影响猪采食行为的肠道微生物种类鉴别

doi:10.11843/j.issn.0366-6964.2023.01.020

Abstract

Abstract: Animals acquire energy and nutrients mainly by feed intake. Exploring the effect of gut microbiota on pig feeding behaviors and investigating its potential mechanism would provide theoretical basis for improving pig feeding behaviors through regulating gut microbiota. A total of 210 commercial Duroc pigs were used in this study. Phenotypes relating to feeding behaviors, including average daily eating time (ADET), average daily eating visits (ADEV) and average daily feed intake (ADFI) were recorded by automatic feeders. Stool samples were collected from the anus at the age of 140 days, and the structure and composition of gut microbiota were obtained by sequencing V3-V4 region of 16S rRNA gene. The Two-part model and co-abundance groups (CAGs) were used to identify the gut microbial taxa associated with feeding behaviors of pigs. The results showed as follows: 1) Correlation analysis between phenotypes showed that ADET was significantly and positively correlated with ADEV (r=0.41, P<0.05) and RFI(r=0.32, P<0.05); ADFI was significantly and positively correlated with RFI (r=0.56, P<0.05) and average daily gain (ADG) (r=0.63, P<0.05). In addition, RFI was significantly positively correlated with backfat thickness (r=0.16, P<0.05). 2) In CAGs analysis, a significant negative correlation was found between CAG2 and ADFI (P<0.05). This CAG mainly included OTUs annotated to Ruminococcaceae, Bacteroidales and Oscillospira, etc. However, CAG9 containing OTUs annotated to Faecalibacterium prausnitzii, Eubacterium biforme and Asteroleplasma anaerobium was significantly and positively correlated with ADFI (P<0.05). 3) In the correlation analysis, there was no OTU that was identified to be significantly associated with feeding behaviors at FDR<0.05. However, 14, 21 and 25 OTUs were identified to showing a tendency of association with ADET, ADEV and ADFI, respectively (P<0.01). Among them, OTUs showing positive correlations with the ADFI were mainly annotated to Prevotella, Ruminococcaceae and Erysipelotrichaceae, etc, while those OTUs having negative correlation were annotated to YRC22, Burkholderiales, Lachnospiraceae and Ruminococcaceae. 4) The functional prediction analysis of the gut microbiota showed that there was a significantly positive correlation between ADFI and biological funtions including Insulin signaling pathway and Lipid metabolism. Whereas the Sphingolipid metabolism was significantly and negatively correlated with ADFI (P<0.05). The results of this study suggest that some bacteria which can produce short-chain fatty acids or lactic acid, such as Burkholderiales, Ruminococcaceae, Christensenellaceae, Lachnospiraceae, etc., may play an important role in inhibiting feed intake, while Prevotella, especially Prevotella copri has the potential effect enhancing host appetite, are the key microorganisms that regulating the host feeding behaviour.

Key words: pig, feeding behavior, 16S rRNA, gut microbiota, feces, co-abundance groups

CLC Number:

S828.4

JIANG Hui, YANG Hui, FANG Shaoming, GAO Jun, CHEN Congying. Identification of Gut Microbial Taxa Associated with Feeding Behaviors in Pigs[J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(1): 213-226.

