Abstract
To study the effect of weaning age on the gut microbiota diversity in the lambs of Chongming white goats, fresh feces from the lambs weaned at 30, 45, and 60 days of age were collected 3 days after weaning at 33, 48, and 63 days of age, for microbial composition analysis by 16S rRNA sequencing. The serum concentrations of lipid metabolites were also investigated at the fecal collection dates. Serum and feces from the ewe-reared groups at 33, 48, and 63 days of age were used as controls. The alpha diversity increased significantly after weaning and with the aging of the lambs. Levels of Ruminococcaceae, Lachnospiraceae, and Ruminococcus varied significantly according to the weaning treatment in lambs (P < 0.05). Butyrate-producing gut bacteria such as Ruminococcaceae_UCG-010, Ruminococcaceae_UCG-013, Ruminococcaceae_UCG-014, Ruminococcaceae_UCG-005, Ruminococcaceae_UCG-002, Lachnospiraceae_AC2044_group, and Lachnospiraceae_NK4B4 were identified as significantly increased genera (P < 0.05) in the feces of weaned Chongming white lambs. Additionally, the abundance of fiber degradation–associated bacteria including Ruminococcaceae_UCG-005, Ruminococcus_1, and Ruminococcus_2 significantly increased with lamb weaning age (P < 0.05). Correlation analysis showed that Lachnospiraceae_AC2044_group, norank_f__Bacteroidales_S24-7_group, and Ruminococcaceae_UCG_005 were negatively correlated, and Lachnoclostridium was positively correlated with levels of cholesterol, while Blautia showed positive correlation with low-density lipoprotein cholesterol in serum samples from weaned lambs. This study helped to understand the maturing development of gut microbiota in Chongming white goats under weaning stress.
Key points
• Effects of weaning age on the gut microbiota diversity in Chongming white goat lambs were studied.
• Some butyrate-producing gut bacteria were significantly increased after weaned.
• Correlations of gut microbiota and lipid metabolites were analyzed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available in the NCBI repository with accession No. SRR13334808 (available at https://www.ncbi.nlm.nih.gov/sra/?term=SRR13334808).
References
Anthony MB, Marc L, Bjoern U (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Brulc J, Antonopoulos D, Miller M, Wilson M, Yannarell A, Dinsdale E, Edwards R, Frank E, Emerson J, Wacklin P, Coutinho P, Henrissat B, Nelson K, White B (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci U S A 106(6):1948–1953. https://doi.org/10.1073/pnas.0806191105
Chai J, Diao Q, Wang H, Tu Y, Tao X, Zhang N (2015) Effects of weaning age on growth, nutrient digestibility and metabolism, and serum parameters in Hu lambs. Anim Nutr 1(4):344–348. https://doi.org/10.1016/j.aninu.2015.11.007
Chika K, Kazushi S, Isao M, Junichiro T, Yumi O, Hidekazu I, Masahiko T, Katsuya S, Masaaki I, Yoshiyuki T, Kojiro T (2015) Comparison of the gut microbiota composition between obese and non-obese individuals in a Japanese population, as analyzed by terminal restriction fragment length polymorphism and next-generation sequencing. BMC Gastroenterol 15:100. https://doi.org/10.1186/s12876-015-0330-2
Clarke SF, Murphy EF, O’Sullivan O, Lucey AJ, Humphreys M, Hogan A, Hayes P, O’Reilly M, Jeffery IB, Wood-Martin R (2014) Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63(12):1913–1920. https://doi.org/10.1136/gutjnl-2013-306541
Edgar R, Haas B, Clemente J, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Ekanayake LJ, Corner-Thomas R, Cranston L, Kenyon P, Morris S (2018) A comparison of liveweight gain of lambs weaned early onto a herb-clover mixed sward and weaned conventionally onto a ryegrass-clover pasture. Asian-Australas J Anim Sci 32(2):201–208. https://doi.org/10.5713/ajas.18.0301
Ekiz B, Kocak O, Yalcintan H, Yilmaz A (2015) Effects of suckling duration on growth, slaughtering and carcass quality characteristics of Kivircik lambs. Trop Anim Health Prod 48(2):395–401. https://doi.org/10.1007/s11250-015-0964-7
Esquivel-Elizondo S, Ilhan ZE, Garcia-Peña EI, Krajmalnik-Brown R (2017) Insights into butyrate production in a controlled fermentation system via gene predictions. mSystems 2(4):e00051–e00017. https://doi.org/10.1128/mSystems.00051-17
