[en] The Jinhua pig is well known in China due to its delicious meat. However, because of large litter size, low birth weight always happens. This experiment used this breed as a model to research bacterial evidence leading to growth restriction and provide a possible solution linked to probiotics. In this experiment, the differences in organs indexes, colonic morphology, short chain fatty acid (SCFA) concentrations, microbiome, and transcriptome were detected between piglets in the standard-birth-weight group (SG) and low-birth-weight group (LG) to find potential evidence leading to low birth weight. We found that LG piglets had a lower liver index (p < 0.05), deeper colonic crypt depth (p < 0.05), fewer goblet cells (p < 0.05), and more inflammatory factor infiltration. In addition, differentially expressed genes (DEGs) were mainly enriched in B-cell immunity and glucose metabolism, and LG piglets had lower concentrations of SCFAs, especially butyrate and isobutyrate (p < 0.05). Finally, most of the significantly differentially abundant microbes were fewer in LG piglets, which affected DEG expressions and SCFA concentrations further resulting in worse energy metabolism and immunity. In conclusion, colonic disrupted microbiota may cause worse glucose metabolism, immunity, and SCFA production in LG piglets, and beneficial microbes colonized in SG piglets may benefit these harmful changes.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Li, Jiaheng ✱; Université de Liège - ULiège > TERRA Research Centre ; Institute of Animal Husbandry and Veterinary Medicine, Jinhua Academy of Agricultural Sciences, Jinhua 321011, China ; State Key Laboratory of Animal Nutrition and Feeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Wei, Zeou ✱; State Key Laboratory of Animal Nutrition and Feeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China ; School of Agriculture and Food Science, University College Dublin, Belfeld, D04 V1W8 Dublin, Ireland
Lou, Fangfang; Institute of Animal Husbandry and Veterinary Medicine, Jinhua Academy of Agricultural Sciences, Jinhua 321011, China
Zhang, Xiaojun; Institute of Animal Husbandry and Veterinary Medicine, Jinhua Academy of Agricultural Sciences, Jinhua 321011, China
Duan, Jiujun; State Key Laboratory of Animal Nutrition and Feeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Luo, Chengzeng; State Key Laboratory of Animal Nutrition and Feeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Hu, Xujin; Institute of Animal Husbandry and Veterinary Medicine, Jinhua Academy of Agricultural Sciences, Jinhua 321011, China
Tu, Pingguang; Institute of Animal Husbandry and Veterinary Medicine, Jinhua Academy of Agricultural Sciences, Jinhua 321011, China
Liu, Lei ; State Key Laboratory of Animal Nutrition and Feeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Zhong, Ruqing ✱; State Key Laboratory of Animal Nutrition and Feeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Chen, Liang; State Key Laboratory of Animal Nutrition and Feeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Du, Xizhong; Institute of Animal Husbandry and Veterinary Medicine, Jinhua Academy of Agricultural Sciences, Jinhua 321011, China
Zhang, Hongfu; State Key Laboratory of Animal Nutrition and Feeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
NSCF - National Natural Science Foundation of China
Funding text :
This work was supported by Jinhua Municipal Government-Academy Cooperation Project (ydhz2021ky08), National Natural Science Foundation of China (32102582), the Youth innovation of Chinese Academy of Agricultural Sciences (Y2023QC09), and the Agricultural Science and Technology Innovation Program (ASTIPIAS07, cxgc-ias-16).
