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Effect of Baicalin-Aluminum Complexes on Fecal Microbiome In International Journal of Molecular Sciences Article Effect of Baicalin-Aluminum Complexes on Fecal Microbiome in Piglets 1,2, 1,2, 1,2 1,2, 1,2 1,2 Shulin Fu y, Feng Zhuang y, Ling Guo , Yinsheng Qiu *, Jianglin Xiong , Chun Ye , Yu Liu 1,2, Zhongyuan Wu 1,2, Yongqing Hou 1,2 and Chien-An Andy Hu 1,3 1 Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University, Wuhan 430023, China; [email protected] (S.F.); [email protected] (F.Z.); [email protected] (L.G.); [email protected] (J.X.); [email protected] (C.Y.); [email protected] (Y.L.); [email protected] (Z.W.); [email protected] (Y.H.); [email protected] (C.-A.A.H.) 2 Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Wuhan 430023, China 3 Biochemistry and Molecular Biology, University of New Mexico School of Medicine, Albuquerque, NM 87131, USA * Correspondence: [email protected] These authors contributed equally to the work. y Received: 22 April 2019; Accepted: 13 May 2019; Published: 14 May 2019 Abstract: The gut microbiome has important effects on gastrointestinal diseases. Diarrhea attenuation functions of baicalin (BA) is not clear. Baicalin–aluminum complexes (BBA) were synthesized from BA, but the BBA’s efficacy on the diarrhea of piglets and the gut microbiomes have not been explored and the mechanism remains unclear. This study has explored whether BBA could modulate the composition of the gut microbiomes of piglets during diarrhea. The results showed that the diarrhea rate reduced significantly after treatment with BBA. BBA altered the overall structure of the gut microbiomes. In addition, the Gene Ontology (GO) enrichment analysis indicated that the functional differentially expressed genes, which were involved in the top 30 GO enrichments, were associated with hydrogenase (acceptor) activity, nicotinamide-nucleotide adenylyltransferase activity, and isocitrate lyase activity, belong to the molecular function. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis showed that flagellar assembly, bacterial chemotaxis, lipopolysaccharide biosynthesis, ATP-binding cassette transporters (ABC) transporters, biosynthesis of amino acids, and phosphotransferase system (PTS) were the most enriched during BBA treatment process. Taken together, our results first demonstrated that BBA treatment could modulate the gut microbiomes composition of piglets with diarrhea, which may provide new potential insights on the mechanisms of gut microbiomes associated underlying the antimicrobial efficacy of BBA. Keywords: baicalin–aluminum complexes; gut microbiomes; diarrhea 1. Introduction Post-weaning diarrhea (PWD) is thought to be one of the most important diseases for the modern pig industry worldwide because it causes serious financial losses [1]. There are many factors related to diarrhea of piglets. Enterotoxigenic Escherichia coli (E. coli) (ETEC) is generally considered to be an important factor associated with PWD of piglets [2]. In addition, previous reports showed that stress factors during weaning period might negatively regulate the response to immune system which could result in alteration of intestinal flora and dysfunction [3,4]. Antibiotics are commonly utilized for controlling PWD of piglets [5]. However, there is a concern that long-term utilization of antibiotics may lead to drug resistance [6] and risk of residue in the human body through food transmission [7]. Therefore, currently developing a new Chinese herbal medicine has become an important approach to solve the diarrhea in piglets. Int. J. Mol. Sci. 2019, 20, 2390; doi:10.3390/ijms20102390 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, 2390 2 of 15 Baicalin–aluminum complexes (BBA) are synthesized from baicalin. Baicalin is an important effective plant-derived compound of the traditional Chinese medicine, which is extracted from Scutellaria baicalensis Georgi (Huang Qin) [8]. Baicalin has been shown exhibiting important biological functions. Baicalin could provide protection against Salmonella typhimurium infection, reduce the bacterial virulence, and modulate host response [9]. Baicalin significantly attenuated the production of HMGB1 in peripheral blood monocytes induced by Haemophilus parasuis during inflammation process [10]. Baicalin triggered the activation of autophagy in the macrophages stimulated by Mycobacterium tuberculosis infection via PI3K/Akt/mTOR pathway, thus producing anti-inflammatory function [11]. It has been documented that baicalin could inhibit the lethality of Shiga-like toxin 2 [12] and provide significant protection to mice from the challenge of Shiga-like toxin-producing Escherichia coli (STEC) O157:H7 [13]. In addition, baicalin has shown an effect on inhibiting growth and reducing antimicrobial