠有益共生菌的相对丰度增加，致病菌的相对丰度降低。根据生态位宽度计算微生物在消化道内的流转分布，确定了8个核心菌属。代谢组学结果显示，在不同的消化道部位共鉴定出554种代谢物。将代谢物分为3个模块：在当前消化道位点丰度增加的代谢物（ICS），无差异流入当前消化道位点的代谢物（UICS），在当前消化道位点丰度减少的代谢物（DCS）。组学可解释性分析表明，UICS对空肠、回肠和结肠基因表达的组学可解释性超过10%。结肠UICS中，1-棕榈酰甘油和脱氧胆酸分别对结肠免疫相关差异基因的组学可解释性为60.74%和11.5%，表明消化道UICS，尤其是1-棕榈酰甘油和脱氧胆酸，可能会影响结肠免疫相关基因的差异表达。本研究初步探究了奶山羊消化道宿主-微生物互作效应的模式，即消化道微生物及其代谢物流转对消化道基因表达存在影响，前肠可通过代谢物的流转影响后肠基因表达。

Abstract Postruminal intestinal inflammation and hindgut acidosis caused by increased dietary starch supply and thereby increased quantities of ruminal degradable starch (RDS) in ruminants have been widely studied. Although the roles of the microbiota in mediating hindgut health that are focused on the hindgut have been widely studied, the absence of whole gastrointestinal insight may influence the depth of research. We integrated the microbiome, metabolome, and host transcriptome changes in the rumen, jejunum, ileum, and colon to investigate the contributions of foregut changes to hindgut gene expression driven by gastrointestinal microbiota and metabolite flow. Forty goats were randomly assigned to receive either a low rumen degradable starch diet (LRDS, RDS=13.85%, n=20) or a high rumen degradable starch diet (HRDS, RDS=20.74%, n=20). Compared with the high RDS (HRDS) group, the low RDS (LRDS) group significantly decreased the diarrheal rate. Based on the mean values of the fecal scores, 6 represented goats of LRDS group (fecal scores=4.58±0.120) and 6 represented goats of HRDS group (fecal scores=3.53±0.343) were selected for sampling and subsequent analysis. LRDS had significantly decreased the colonic pathologic scores. Transcriptomic analysis revealed that LRDS reduced jejunal, ileal, and colonic inflammatory responses. An increase in beneficial commensals and a decreased abundance of pathogenic genera in the small intestine and hindgut were found in goats fed the LRDS diet using 16S rRNA gene sequencing. To identify microbial transmission as well as the transmission of microbial metabolites, 8 genera were identified as core genera according to their calculated niche width. Metabolomics analysis revealed that a total of 554 metabolites were identified among different gastrointestinal sites. Then, metabolites were incorporated into 3 modules: metabolites increased in the current site (ICS), unchanged inflow metabolites in the current site (UICS), and metabolites decreased in the current site (DCS). The results indicated that the UICS metabolites contributed more than 10% to host gene expression in the jejunum, ileum, and colon. When we further focused on the effects of colonic UICS metabolites on the colonic immune-related differentially expressed genes, the results indicated that 1-palmitoylglycerol and deoxycholic acid contributed 60.74% and 11.5% to the colonic immune-related differentially expressed genes, respectively. Our findings provide a preliminary framework of microbial effects that includes the microbiota and their metabolite changes, especially reduced 1-palmitoylglycerol and deoxycholic acid, in the former gastrointestinal tract that could be involved in the alleviation of colonic inflammation in goats fed LRDS diets.

Keywords: ruminal degradable starch matter flow microbiome, metabolome colonic inflammation

Online: 10 May 2024

Fund: The authors acknowledge all members of the Innovative Research Team of Animal Nutrition & Healthy Feeding of Northwest A&F University for providing assistance. This research was financially supported by the National Natural Science Foundation of China (32072761, 31902184, 32102570) and the Shaanxi Provincial Science and Technology Association Young Talents Lifting Program Project (20220203).

About author: #Correspondence Junhu Yao, E-mail: yaojunhu2004@sohu.com; Shengru Wu, E-mail: wushengru2013@163.com

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Chunjia Jin, Ziqi Liang, Xiaodong Su, Peiyue Wang, Xiaodong Chen, Yue Wang, Xinjian Lei, Junhu Yao, Shengru Wu. 2024. Low rumen degradable starch reduces diarrhea and colonic inflammation by influencing the whole gastrointestinal microbiota and metabolite flow in dairy goats. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.04.015

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