Xu N.-Y. Zhang S.-Q. Peng S.-H. Investigation on the distribution and their effects on reproduction traits of three major genes in Jinhua pigs Yi Chuan Xue Bao = Acta Genet. Sin. 2003 30 1090 1096
Amdi C. Lynegaard J.C. Thymann T. Williams A.R. Intrauterine growth restriction in piglets alters blood cell counts and impairs cytokine responses in peripheral mononuclear cells 24 days post-partum Sci. Rep. 2020 10 4683 10.1038/s41598-020-61623-w 32170117
Niu Y. He J. Zhao Y. Shen M. Zhang L. Zhong X. Wang C. Wang T. Effect of curcumin on growth performance, inflammation, insulin level, and lipid metabolism in weaned piglets with IUGR Animals 2019 9 1098 10.3390/ani9121098 31818040
Vuguin P. Animal models for assessing the consequences of intrauterine growth restriction on subsequent glucose metabolism of the offspring: A review J. Matern.-Fetal Neonatal Med. 2002 11 254 257 10.1080/jmf.11.4.254.257 12375680
Akhtar M. Chen Y. Ma Z. Zhang X. Shi D. Khan J.A. Liu H. Gut microbiota-derived short chain fatty acids are potential mediators in gut inflammation Anim. Nutr. 2022 8 350 360 10.1016/j.aninu.2021.11.005
Wang J. Zhu P. Zheng X. Ma Z. Cui C. Wu C. Zeng X. Guan W. Chen F. Altered Liver Metabolism, Mitochondrial Function, Oxidative Status, and Inflammatory Response in Intrauterine Growth Restriction Piglets with Different Growth Patterns before Weaning Metabolites 2022 12 1053 10.3390/metabo12111053 36355136
Qi M. Tan B. Wang J. Liao S. Li J. Cui Z. Shao Y. Ji P. Yin Y. Postnatal growth retardation is associated with deteriorated intestinal mucosal barrier function using a porcine model J. Cell. Physiol. 2021 236 2631 2648 10.1002/jcp.30028 32853405
Li Y. Zhang H. Su W. Ying Z. Chen Y. Zhang L. Lu Z. Wang T. Effects of dietary Bacillus amyloliquefaciens supplementation on growth performance, intestinal morphology, inflammatory response, and microbiota of intra-uterine growth retarded weanling piglets J. Anim. Sci. Biotechnol. 2018 9 22 10.1186/s40104-018-0236-2 29564121
Wang X. Zhu Y. Feng C. Lin G. Wu G. Li D. Wang J. Innate differences and colostrum-induced alterations of jejunal mucosal proteins in piglets with intra-uterine growth restriction Br. J. Nutr. 2018 119 734 747 10.1017/S0007114518000375
Vaughan A.T. Roghanian A. Cragg M.S. B cells—Masters of the immunoverse Int. J. Biochem. Cell Biol. 2011 43 280 285 10.1016/j.biocel.2010.12.005
Bouaziz J.D. Calbo S. Maho-Vaillant M. Saussine A. Bagot M. Bensussan A. Musette P. IL-10 produced by activated human B cells regulates CD4+ T-cell activation in vitro Eur. J. Immunol. 2010 40 2686 2691 10.1002/eji.201040673 20809522
Thursby E. Juge N. Introduction to the human gut microbiota Biochem. J. 2017 474 1823 1836 10.1042/BCJ20160510
Jandhyala S.M. Talukdar R. Subramanyam C. Vuyyuru H. Sasikala M. Reddy D.N. Role of the normal gut microbiota World J. Gastroenterol. WJG 2015 21 8787 10.3748/wjg.v21.i29.8787 26269668
Abraham C. Medzhitov R. Interactions between the host innate immune system and microbes in inflammatory bowel disease Gastroenterology 2011 140 1729 1737 10.1053/j.gastro.2011.02.012 21530739
D’Inca R. Kloareg M. Gras-Le Guen C. Le Huërou-Luron I. Intrauterine growth restriction modifies the developmental pattern of intestinal structure, transcriptomic profile, and bacterial colonization in neonatal pigs J. Nutr. 2010 140 925 931 10.3945/jn.109.116822 20335628
Zhang W. Ma C. Xie P. Zhu Q. Wang X. Yin Y. Kong X. Gut microbiota of newborn piglets with intrauterine growth restriction have lower diversity and different taxonomic abundances J. Appl. Microbiol. 2019 127 354 369 10.1111/jam.14304 31077497
Tang W. Zhang W. Azad M.A.K. Ma C. Zhu Q. Kong X. Metabolome, microbiome, and gene expression alterations in the colon of newborn piglets with intrauterine growth restriction Front. Microbiol. 2022 13 989060 10.3389/fmicb.2022.989060 36187985
