Please wait a minute...
Journal of Integrative Agriculture  2023, Vol. 22 Issue (2): 537-550    DOI: 10.1016/j.jia.2022.08.055
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
The succession of fecal bacterial community and its correlation with the changes of serum immune indicators in lambs from birth to 4 months
YIN Xue-jiao*, JI Shou-kun*, DUAN Chun-hui, TIAN Pei-zhi, JU Si-si, YAN Hui, ZHANG Ying-jie, LIU Yue-qin

College of Animal Science and Technology, Hebei Agricultural University, Baoding 071000, P.R.China

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      

微生物在胃肠道发育早期的定植和演替过程对于宿主免疫系统的发育十分重要。本试验以湖羊为研究对象,选择10只初生湖羊母羔(2.87 ± 0.28 kg),利用16S rDNA测序手段,测定0,3,10,20,30,45,60,90,120日龄羔羊粪便细菌区系,探究羔羊从出生至120日龄,体重、血清指标和粪便细菌群落的动态变化,及三者之间的关系。研究结果表明,羔羊生长性能、血清指标、粪便细菌群落和粪便细菌功能均受羔羊日龄的影响(P<0.05)。羔羊平均日增重在60-90日龄时最低(P<0.05),可能是断奶应激造成。羔羊的免疫反应在30日龄时最高,此时羔羊血清中免疫球蛋白(免疫球蛋白A,免疫球蛋白G,免疫球蛋白M)、细胞因子(白细胞介素-,白细胞介素-6,白细胞介素-12、白细胞介素-17、肿瘤坏死因子-α)和肠道通透性指标(D-乳酸和内毒素)水平高于其它日龄组(P<0.05)。各日龄组内粪便细菌群落相似性分析表明,同日龄组内相似性在断奶前较低,在断奶(60日龄)后显著增加(P<0.05)。各日龄与120日龄粪便细菌群落相似性表明,30日龄后,与120日龄的相似性显著增加(P<0.05)。粪便细菌属Lachnospiraceae UCG-010, Eubacterium coprostanoligenes group, Ruminococcaceae UCG-005, Ruminococcaceae UCG-009, Ruminococcaceae UCG-013, Ruminiclostridium 6, Ruminococcaceae UCG-008Oscillibacter与血清中内毒素、D-乳酸、免疫球蛋白(免疫球蛋白A,免疫球蛋白G,免疫球蛋白M)、细胞免疫因子(白细胞介素-,白细胞介素-6,白细胞介素-12和白细胞介素-17)和肿瘤坏死因子-α水平呈负相关(P<0.05),并且这些属的相对丰度从45日龄时增加。本研究结果表明,与血清免疫指标相关属的相对丰度从45日龄起随羔羊年龄增加,羔羊出生至45日龄可能存在关键调控时期,为调控羔羊微生物以提高羔羊免疫性能提供机会。本研究分析比较了羔羊初生至120日龄,粪便细菌建立过程及其与羔羊体重和血清免疫指标的关系,分析发现了调控羔羊微生物区系的关键时期。


Early bacterial colonization and succession within the gastrointestinal tract have been suggested to be crucial in the development of host immunity.  In this study, we have investigated the changes in live weight and concentrations of selected serum parameters in relation to their fecal bacterial communities as determined by high throughput sequencing of the 16S rRNA gene over the same period in lambs.  The results showed that lambs’ growth performance, the serum parameters, fecal bacterial community and fecal bacterial functions were all affected (P<0.05) by age of the lambs.  Similarity within age groups of fecal microbiota was lower in the preweaning period and increased sharply (P<0.05) after weaning at 60 days.  The similarity between the samples collected from birth to 90 days of age and those collected at 120 days of age, increased (P<0.05) sharply after 30 days of age.  Some age-associated changes in microbial genera were correlated with the changes in concentrations of immune indicators, including negative (P<0.05) correlations between the relative abundance of Lachnospiraceae UCG-010, Eubacterium coprostanoligenes group, Ruminococcaceae UCG-005, Ruminococcaceae UCG-009, Ruminococcaceae UCG-013, Ruminiclostridium 6, Ruminococcaceae UCG-008, and Oscillibacter with serum concentrations of lipopolysaccharide (LPS), D-lactate dehydrogenase (DLA), immunoglobulin (IgA, IgM, and IgG), and cytokines (interleukin-1β (IL-1β), IL-6, IL-12, and IL-17), tumor necrosis factor-α (TNF-α), and the relative abundance of these genera increased from 45 days of age.  In conclusion, these results suggested that the age-related abundances of particular genera were correlated with serum markers of immunity in lambs, and there might be a critical window in the period from birth to 45 days of age which provide an opportunity for potential manipulation of the fecal microbial ecosystems to enhance immune function.