References 57

[1]	杨国明.猪采食行为研究进展[J].猪业科学,2006,23(3):14-16.YANG G M.Research progress in feeding behavior of pigs[J].Swine Industry Science,2006,23(3):14-16.(in Chinese)
[2]	FETISSOV S O.Role of the gut microbiota in host appetite control:Bacterial growth to animal feeding behaviour[J].Nat Rev Endocrinol,2017,13(1):11-25.
[3]	KEEN-RHINEHART E,ONDEK K,SCHNEIDER J E.Neuroendocrine regulation of appetitive ingestive behavior[J].Front Neurosci,2013,7:213.
[4]	张亚南,余凯凡,朱伟云.肠道微生物调控宿主食欲的研究进展[J].微生物学报,2017,57(7):951-960.ZHANG Y N,YU K F,ZHU W Y.Role of gut microbiota in host appetite control[J].Acta Microbiologica Sinica,2017,57(7):951-960.(in Chinese)
[5]	VAN DE WOUW M,SCHELLEKENS H,DINAN T G,et al.Microbiota-gut-brain axis:Modulator of host metabolism and appetite[J].J Nutr,2017,147(5):727-745.
[6]	LI Y Q,XI Y M,WANG Z D,et al.Combined signature of rumen microbiome and metabolome in dairy cows with different feed intake levels[J].J Anim Sci,2020,98(3):skaa070.
[7]	FORSYTHE P,BIENENSTOCK J,KUNZE W A.Vagal pathways for microbiome-brain-gut axis communication[M]//LYTE M,CRYAN J F.Microbial Endocrinology:The Microbiota-Gut-Brain Axis in Health and Disease.New York:Springer,2014:115-133.
[8]	SHARON G,GARG N,DEBELIUS J,et al.Specialized metabolites from the microbiome in health and disease[J].Cell Metab,2014,20(5):719-730.
[9]	DESBONNET L,GARRETT L,CLARKE G,et al.The probiotic Bifidobacteria infantis:an assessment of potential antidepressant properties in the rat[J].J Psychiatr Res,2008,43(2):164-174.
[10]	TILIGADA E,WILSON J F.Regulation of α-melanocyte-stimulating hormone release from superfused slices of rat hypothalamus by serotonin and the interaction of serotonin with the dopaminergic system inhibiting peptide release[J].Brain Res,1989,503(2):225-228.
[11]	BRETON J,TENNOUNE N,LUCAS N,et al.Gut commensal E. coli proteins activate host satiety pathways following nutrient-induced bacterial growth[J].Cell Metab,2016,23(2):324-334.
[12]	YANG H,YANG M,FANG S M,et al.Evaluating the profound effect of gut microbiome on host appetite in pigs[J].BMC Microbiol,2018,18(1):215.
[13]	KAOUTARI A E,ARMOUGOM F,GORDON J I,et al.The abundance and variety of carbohydrate-active enzymes in the human gut microbiota[J].Nat Rev Microbiol,2013,11(7):497-504.
[14]	PSICHAS A,SLEETH M L,MURPHY K G,et al.The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents[J].Int J Obes (Lond),2015,39(3):424-429.
[15]	LEE J H,LEE J.Indole as an intercellular signal in microbial communities[J].FEMS Microbiol Rev,2010,34(4):426-444.
[16]	CHIMEREL C,EMERY E,SUMMERS D K,et al.Bacterial metabolite indole modulates incretin secretion from intestinal enteroendocrine L cells[J].Cell Rep,2014,9(4):1202-1208.
[17]	JIANG H,FANG S M,YANG H,et al.Identification of the relationship between the gut microbiome and feed efficiency in a commercial pig cohort[J].J Anim Sci,2021,99(3):skab045.
[18]	MCORIST A L,JACKSON M,BIRD A R.A comparison of five methods for extraction of bacterial DNA from human faecal samples[J].J Microbiol Methods,2002,50(2):131-139.
[19]	田威龙,司景磊,刘笑笑,等.高脂高糖饮食对小型猪肠道微生物的影响[J].畜牧兽医学报,2022,53(4):1143-1153.TIAN W L,SI J L,LIU X X,et al.Effects of high-fat and high-sugar diet on intestinal microbiota in mini-pigs[J].Acta Veterinaria et Zootechnica Sinica,2022,53(4):1143-1153.(in Chinese)