Luo C. Xia B. Zhong R. Shen D. Li J. Chen L. Zhang H. Early-Life Nutrition Interventions Improved Growth Performance and Intestinal Health via the Gut Microbiota in Piglets Front. Nutr. 2021 8 783688 10.3389/fnut.2021.783688 35047544
Cruzat V. Macedo Rogero M. Noel Keane K. Curi R. Newsholme P. Glutamine: Metabolism and immune function, supplementation and clinical translation Nutrients 2018 10 1564 10.3390/nu10111564
Cui Y. Zhang L. Lu C. Dou M. Jiao Y. Bao Y. Shi W. Effects of compound small peptides of Chinese medicine on intestinal immunity and cecal intestinal flora in CTX immunosuppressed mice Front. Microbiol. 2022 13 959726 10.3389/fmicb.2022.959726
Teixeira L.G. Leonel A.J. Aguilar E.C. Batista N.V. Alves A.C. Coimbra C.C. Ferreira A.V. de Faria A.M.C. Cara D.C. Alvarez Leite J.I. The combination of high-fat diet-induced obesity and chronic ulcerative colitis reciprocally exacerbates adipose tissue and colon inflammation Lipids Health Dis. 2011 10 204 10.1186/1476-511X-10-204 22073943
Xia B. Zhong R. Wu W. Luo C. Meng Q. Gao Q. Zhao Y. Chen L. Zhang S. Zhao X. Mucin O-glycan-microbiota axis orchestrates gut homeostasis in a diarrheal pig model Microbiome 2022 10 139 10.1186/s40168-022-01326-8
Houghteling P.D. Walker W.A. Why is initial bacterial colonization of the intestine important to infants’ and children’s health? J. Pediatr. Gastroenterol. Nutr. 2015 60 294 307 10.1097/MPG.0000000000000597 25313849
Nakagawa Y. Shimano H. CREBH regulates systemic glucose and lipid metabolism Int. J. Mol. Sci. 2018 19 1396 10.3390/ijms19051396 29738435
Nakagawa Y. Satoh A. Yabe S. Furusawa M. Tokushige N. Tezuka H. Mikami M. Iwata W. Shingyouchi A. Matsuzaka T. Hepatic CREB3L3 controls whole-body energy homeostasis and improves obesity and diabetes Endocrinology 2014 155 4706 4719 10.1210/en.2014-1113 25233440
Min A.-K. Jeong J. Go Y. Choi Y.-K. Kim Y.-D. Lee I.-K. Park K.-G. cAMP response element binding protein H mediates fenofibrate-induced suppression of hepatic lipogenesis Diabetologia 2013 56 412 422 10.1007/s00125-012-2771-2 23150180
Ruppert P.M. Park J.-G. Xu X. Hur K.Y. Lee A.-H. Kersten S. Transcriptional profiling of PPARα−/− and CREB3L3−/− livers reveals disparate regulation of hepatoproliferative and metabolic functions of PPARα BMC Genom. 2019 20 199 10.1186/s12864-019-5563-y 30866796
Sampieri L. Di Giusto P. Alvarez C. CREB3 transcription factors: ER-golgi stress transducers as hubs for cellular homeostasis Front. Cell Dev. Biol. 2019 7 123 10.3389/fcell.2019.00123
Wu Z. Chen S. Jia X. Lai S. Association of a synonymous mutation of the PGAM2 gene and growth traits in rabbits Czech J. Anim. Sci 2015 60 139 144 10.17221/8079-CJAS
Xu Y. Li F. Lv L. Li T. Zhou X. Deng C.-X. Guan K.-L. Lei Q.-Y. Xiong Y. Oxidative stress activates SIRT2 to deacetylate and stimulate phosphoglycerate mutase Cancer Res. 2014 74 3630 3642 10.1158/0008-5472.CAN-13-3615
Naini A. Toscano A. Musumeci O. Vissing J. Akman H.O. DiMauro S. Muscle phosphoglycerate mutase deficiency revisited Arch. Neurol. 2009 66 394 398 10.1001/archneurol.2008.584
Zhou H. Brekman A. Zuo W.-L. Ou X. Shaykhiev R. Agosto-Perez F.J. Wang R. Walters M.S. Salit J. Strulovici-Barel Y. POU2AF1 functions in the human airway epithelium to regulate expression of host defense genes J. Immunol. 2016 196 3159 3167 10.4049/jimmunol.1502400 26927796
Corcoran L. Emslie D. Kratina T. Shi W. Hirsch S. Taubenheim N. Chevrier S. Oct2 and Obf1 as facilitators of B: T cell collaboration during a humoral immune response Front. Immunol. 2014 5 108 10.3389/fimmu.2014.00108 24688485
Yang J. Reth M. Oligomeric organization of the B-cell antigen receptor on resting cells Nature 2010 467 465 469 10.1038/nature09357 20818374