Keywords:  fecal bacteria       establishment        sheep        serum parameter        early life  
Received: 01 September 2021   Accepted: 31 March 2022
Fund: This study was supported by the China Agriculture Research System of MARA and MOF (CARS-38), the National Key Research & Development Program of China (2018YFD0502100) and the Scientific Research Foundation of Hebei Agricultural University, China (YJ201825).  

About author:  Received 1 September, 2021 Accepted 31 March, 2022 YIN Xue-jiao, E-mail:; Correspondence ZHANG Ying-jie, Tel: +86-312-7528366, E-mail: zhangyingjie66@ * These authors contributed equally to this study.

Cite this article: 

YIN Xue-jiao, JI Shou-kun, DUAN Chun-hui, TIAN Pei-zhi, JU Si-si, YAN Hui, ZHANG Ying-jie, LIU Yue-qin. 2023. The succession of fecal bacterial community and its correlation with the changes of serum immune indicators in lambs from birth to 4 months. Journal of Integrative Agriculture, 22(2): 537-550.

Arrieta M C, Stiemsma L T, Amenyogbe N, Brown E M, Finlay B. 2014. The intestinal microbiome in early life: health and disease. Frontiers in Immunology, 5, 427. 
Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende D R, Fernandes G R, Tap J, Bruls T, Batto J M, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, et al. 2011. Enterotypes of the human gut microbiome. Nature, 473, 174–180. 
Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende D R, Fernandes G R, Tap J, Bruls T, Batto J M, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, et al. 2014. Addendum: Enterotypes of the human gut microbiome. Nature, 506, 516. 
Breiman L. 2001. Random forests. Machine Learning, 45, 5–32.
Browne H P, Forster S C, Anonye B O, Kumar N, Neville B A, Stares M D, Goulding D, Lawley T D. 2016. Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature, 533, 543–546.
Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336.
Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Huntley J, Fierer N, Owens S M, Betley J, Fraser L, Bauer M, Gormley N, Gilbert J A, Smith G, Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6, 1621–1624.
Cheng S, Ma X, Geng S, Jiang X, Li Y, Hu L, Li J, Wang Y, Han X. 2018. Fecal microbiota transplantation beneficially regulates intestinal mucosal autophagy and alleviates gut barrier injury. mSystems, 3, e00137–e00155.
Correa-Oliveira R, Fachi J L, Vieira A, Sato F T, Vinolo M A. 2016. Regulation of immune cell function by short-chain fatty acids. Clinical & Translational Immunology, 5, e73. 
Dill-McFarland K A, Breaker J D, Suen G. 2017. Microbial succession in the gastrointestinal tract of dairy cows from 2 weeks to first lactation. Scientific Reports, 7, 40864.
Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998. 
Faith J J, Guruge J L, Charbonneau M, Subramanian S, Seedorf H, Goodman A L, Clemente J C, Knight R, Heath A C, Leibel R L, Rosenbaum M, Gordon J I. 2013. The long-term stability of the human gut microbiota. Science, 341, 2862.
Falentin H, Rault L, Nicolas A, Bouchard D S, Lassalas J, Lamberton P, Aubry J M, Marnet P G, Le Loir Y, Even S. 2016. Bovine teat microbiome analysis revealed reduced alpha diversity and significant changes in taxonomic profiles in quarters with a history of mastitis. Frontiers in Microbiology, 7, 480. 