resistance of Escherichia coli [14]. Alum contains aluminum sulfate and has been shown to possess good antibacterial activity [15]. It has been documented that a commercial product, Huangqinsulv capsule, of which the main active ingredient is baicalin-aluminium complex, was synthesized by using alum and the extracts of Scutellaria baicalensis Georgi [16]. Huangqinsulv capsule was utilized clinically to treat human diarrhea for more than 30 years. However, whether BBA could inhibit bacterial virulence-related factors and modulate the composition of the gut microbiome of piglets during diarrhea has not been deeply studied. Previous research has reported that dynamic gut microbiomes have key effects on maintaining balance and host’s health, may be through crosstalk between host immunity and microorganism [17,18]. If the dynamic balance of the interaction between host and microbe is broken, intestinal inflammation diseases such as PWD of piglets might occur [19]. It has been recorded that a disorder of gastrointestinal flora balance could cause inflammatory bowel disease [20]. Therefore, regulation of the gut microbiomes may serve as a target to control some diseases, such as nonalcoholic fatty liver disease (NAFLD) [21]. Metagenomic analysis provides a favorable platform for understanding changes of gut flora during disease processes. The technology could exactly reveal more active microbial communities [22]. In this study, thirty piglets with PWD were chosen to explore the efficacy of BBA on the treatment of diarrhea and the structural changes of the gut microbiomes in response to the treatment with BBA. The results demonstrated that the rate of diarrhea among piglets reduced significantly after treatment with BBA, and BBA could modulate the composition of gut microbiomes of piglets by metagenomic analysis, which may provide new potential insights on the mechanisms of gut microbiomes associated underlying the anti-microbiological efficacy of BBA. 2. Results 2.1. BBA Significantly Reduced the Diarrhea Rates of Piglets During clinical observation, on the day with the piglets administrated with BBA, the diarrhea rates of the piglets significantly reduced compared with the untreated group (Figure1)( p < 0.05). Furthermore, on the third day, no clinical symptoms of piglets with BBA treatment were observed, but the untreated group still displayed diarrhea (Figure1). Int. J. J. Mol. Mol. Sci. Sci. 20182019,, 1920,, x 2390 FOR PEER REVIEW 33 of of 1514 Figure 1. Baicalin–aluminum complexes (BBA) significantly inhibited the diarrhea rates of piglets. * indicatesFigure 1. significanceBaicalin–aluminum at p < 0.05. complexes (BBA) significantly inhibited the diarrhea rates of piglets. * indicates significance at p < 0.05. 2.2. Overall Structural Modulation of Gut Microbiome Following Treatment with BBA 2.2. OverallIn this Structural study, the Modulation metagenomic of Gut sequencing Microbiome analysis Following was Treatment used to detect with BBA the structural changes in the gutIn microbiomesthis study, the in metagenomic the two groups sequencing before and analysis after treatment was used with to detect BBA or the not. structural The results changes showed in thatthe gut high-throughput microbiomes metagenomicin the two groups sequencing before produced and after 562,699,940 treatment clean with reads BBA fromor not. 6 stool The samples results withshowed 93,783,323 that high-throughput11,256,477 sequences metagenomic per sample sequen (Tablecing1 ,produced Supplemental 562,699,940 Table S1). clean reads from 6 ± stool samples with 93,783,323 ± 11,256,477 sequences per sample (Table 1, Supplemental Table S1). Table 1. Statistical summary analysis of gut microbiome. Table 1. Statistical summary analysis of gut microbiome. Samples Raw Reads Clean Reads Clean Ratio (%) Mapped Ratio (%) TreatedSamples with BAA 89,537,684Raw Reads5,405,796.2 87,247,590.3Clean Reads5,144,406.2 Clean 94.9 Ratio0.2 (%) Mapped 99.1 Ratio0.1 (%) ± ± ± ± TreatedUntreated with BAA 103,588,655.389,537,684 ± 5,405,796.213,288,842.4 100,319,056.387,247,590.3 ± 12,734,141.25,144,406.2 92.694.9 ± 0.2 99.1 99.0 ± 0.10.1 Untreated 103,588,655.3 ±± 13,288,842.4 100,319,056.3 ±± 12,734,141.2 92.6 ± 0.2 99.0 ±± 0.1 Unweighted UniFracUniFrac PCoA PCoA was was utilized utilized to detect to detect the composition the composition of microbiomes of microbiomes from diff erentfrom groupsdifferent in groups view of in the view evolutionary of the evolutionary distance [23]. distance PCoA analysis [23]. PCoA showed analysis that BBA showed treatment that group BBA andtreatment control group group and displayed control changes, group anddisplayed a distinct change clusters, ofand the a piglets’distinct gut cluster microbiome of the compositionpiglets’ gut frommicrobiome
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