Pelanda R. Braun U. Hobeika E. Nussenzweig M.C. Reth M. B cell progenitors are arrested in maturation but have intact VDJ recombination in the absence of Ig-α and Ig-β J. Immunol. 2002 169 865 872 10.4049/jimmunol.169.2.865 12097390
Choi J. Zhou N. Busino L. KLHL6 is a tumor suppressor gene in diffuse large B-cell lymphoma Cell Cycle 2019 18 249 256 10.1080/15384101.2019.1568765 30646831
Pizzorno J.E. Murray M.T. Joiner-Bey H. The Clinician’s Handbook of Natural Medicine E-Book Elsevier Health Sciences Maryland Heights, MO, USA 2016
Pan H. Liu Z. Roles of dietary fiber and gut microbial metabolites short-chain fatty acids in regulating mitochondrial function in central nervous system Molecular Nutrition and Mitochondria Elsevier Amsterdam, The Netherlands 2023 243 251
Thakur B.K. Dasgupta N. Ta A. Das S. Physiological TLR5 expression in the intestine is regulated by differential DNA binding of Sp1/Sp3 through simultaneous Sp1 dephosphorylation and Sp3 phosphorylation by two different PKC isoforms Nucleic Acids Res. 2016 44 5658 5672 10.1093/nar/gkw189 27060138
Jiang L. Wang J. Liu Z. Jiang A. Li S. Wu D. Zhang Y. Zhu X. Zhou E. Wei Z. Sodium butyrate alleviates lipopolysaccharide-induced inflammatory responses by down-regulation of NF-κB, NLRP3 signaling pathway, and activating histone acetylation in bovine macrophages Front. Vet. Sci. 2020 7 579674 10.3389/fvets.2020.579674
Lee C. Kim B.G. Kim J.H. Chun J. Im J.P. Kim J.S. Sodium butyrate inhibits the NF-kappa B signaling pathway and histone deacetylation, and attenuates experimental colitis in an IL-10 independent manner Int. Immunopharmacol. 2017 51 47 56 10.1016/j.intimp.2017.07.023
Heimann E. Nyman M. Pålbrink A.-K. Lindkvist-Petersson K. Degerman E. Branched short-chain fatty acids modulate glucose and lipid metabolism in primary adipocytes Adipocyte 2016 5 359 368 10.1080/21623945.2016.1252011
Schroeder B.O. Fight them or feed them: How the intestinal mucus layer manages the gut microbiota Gastroenterol. Rep. 2019 7 3 12 10.1093/gastro/goy052 30792861
Liu Y. Azad M.A.K. Zhu Q. Yu Z. Kong X. Dietary bile acid supplementation alters plasma biochemical and hormone indicators, intestinal digestive capacity, and microbiota of piglets with normal birth weight and intrauterine growth retardation Front. Microbiol. 2022 13 1053128 10.3389/fmicb.2022.1053128
Jiang L. Feng C. Tao S. Li N. Zuo B. Han D. Wang J. Maternal imprinting of the neonatal microbiota colonization in intrauterine growth restricted piglets: A review J. Anim. Sci. Biotechnol. 2019 10 1 8 10.1186/s40104-019-0397-7 31737268
Sharma G. Garg N. Hasan S. Shirodkar S. Prevotella: An insight into its characteristics and associated virulence factors Microb. Pathog. 2022 169 105673 10.1016/j.micpath.2022.105673 35843443
Ley R.E. Prevotella in the gut: Choose carefully Nat. Rev. Gastroenterol. Hepatol. 2016 13 69 70 10.1038/nrgastro.2016.4
Tong L.-T. Xiao T. Wang L. Lu C. Liu L. Zhou X. Wang A. Qin W. Wang F. Plant protein reduces serum cholesterol levels in hypercholesterolemia hamsters by modulating the compositions of gut microbiota and metabolites Iscience 2021 24 103435 10.1016/j.isci.2021.103435
Ormerod K.L. Wood D.L. Lachner N. Gellatly S.L. Daly J.N. Parsons J.D. Dal’Molin C.G. Palfreyman R.W. Nielsen L.K. Cooper M.A. Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals Microbiome 2016 4 36 10.1186/s40168-016-0181-2
Lopetuso L.R. Scaldaferri F. Petito V. Gasbarrini A. Commensal Clostridia: Leading players in the maintenance of gut homeostasis Gut Pathog. 2013 5 23 10.1186/1757-4749-5-23
Li Z. Liu S. Zhao Y. Wang J. Ma X. Compound organic acid could improve the growth performance, immunity and antioxidant properties, and intestinal health by altering the microbiota profile of weaned piglets J. Anim. Sci. 2023 101 skad196 10.1093/jas/skad196