[20]	谭占坤,商振达,刘锁珠,等.西藏高原藏猪盲肠微生物群落结构与多样性的研究[J].畜牧兽医学报,2020,51(9):2147-2155.TAN Z K,SHANG Z D,LIU S Z,et al.Study on the cecal microbial community structure and diversity of Tibetan pigs in Tibetan Plateau[J].Acta Veterinaria et Zootechnica Sinica,2020,51(9):2147-2155.(in Chinese)
[21]	BOLGER A M,LOHSE M,USADEL B.Trimmomatic:A flexible trimmer for Illumina sequence data[J].Bioinformatics,2014,30(15):2114-2120.
[22]	MAGOČ T,SALZBERG S L.FLASH:fast length adjustment of short reads to improve genome assemblies[J].Bioinformatics,2011,27(21):2957-2963.
[23]	EDGAR R C.Search and clustering orders of magnitude faster than BLAST[J].Bioinformatics,2010,26(19):2460-2461.
[24]	ROGNES T,FLOURI T,NICHOLS B,et al.VSEARCH:A versatile open source tool for metagenomics[J].PeerJ,2016,4:e2584.
[25]	WANG Q,GARRITY G M,TIEDJE J M,et al.Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy[J].Appl Environ Microbiol,2007,73(16):5261-5267.
[26]	VENKATARAMAN A,BASSIS C M,BECK J M,et al.Application of a neutral community model to assess structuring of the human lung microbiome[J].mBio,2015,6(1):e02284-14.
[27]	LANGILLE M G I,ZANEVELD J,CAPORASO J G,et al.Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences[J].Nat Biotechnol,2013,31(9):814-821.
[28]	FRIEDMAN J,ALM E J.Inferring correlation networks from genomic survey data[J].PLoS Comput Biol,2012,8(9):e1002687.
[29]	MURTAGH F,LEGENDRE P.Ward's hierarchical agglomerative clustering method:which algorithms implement Ward's criterion?[J].J Classif,2014,31(3):274-295.
[30]	ZHANG Q P,WU Y Q,WANG J,et al.Accelerated dysbiosis of gut microbiota during aggravation of DSS-induced colitis by a butyrate-producing bacterium[J].Sci Rep,2016,6:27572.
[31]	SHANNON P,MARKIEL A,OZIER O,et al.Cytoscape:A software environment for integrated models of biomolecular interaction networks[J].Genome Res,2003,13(11):2498-2504.
[32]	REVELLE W.Psych:Procedures for psychological,psychometric,and personality research[R].Package version 1.8.12, 2018.
[33]	FU J Y,BONDER M J,CENIT M C,et al.The gut microbiome contributes to a substantial proportion of the variation in blood lipids[J].Circ Res,2015,117(9):817-824.
[34]	KOLDE R.Pheatmap:Pretty heatmaps[R].Package version 1.0.12, 2015.
[35]	ZHOU H,YU B,HE J,et al.The optimal combination of dietary starch,non-starch polysaccharides,and mannan-oligosaccharide increases the growth performance and improves butyrate-producing bacteria of weaned pigs[J].Animals (Basel),2020,10(10):1745.
[36]	郭晓红,郭玉龙,刘亚丹,等.仔猪不同发育阶段结肠微生物菌群特征分析[J].畜牧兽医学报,2019,50(9):1759-1774.GUO X H,GUO Y L,LIU Y D,et al.Characteristics of intestinal microflora of colon at different developmental stages in piglets[J].Acta Veterinaria et Zootechnica Sinica,2019,50(9):1759-1774.(in Chinese)
[37]	SPRING S,PREMATHILAKE H,BRADWAY C,et al.Effect of very low-protein diets supplemented with branched-chain amino acids on energy balance,plasma metabolomics and fecal microbiome of pigs[J].Sci Rep,2020,10(1):15859.
[38]	YANG H,XIAO Y P,WANG J J,et al.Core gut microbiota in Jinhua pigs and its correlation with strain,farm and weaning age[J].J Microbiol,2018,56(5):346-355.
[39]	LI Y,XU F L,TONG X,et al.Effects of Macleaya cordata extract on small intestinal morphology and gastrointestinal microbiota diversity of weaned pigs[J].Livest Sci,2020,237:104040.
[40]	THONGBUNROD N,CHAIPRASERT P.Efficacy and metagenomic analysis of the stabilized anaerobic lignocellulolytic microbial consortium from Bubalus bubalis rumen with rice straw enrichment for methane production[J].BioEnerg Res,2021,14(3):870-890.