Geirnaert A, Calatayud M, Grootaert C, Laukens D, Devriese S, Smagghe G, De Vos M, Boon N, Van de Wiele T (2017) Butyrate-producing bacteria supplemented in vitro to Crohn’s disease patient microbiota increased butyrate production and enhanced intestinal epithelial barrier integrity. Sci Rep 7(1):11450. https://doi.org/10.1038/s41598-017-11734-8
Gibson GR (2010) Physiology and ecology of the sulphate-reducing bacteria. J Appl Bacteriol 69(6):769–797. https://doi.org/10.1038/nrmicro1892
Guerra C, Heintz-Buschart A, Sikorski J, Chatzinotas A, Guerrero-Ramírez N, Cesarz S, Beaumelle L, Rillig M, Maestre F, Delgado-Baquerizo M, Buscot F, Overmann J, Patoine G, Phillips H, Winter M, Wubet T, Küsel K, Bardgett R, Cameron E, Cowan D, Grebenc T, Marín C, Orgiazzi A, Singh B, Wall D, Eisenhauer N (2020) Blind spots in global soil biodiversity and ecosystem function research. Nat Commun 11(1):3870. https://doi.org/10.1038/s41467-020-17688-2
Hills R, Pontefract B, Mishcon H, Black C, Sutton S, Theberge C (2019) Gut microbiome: profound implications for diet and disease. Nutrients 11(7):1613. https://doi.org/10.3390/nu11071613
Huan L, Tongtong L, Beasley DE, Petr H, Zhishu X, Shiheng Z, Jiabao L, Qiang L, **angzhen L (2016) Diet diversity is associated with beta but not alpha diversity of pika gut microbiota. Front Microbiol 7:1169. https://doi.org/10.3389/fmicb.2016.01169
Konstantinov S, Awati A, Williams B, Miller B, Jones P, Stokes C, Akkermans A, Smidt H, de Vos W (2006) Post-natal development of the porcine microbiota composition and activities. Environ Microbiol 8(7):1191–1199. https://doi.org/10.1111/j.1462-2920.2006.01009.x
Le Roy T, Lécuyer E, Chassaing B, Rhimi M, Lhomme M, Boudebbouze S, Ichou F, Haro Barceló J, Huby T, Guerin M, Giral P, Maguin E, Kapel N, Gérard P, Clément K, Lesnik P (2019) The intestinal microbiota regulates host cholesterol homeostasis. BMC Biol 17(1):94. https://doi.org/10.1186/s12915-019-0715-8
Lepherd ML, Canfield PJ, Hunt GB, Bosward KL (2010) Haematological, biochemical and selected acute phase protein reference intervals for weaned female Merino lambs. Aust Vet J 87(1):5–11. https://doi.org/10.1111/j.1751-0813.2008.00382.x
Li C, Wang W, Liu T, Zhang Q, Wang G, Li F, Li F, Yue X, Li T (2018a) Effect of early weaning on the intestinal microbiota and expression of genes related to barrier function in lambs. Front Microbiol 9:1431. https://doi.org/10.3389/fmicb.2018.01431
Li P, Xue Y, Shi J, Pan A, Tang X, Ming F (2018b) The response of dominant and rare taxa for fungal diversity within different root environments to the cultivation of Bt and conventional cotton varieties. Microbiome 6(1):184. https://doi.org/10.1186/s40168-018-0570-9
Lin Z, Ye W, Zu X, **e H, Li H, Li Y, Zhang W (2018) Integrative metabolic and microbial profiling on patients with Spleen-yang-deficiency syndrome. Sci Rep 8(1):6619. https://doi.org/10.1038/s41598-018-24130-7
Mach N, Foury A, Kittelmann S, Reigner F, Moroldo M, Ballester M, Esquerré D, Rivière J, Sallé G, Gérard P, Moisan M, Lansade L (2017) The effects of weaning methods on gut microbiota composition and horse physiology. Front Physiol 8:535. https://doi.org/10.3389/fphys.2017.00535
Magoč T, Salzberg S (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Meale S, Li S, Azevedo P, Derakhshani H, DeVries T, Plaizier J, Steele M, Khafipour E (2017) Weaning age influences the severity of gastrointestinal microbiome shifts in dairy calves. Sci Rep 7(1):198. https://doi.org/10.1038/s41598-017-00223-7
Meehan C, Beiko R (2014) A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol 6(3):703–713. https://doi.org/10.1093/gbe/evu050
Méndez-Salazar E, Ortiz-López M, Granados-Silvestre M, Palacios-González B, Menjivar M (2018) Firmicutes altered gut microbiota and compositional changes in and in Mexican undernourished and obese children. Front Microbiol 9:2494. https://doi.org/10.3389/fmicb.2018.02494
Murugesan S, Ulloa-Martínez M, Martínez-Rojano H, Galván-Rodríguez F, Miranda-Brito C, Romano M, Piña-Escobedo A, Pizano-Zárate M, Hoyo-Vadillo C, García-Mena J (2015) Study of the diversity and short-chain fatty acids production by the bacterial community in overweight and obese Mexican children. Eur J Clin Microbiol Infect Dis 34(7):1337–1346. https://doi.org/10.1007/s10096-015-2355-4