Accetto T. Avguštin G. The diverse and extensive plant polysaccharide degradative apparatuses of the rumen and hindgut Prevotella species: A factor in their ubiquity? Syst. Appl. Microbiol. 2019 42 107 116 10.1016/j.syapm.2018.10.001
Zhao L. Zhang F. Ding X. Wu G. Lam Y.Y. Wang X. Fu H. Xue X. Lu C. Ma J. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes Science 2018 359 1151 1156 10.1126/science.aao5774 29590046
Huang C. Ge F. Yao X. Guo X. Bao P. Ma X. Wu X. Chu M. Yan P. Liang C. Microbiome and metabolomics reveal the effects of different feeding systems on the growth and ruminal development of yaks Front. Microbiol. 2021 12 682989 10.3389/fmicb.2021.682989 34248900
Wang B. Luo Y. Su R. Yao D. Hou Y. Liu C. Du R. Jin Y. Impact of feeding regimens on the composition of gut microbiota and metabolite profiles of plasma and feces from Mongolian sheep J. Microbiol. 2020 58 472 482 10.1007/s12275-020-9501-0 32323198
Lin H. Meng L. Sun Z. Sun S. Huang X. Lin N. Zhang J. Lu W. Yang Q. Chi J. Yellow wine polyphenolic compound protects against doxorubicin-induced cardiotoxicity by modulating the composition and metabolic function of the gut microbiota Circ. Heart Fail. 2021 14 e008220 10.1161/CIRCHEARTFAILURE.120.008220 34665676
Lundell A.-C. Björnsson V. Ljung A. Ceder M. Johansen S. Lindhagen G. Törnhage C.-J. Adlerberth I. Wold A.E. Rudin A. Infant B cell memory differentiation and early gut bacterial colonization J. Immunol. 2012 188 4315 4322 10.4049/jimmunol.1103223
Huang Y. Tang J. Cai Z. Zhou K. Chang L. Bai Y. Ma Y. Prevotella induces the production of Th17 cells in the colon of mice J. Immunol. Res. 2020 2020 9607328 10.1155/2020/9607328 33204736
Takeuchi Y. Hirota K. Sakaguchi S. Impaired T cell receptor signaling and development of T cell–mediated autoimmune arthritis Immunol. Rev. 2020 294 164 176 10.1111/imr.12841 31944330
Larsen J.M. The immune response to Prevotella bacteria in chronic inflammatory disease Immunology 2017 151 363 374 10.1111/imm.12760
Hua Z. Hou B. TLR signaling in B-cell development and activation Cell. Mol. Immunol. 2013 10 103 106 10.1038/cmi.2012.61
Bunker J.J. Flynn T.M. Koval J.C. Shaw D.G. Meisel M. McDonald B.D. Ishizuka I.E. Dent A.L. Wilson P.C. Jabri B. Innate and adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A Immunity 2015 43 541 553 10.1016/j.immuni.2015.08.007
Babbar A. Hitch T.C. Pabst O. Clavel T. Hübel J. Eswaran S. Wagner N. Schippers A. The compromised mucosal immune system of β7 integrin-deficient mice has only minor effects on the fecal microbiota in homeostasis Front. Microbiol. 2019 10 2284 10.3389/fmicb.2019.02284 31636620
Shan Y. Sun C. Li J. Shao X. Wu J. Zhang M. Yao H. Wu X. Characterization of Purified Mulberry Leaf Glycoprotein and Its Immunoregulatory Effect on Cyclophosphamide-Treated Mice Foods 2022 11 2034 10.3390/foods11142034 35885277
Jiang S. Xie S. Lv D. Wang P. He H. Zhang T. Zhou Y. Lin Q. Zhou H. Jiang J. Alteration of the gut microbiota in Chinese population with chronic kidney disease Sci. Rep. 2017 7 2870 10.1038/s41598-017-02989-2 28588309
Han M. Zhang M. Wang X. Bai X. Yue T. Gao Z. Cloudy apple juice fermented by Lactobacillus prevents obesity via modulating gut microbiota and protecting intestinal tract health Nutrients 2021 13 971 10.3390/nu13030971 33802755
Gao Q. Sun G. Duan J. Luo C. Yangji C. Zhong R. Chen L. Zhu Y. Wangdui B. Zhang H. Alterations in gut microbiota improve SCFA production and fiber utilization in Tibetan pigs fed alfalfa diet Front. Microbiol. 2022 13 969524 10.3389/fmicb.2022.969524
Wang L. Ren B. Hui Y. Chu C. Zhao Z. Zhang Y. Zhao B. Shi R. Ren J. Dai X. Methionine restriction regulates cognitive function in high-fat diet-fed mice: Roles of diurnal rhythms of SCFAs producing-and inflammation-related microbes Mol. Nutr. Food Res. 2020 64 2000190 10.1002/mnfr.202000190