Geng S T, Zhang Z Y, Wang Y X, Lu D, Yu J, Zhang J B, Kuang Y Q, Wang K H. 2020. Regulation of gut microbiota on immune reconstitution in patients with acquired immunodeficiency syndrome. Frontiers in Microbiology, 11, 594820. 
Guo C Y, Ji S K, Yan H, Wang Y J, Liu J J, Cao Z J, Yang H J, Zhang W J, Li S L. 2020. Dynamic change of the gastrointestinal bacterial ecology in cows from birth to adulthood. Microbiology Open, 9, e1119.
Hill C J, Lynch D B, Murphy K, Ulaszewska M, Jeffery I B, O’Shea C A, Watkins C, Dempsey E, Mattivi F, Tuohy K, Ross R P, Ryan C A, O’Toole P W, Stanton C. 2017. Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort. Microbiome, 5, 4. 
Ivanov I I, Atarashi K, Manel N, Brodie E L, Shima T, Karaoz U, Wei D, Goldfarb K C, Santee C A, Lynch S V, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman D R. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell, 139, 485–498. 
Koch M A, Reiner G L, Lugo K A, Kreuk L S, Stanbery A G, Ansaldo E, Seher T D, Ludington W B, Barton G M. 2016. Maternal IgG and IgA antibodies dampen mucosal t helper cell responses in early life. Cell, 165, 827–841.
Kosiewicz M M, Zirnheld A L, Alard P. 2011. Gut microbiota, immunity, and disease: A complex relationship. Frontiers in Microbiology, 2, 180. 
Laforest-Lapointe I, Arrieta M C. 2017. Patterns of early-life gut microbial colonization during human immune development: An ecological perspective. Frontiers in Immunology, 8, 788.
Lécuyer E, Rakotobe S, Lengliné-Garnier H, Lebreton C, Picard M, Juste C, Fritzen R, Eberl G, McCoy K D, Macpherson A J, Reynaud C A, Cerf-Bensussan N, Gaboriau-Routhiau V. 2014. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity, 40, 608–620.
Li C, Zhang Q, Wang G, Niu X, Wang W, Li F, Li F, Zhang Z. 2022. The functional development of the rumen is influenced by weaning and associated with ruminal microbiota in lambs. Animal Biotechnology, 33, 612–628. 
Liang J Q, Li T, Nakatsu G, Chen Y X, Yau T O, Chu E, Wong S, Szeto C H, Ng S C, Chan F K L, Fang J Y, Sung J J Y, Yu J. 2020. A novel faecal Lachnoclostridium marker for the non-invasive diagnosis of colorectal adenoma and cancer. Gut, 69, 1248–1257. 
Liaw A, Wiener M. 2002. Classification and regression by random forest. R News, 23, 18–22.
Ma T, Villot C, Renaud D, Skidmore A, Chevaux E, Steele M, Guan L L. 2020. Linking perturbations to temporal changes in diversity, stability, and compositions of neonatal calf gut microbiota: prediction of diarrhea. The ISME Journal, 14, 2223–2235.
Munyaka P M, Eissa N, Bernstein C N, Khafipour E, Ghia J E. 2015. Antepartum antibiotic treatment increases offspring susceptibility to experimental colitis: A role of the gut microbiota. PLoS ONE, 10, e0142536. 
Nemati M, Amanlou H, Khorvash M, Moshiri B, Mirzaei M, Khan M A, Ghaffari M H. 2015. Rumen fermentation, blood metabolites, and growth performance of calves during transition from liquid to solid feed: Effects of dietary level and particle size of alfalfa hay. Journal of Dairy Science, 98, 7131–7141.
de Oliveira M N, Jewell K A, Freitas F S, Benjamin L A, Tótola M R, Borges A C, Moraes C A, Suen G 2013. Characterizing the microbiota across the gastrointestinal tract of a Brazilian Nelore steer. Veterinary Microbiology, 164, 307–314. 