Nagalingam N, Kao J, Young V (2011) Microbial ecology of the murine gut associated with the development of dextran sodium sulfate-induced colitis. Inflamm Bowel Dis 17(4):917–926. https://doi.org/10.1002/ibd.21462
Nirmalkar K, Murugesan S, Pizano-Zárate M, Villalobos-Flores L, García-González C, Morales-Hernández R, Nuñez-Hernández J, Hernández-Quiroz F, Romero-Figueroa M, Hernández-Guerrero C, Hoyo-Vadillo C, García-Mena J (2018) Gut microbiota and endothelial dysfunction markers in obese Mexican children and adolescents. Nutrients 10(12):2009. https://doi.org/10.3390/nu10122009
Rowan F, Docherty NG, Murphy M, Murphy B, Coffey JC, O’Connell PR (2010) Desulfovibrio bacterial species are increased in ulcerative colitis. Dis Colon Rectum 53(11):1530–1536. https://doi.org/10.1007/DCR.0b013e3181f1e620
Shaw KL, Nolan JV, Lynch JJ, Coverdale OR, Gill HS (1995) Effects of weaning, supplementation and gender on acquired immunity to Haemonchus contortus in lambs. Int J Parasitol 25(3):381–387. https://doi.org/10.1016/0020-7519(94)00098-9
Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, Thangaraju M, Prasad P, Manicassamy S, Munn D, Lee J, Offermanns S, Ganapathy V (2014) Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 40(1):128–139. https://doi.org/10.1016/j.immuni.2013.12.007
Tang W, Yao X, **a F, Yang M, Chen Z, Zhou B, Liu Q (2018) Modulation of the gut microbiota in rats by Hugan Qingzhi Tablets during the treatment of high-fat-diet-induced nonalcoholic fatty liver disease. Oxidative Med Cell Longev 2018:7261619–7261614. https://doi.org/10.1155/2018/7261619
Teke B, Akdag F (2012) The effects of age of lamb and parity of dam and sex and birth type of lamb on suckling behaviors of Karayaka lambs. Small Rumin Res 103(2-3):176–181. https://doi.org/10.1016/j.smallrumres.2011.08.012
Thursby E, Juge N (2017) Introduction to the human gut microbiota. Biochem J 474(11):1823–1836. https://doi.org/10.1042/BCJ20160510
Vital M, Howe A, Tiedje J (2014) Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. mBio 5(2):e00889. https://doi.org/10.1128/mBio.00889-14
Yang H, **ao Y, Wang J, **ang Y, Gong Y, Wen X, Li D (2018) Core gut microbiota in **hua pigs and its correlation with strain, farm and weaning age. J Microbiol 56(5):346–355. https://doi.org/10.1007/s12275-018-7486-8
Zhang J, Xu C, Huo D, Hu Q, Peng Q (2017) Comparative study of the gut microbiome potentially related to milk protein in Murrah buffaloes (Bubalus bubalis) and Chinese Holstein cattle. Sci Rep 7:42189. https://doi.org/10.1038/srep42189
Zhang Q, Li C, Niu X, Zhang Z, Li F, Li F (2018) An intensive milk replacer feeding program benefits immune response and intestinal microbiota of lambs during weaning. BMC Vet Res 14(1):366. https://doi.org/10.1186/s12917-018-1691-x
Funding
This research was, in part or in whole, supported by the National Natural Science Foundation of China (Grant No. 31902149), Shanghai Agriculture Applied Technology Development Program (Grant No. Z20200105), and Shanghai Committee of Science and Technology (Grant No. 19140900100).
Author information
Authors and Affiliations
Contributions
R.R. L., Y.X. L., and L.H. Z. conceived and designed the research. R.R. L., Y.H. L., J.J. D., and L.H. Z. performed experiments. R.R. L. and X.H. X. analyzed the data. R.R. L., X.H. X., and L.H. Z. wrote the manuscript. All authors read, revised, and approved the manuscript.
Corresponding authors
Ethics declarations
This study was conducted based on the suggestions of the Guides for Experimental Animals established by the Ethics and Animal Welfare Committee of Shanghai Academy of Agricultural Sciences (Shanghai, China).
Ethics approval
This article does not contain any studies with human participants performed by any of the authors.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(PDF 113 kb).
Rights and permissions
About this article
Cite this article
Liao, R., **e, X., LV, Y. et al. Ages of weaning influence the gut microbiota diversity and function in Chongming white goats. Appl Microbiol Biotechnol 105, 3649–3658 (2021). https://doi.org/10.1007/s00253-021-11301-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-021-11301-2