|
Special Issue:
动物营养合辑Animal Nutrition
|
|
|
|
| Dynamic change of fungal community in the gastrointestinal tract of growing lambs |
| 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 |
|
|
|
|
摘要
胃肠道真菌群落对于动物的健康和生长性能十分重要，但目前其在消化道内的定植过程尚不清楚。本研究目的是探究生长羔羊从出生至四月龄胃肠道真菌群落的发育规律。本实验选择10只初生湖羊母羔（2.87 ± 0.28 kg）作为实验动物，利用IT1S rDNA测序手段，测定0,3,10,20,30,45,60,90,120日龄羔羊瘤胃和直肠内容物真菌区系，联合随机森林分析，探究10只湖羊母羔从出生至4月龄瘤胃和直肠真菌群落的动态变化，确定真菌区系在胃肠道的建立过程。结果表明，随着羔羊日龄的增加，胃肠道真菌群落的组成、多样性和菌群丰度受到显著影响(P<0.05)。在门水平上，Ascomycota和Basidiomycota在瘤胃和直肠样品中均占主导地位。各日龄组内瘤胃真菌群落相似性在45日龄时显著增加(P<0.05)，而各日龄组内直肠真菌群落相似性在60日龄后显著增加(P<0.05)。随年龄变化的属，Acremonium, Microascus, Valsonectria, Myrmecridium, Scopulariopsis, Myrothecium, Saccharomyces 和 Stephanonectria在瘤胃和直肠中均随羔羊年龄变化而改变，说明这些真菌可能在羔羊生长发育过程中起到关键性作用，并且说明上消化道的微生物可能会对下消化道的微生物区系产生影响。主坐标分析结果表示，瘤胃和直肠真菌群落存在显著差异(P<0.05)。本研究表明，真菌群落在胃肠道演替过程可以分为三个阶段：定植阶段（0-10日龄），过渡阶段（10-45日龄），和相对稳定的逐渐成熟阶段（45-120日龄）。本实验结果表明，羔羊的年龄和胃肠道的不同部位均会影响真菌群落组成，为真菌在羔羊早期生长发育过程的调控奠定理论基础。本研究较全面的比较分析了120日龄之前，湖羊羔羊胃肠道真菌建立过程和此过程中逐步行使主导作用的优势菌群，分析发现了不同日龄阶段胃肠道真菌结构的特征。
Abstract
Although fungal communities in the gastrointestinal tract have a significant role in animal health and performance, their dynamics within the tract are not well known. Thus, this study investigated fungal community dynamics in the rumen and rectum of lambs from birth to 4 mon of age by using IT1S rDNA sequencing technology together with the RandomForest approach to determine age-related changes in the fungal ecology. The results indicated that gastrointestinal fungal community composition, diversity, and abundance altered (P<0.05) with the increasing age of the lambs. Two phyla, Ascomycota and Basidiomycota, dominated the samples. Similarity within age groups of the rumen fungi increased sharply after 45 days of age, while the similarity increased (P<0.05) significantly after 60 days of age in the rectum. The age-related genera, Acremonium, Microascus, Valsonectria, Myrmecridium, Scopulariopsis, Myrothecium, Saccharomyces, and Stephanonectria, were presented in both ruminal and rectal communities, and their changes in relative abundance were consistent at both sites. The principal coordinates analysis showed significant differences (P<0.05) between the fungal communities in the rumen and rectum. Our findings demonstrate that both the age of lambs and the gastrointestinal tract region can affect the composition of these fungal communities, and this provides new insight and directions for future studies in this research area.
|
|
Received: 28 June 2021
Accepted: 09 December 2021
|
| Fund: This work was supported by the China Agriculture Research System of MARA and MOF (CARS-38), the National Key R&D Program of China (2018YFD0502100), the Precision Animal Husbandry Discipline Group Construction Project of Hebei Agricultural University, China (1090064), and the Scientific Research Foundation of Hebei Agricultural University, China (YJ201825). |
| About author: YIN Xue-jiao, E-mail: bdyinxuejiao@foxmail.com; Correspondence ZHANG Ying-jie, Tel: +86-312-7528366, E-mail: zhangyingjie66@126.com; LIU Yue-qin, Tel: +86-312-7528886, E-mail: liuyueqin66@126.com |
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.
2022.
Dynamic change of fungal community in the gastrointestinal tract of growing lambs. Journal of Integrative Agriculture, 21(11): 3314-3328.
|
Abecia L, Martinez-Fernandez G, Waddams K, Martin-Garcia A I, Pinloche E, Creevey C J, Denman S E, Newbold C J, Yanez-Ruiz D R. 2018. Analysis of the rumen microbiome and metabolome to study the effect of an antimethanogenic treatment applied in early life of kid goats. Frontiers in Microbiology, 9, 2227.
Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, Khan M T, Zhang J, Li J, Xiao L, Al-Aama J, Zhang D, Lee Y S, Kotowska D, Colding C, Tremaroli V, Yin Y, Bergman S, Xu X, Madsen L, Kristiansen K, Dahlgren J, Wang J. 2015. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host & Microbe, 17, 690–703.
Belanche A, Yáñez-Ruiz D R, Detheridge A P, Griffith G W, Kingston-Smith A H, Newbold C J. 2019. Maternal versus artificial rearing shapes the rumen microbiome having minor long-term physiological implications. Environmental Microbiology, 21, 4360–4377.
Bi Y, Tu Y, Zhang N, Wang S, Zhang F, Suen G, Shao D, Li S, Diao Q. 2021. Multiomics analysis reveals the presence of a microbiome in the gut of fetal lambs. Gut, 70, 853–864.
Breiman L. 2001. Random Forests. Machine Learning, 45, 5–32.
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.
Chen D, Yan J, Shen W, Song Y, Lan X, Yi K, Muhammad A U R. 2020. Effect of inclusion of HMBi in the ration of goats on feed intake, nutrient digestibility, rumen bacteria community and blood serum parameters. Journal of Animal Physiology and Animal Nutrition, 104, 987–997.
Chung H, Pamp S J, Hill J A, Surana N K, Edelman S M, Troy E B, Reading N C, Villablanca E J, Wang S, Mora J R, Umesaki Y, Mathis D, Benoist C, Relman D A, Kasper D L. 2012. Gut immune maturation depends on colonization with a host-specific microbiota. Cell, 149, 1578–1593.
Clemente J C, Ursell L K, Parfrey L W, Knight R. 2012. The impact of the gut microbiota on human health: an integrative view. Cell, 148, 1258–1270.
De Mulder T, Vandaele L, Peiren N, Haegeman A, Ruttink T, De Campeneere S, Van De Wiele T, Goossens K. 2018. Cow responses and evolution of the rumen bacterial and methanogen community following a complete rumen content transfer. The Journal of Agricultural Science, 156, 1047–1058.
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.
Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder M J, Valles-Colomer M, Vandeputte D, Tito R Y, Chaffron S, Rymenans L, Verspecht C, De Sutter L, Lima-Mendez G, D’hoe K, Jonckheere K, Homola D, Garcia R, Tigchelaar E F, Eeckhaudt L, Fu J, Henckaerts L, Zhernakova A, Wijmenga C, Raes J. 2016. Population-level analysis of gut microbiome variation. Science, 352, 560–564.
Favier C F, Vaughan E E, De Vos W M, Akkermans A D. 2002. Molecular monitoring of succession of bacterial communities in human neonates. Applied and Environmental Microbiology, 68, 219–226.
Gruninger R J, Puniya A K, Callaghan T M, Edwards J E, Youssef N, Dagar S S, Fliegerova K, Griffith G W, Forster R, Tsang A, McAllister T, Elshahed M S. 2014. Anaerobic fungi (phylum Neocallimastigomycota): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential. FEMS Microbiology Ecology, 90, 1–17.
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. Microbiologyopen, 9, e1119.
Guzman C E, Bereza-Malcolm L T, De Groef B, Franks A E. 2015. Presence of selected methanogens, fibrolytic bacteria, and proteobacteria in the gastrointestinal tract of neonatal dairy calves from birth to 72 hours. PLoS One, 10, e0133048.
Holmes E, Li J V, Marchesi J R, Nicholson J K. 2012. Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metabolism, 16, 559–564.
Huang S, Ji S, Yan H, Hao Y, Zhang J, Wang Y, Cao Z, Li S. 2020. The day-to-day stability of the ruminal and fecal microbiota in lactating dairy cows. Microbiologyopen, 9, e990.
Huseyin C E, O’Toole P W, Cotter P D, Scanlan P D. 2017. Forgotten fungi - the gut mycobiome in human health and disease. FEMS Microbiology Reviews, 41, 479–511.
Jami E, Israel A, Kotser A, Mizrahi I. 2013. Exploring the bovine rumen bacterial community from birth to adulthood. The ISME Journal, 7, 1069–1079.
Ji S, Jiang T, Yan H, Guo C, Liu J, Su H, Alugongo G M, Shi H, Wang Y, Cao Z, Li S. 2018. Ecological restoration of antibiotic-disturbed gastrointestinal microbiota in foregut and hindgut of cows. Frontiers in Cellular and Infection Microbiology, 8, 79.