[41]	BANIEL A,AMATO K R,BEEHNER J C,et al.Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas[J].Microbiome,2021,9(1):26.
[42]	张德明,黄嘉訸,李劲树,等.猪肠道微生物及其代谢产物与肠道屏障研究进展[J].畜牧兽医学报,2022,53(5):1334-1344.ZHANG D M,HUANG J H,LI J S,et al.Research progress of gut microbiota,metabolites and gut barrier in pigs[J].Acta Veterinaria et Zootechnica Sinica,2022,53(5):1334-1344.(in Chinese)
[43]	LIANG J,KOU S S,CHEN C,et al.Effects of Clostridium butyricum on growth performance,metabonomics and intestinal microbial differences of weaned piglets[J].BMC Microbiol,2021,21(1):85.
[44]	LEE G H,RHEE M S,CHANG D H,et al.Oscillibacter ruminantium sp.nov.,isolated from the rumen of Korean native cattle[J].Int J Syst Evol Microbiol,2013,63(Pt 6):1942-1946.
[45]	MYER P R,FREETLY H C,WELLS J E,et al.Analysis of the gut bacterial communities in beef cattle and their association with feed intake,growth,and efficiency[J].J Anim Sci,2017,95(7):3215-3224.
[46]	TRUAX A D,CHEN L,TAM J W,et al.The inhibitory innate immune sensor NLRP12 maintains a threshold against obesity by regulating gut microbiota homeostasis[J].Cell Host Microbe,2018,24(3):364-378.e6.
[47]	WANG Y Y,LIU F,URBAN J F,et al.Ascaris suum infection was associated with a worm-independent reduction in microbial diversity and altered metabolic potential in the porcine gut microbiome[J].Int J Parasitol,2019,49(3-4):247-256.
[48]	OGATA T,MAKINO H,ISHIZUKA N,et al.Long-term high-grain diet altered the ruminal pH,fermentation,and composition and functions of the rumen bacterial community,leading to enhanced lactic acid production in Japanese black beef cattle during fattening[J].PLoS One,2019,14(11):e0225448.
[49]	SONG J J,TIAN W J,KWOK L Y,et al.Effects of microencapsulated Lactobacillus plantarum LIP-1 on the gut microbiota of hyperlipidaemic rats[J].Br J Nutr,2017,118(7):481-492.
[50]	SILBERBAUER C J,SURINA-BAUMGARTNER D M,ARNOLD M,et al.Prandial lactate infusion inhibits spontaneous feeding in rats[J].Am J Physiol Regul Integr Comp Physiol,2000,278(3):R646-R653.
[51]	MYER P R,WELLS J E,SMITH T P L,et al.Microbial community profiles of the colon from steers differing in feed efficiency[J].Springerplus,2015,4:454.
[52]	QUEIPO-ORTUÑO M I,SEOANE L M,MURRI M,et al.Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels[J].PLoS One,2013,8(5):e65465.
[53]	MOROTOMI M,NAGAI F,WATANABE Y.Description of Christensenella minuta gen.nov.,sp.nov.,isolated from human faeces,which forms a distinct branch in the order Clostridiales,and proposal of Christensenellaceae fam.nov[J].Int J Syst Evol Microbiol,2012,62(1):144-149.
[54]	GOODRICH J K,WATERS J L,POOLE A C,et al.Human genetics shape the gut microbiome[J].Cell,2014,159(4):789-799.
[55]	RODIN J.Insulin levels,hunger,and food intake:an example of feedback loops in body weight regulation[J].Health Psychol,1985,4(1):1-24.
[56]	HOUSEKNECHT K L,SPURLOCK M E.Leptin regulation of lipid homeostasis:dietary and metabolic implications[J].Nutr Res Rev,2003,16(1):83-96.
[57]	WALLS S M Jr,ATTLE S J,BRULTE G B,et al.Identification of sphingolipid metabolites that induce obesity via misregulation of appetite,caloric intake and fat storage in Drosophila[J].PLoS Genet,2013,9(12):e1003970.

Identification of Gut Microbial Taxa Associated with Feeding Behaviors in Pigs

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