Penders J, Stobberingh E E, van den Brandt P A, Thijs C. 2007. The role of the intestinal microbiota in the development of atopic disorders. Allergy, 62, 1223–1236. 
Rault L, Lévêque P A, Barbey S, Launay F, Larroque H, Le Loir Y, Germon P, Guinard-Flament J, Even S. 2020. Bovine teat cistern microbiota composition and richness are associated with the immune and microbial responses during transition to once-daily milking. Frontiers in Microbiology, 11, 602404.
Rodriguez J M, Murphy K, Stanton C, Ross R P, Kober O I, Juge N, Avershina E, Rudi K, Narbad A, Jenmalm M C, Marchesi J R, Collado M C. 2015. The composition of the gut microbiota throughout life, with an emphasis on early life. Microbial Ecology in Health and Disease, 26, 26050.
Schwaiger K, Storch J, Bauer C, Bauer J. 2020. Development of selected bacterial groups of the rectal microbiota of healthy calves during the first week postpartum. Journal of Applied Microbiology, 128, 366–375. 
Selber-Hnatiw S, Rukundo B, Ahmadi M, Akoubi H, Al-Bizri H, Aliu A F, Ambeaghen T U, Avetisyan L, Bahar I, Baird A, Begum F, Ben Soussan H, Blondeau-Éthier V, Bordaries R, Bramwell H, Briggs A, Bui R, Carnevale M, Chancharoen M, Chevassus T, et al. 2017. Human gut microbiota: Toward an ecology of disease. Frontiers in Microbiology, 8, 1265. 
Sommer F, Bäckhed F. 2013. The gut microbiota - masters of host development and physiology. Nature Reviews Microbiology, 11, 227–238.
Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam M A, Benezra A, DeStefano J, Meier M F, Muegge B D, Barratt M J, VanArendonk L G, Zhang Q, Province M A, Petri Jr W A, Ahmed T, Gordon J I. 2014. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature, 510, 417–421.
Vojinovic D, Radjabzadeh D, Kurilshikov A, Amin N, Wijmenga C, Franke L, Ikram M A, Uitterlinden A G, Zhernakova A, Fu J, Kraaij R, van Duijn C M. 2019. Relationship between gut microbiota and circulating metabolites in population-based cohorts. Nature Communications, 10, 5813. 
Wemheuer F, Taylor J A, Daniel R, Johnston E, Meinicke P, Thomas T, Wemheuer B. 2020. Tax4Fun2: prediction of habitat-specific functional profiles and functional redundancy based on 16S rRNA gene sequences. Environmental Microbiome, 15, 11.
Yassour M, Vatanen T, Siljander H, Hämäläinen A M, Härkönen T, Ryhänen S J, Franzosa E A, Vlamakis H, Huttenhower C, Gevers D, Lander E S, Knip M, Diabimmune Study Group, Xavier R J. 2016. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Science Translational Medicine, 8, 343ra381. 
Yin X, Ji S, Duan C, Ju S, Zhang Y, Yan H, Liu Y. 2021. Rumen fluid transplantation affects growth performance of weaned lambs by altering gastrointestinal microbiota, immune function and feed digestibility. Animal, 15, 100076. 
Yin X J, Ji S K, Duan C H, Tian P Z, Ju S S, Yan H, Zhang Y J, Liu Y Q. 2022. Dynamic change of fungal community in the gastrointestinal tract of growing lambs. Journal of Integrative Agriculture, 21, 3314–3328.
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 Veterinary Research, 14, 366.
Zhang X, Gu S, You L, Xu Y, Zhou D, Chen Y, Yan R, Jiang H, Li Y, Lv L, Qian W. 2020. Gut microbiome and metabolome were altered and strongly associated with platelet count in adult patients with primary immune thrombocytopenia. Frontiers in Microbiology, 11, 1550. 

No related articles found!
No Suggested Reading articles found!