Klein-Jöbstl D, Schornsteiner E, Mann E, Wagner M, Drillich M, Schmitz-Esser S. 2014. Pyrosequencing reveals diverse fecal microbiota in Simmental calves during early development. Frontiers in Microbiology, 5, 622.
Kumar S, Indugu N, Vecchiarelli B, Pitta D W. 2015. Associative patterns among anaerobic fungi, methanogenic archaea, and bacterial communities in response to changes in diet and age in the rumen of dairy cows. Frontiers in Microbiology, 6, 781.
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.
Langda S, Zhang C, Zhang K, Gui B, Ji D, Deji C, Cuoji A, Wang X, Wu Y. 2020. Diversity and composition of rumen bacteria, fungi, and protozoa in goats and sheep living in the same high-altitude pasture. Animals, 10, 186.
Lee S M, Donaldson G P, Mikulski Z, Boyajian S, Ley K, Mazmanian S K. 2013. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature, 501, 426–429.
Li B, Zhang K, Li C, Wang X, Chen Y, Yang Y. 2019. Characterization and comparison of microbiota in the gastrointestinal tracts of the goat (Capra hircus) during preweaning development. Frontiers in Microbiology, 10, 2125.
Li J, Chen D, Yu B, He J, Zheng P, Mao X, Yu J, Luo J, Tian G, Huang Z, Luo Y. 2018. Fungi in gastrointestinal tracts of human and mice: from community to functions. Microbial Ecology, 75, 821–829.
Liaw A, Wiener M. 2002. Classification and Regression by randomForest. 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.
McCann J C, Wickersham T A, Loor J J. 2014. High-throughput methods redefine the rumen microbiome and its relationship with nutrition and metabolism. Bioinformatics and Biology Insights, 8, 109–125.
Newbold C J, Ramos-Morales E. 2020. Review: Ruminal microbiome and microbial metabolome: effects of diet and ruminant host. Animal, 14, s78–s86.
NY/T 816–2004. 2004. Feeding standard of meat-producing sheep and goats. Ministry of Agriculture of China. (in Chinese)
Parker A, Lawson M A E, Vaux L, Pin C. 2018. Host-microbe interaction in the gastrointestinal tract. Environmental Microbiology, 20, 2337–2353.
Peng X, Wilken S E, Lankiewicz T S, Gilmore S P, Brown J L, Henske J K, Swift C L, Salamov A, Barry K, Grigoriev I V, Theodorou M K, Valentine D L, O’Malley M A. 2021. Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes. Nature Microbiology, 6, 499–511.
Quercia S, Freccero F, Castagnetti C, Soverini M, Turroni S, Biagi E, Rampelli S, Lanci A, Mariella J, Chinellato E, Brigidi P, Candela M. 2019. Early colonisation and temporal dynamics of the gut microbial ecosystem in standardbred foals. Equine Veterinary Journal, 51, 231–237.
Schei K, Avershina E, Øien T, Rudi K, Follestad T, Salamati S, Ødegård R A. 2017. Early gut mycobiota and mother-offspring transfer. Microbiome, 5, 107.
Solomon K V, Haitjema C H, Henske J K, Gilmore S P, Borges-Rivera D, Lipzen A, Brewer H M, Purvine S O, Wright A T, Theodorou M K, Grigoriev I V, Regev A, Thompson D A, O’Malley M A. 2016. Early-branching gut fungi possess a large, comprehensive array of biomass-degrading enzymes. Science, 351, 1192–1195.
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 W A Jr, Ahmed T, Gordon J I. 2014. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature, 510, 417–421.
Tremaroli V, Bäckhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature, 489, 242–249.
Wheeler M L, Limon J J, Underhill D M. 2017. Immunity to commensal fungi: Detente and disease. Annual Review of Pathology, 12, 359–385.
Yáñez-Ruiz D R, Abecia L, Newbold C J. 2015. Manipulating rumen microbiome and fermentation through interventions during early life: a review. Frontiers in Microbiology, 6, 1133.
Yeoman C J, Ishaq S L, Bichi E, Olivo S K, Lowe J, Aldridge B M. 2018. Biogeographical differences in the influence of maternal microbial sources on the early successional development of the bovine neonatal gastrointestinal tract. Scientific Reports, 8, 3197.
Yeoman C J, White B A. 2014. Gastrointestinal tract microbiota and probiotics in production animals. Annual Review of Animal Biosciences, 2, 469–486.
Zhang J, Zhang N, Liu Y X, Zhang X, Hu B, Qin Y, Xu H, Wang H, Guo X, Qian J, Wang W, Zhang P, Jin T, Chu C, Bai Y. 2018. Root microbiota shift in rice correlates with resident time in the field and developmental stage. Science China (Life Sciences), 61, 613–621.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
