江山乌猪肠道黏膜菌群组成及其功能的性别差异
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浙江农林大学科研发展基金(2023LFR006);动物分子营养学教育部重点实验室(浙江大学)开放性课题(KLMAN202307)


Differences of the composition and functions of intestinal mucosal microbiota between male and female Jiangshan Black pigs
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    摘要:

    肠道黏膜微生物在调控宿主生理功能方面发挥重要作用,其结构组成受到多种因素影响。性别被认为是塑造肠道微生物的因素之一。然而,性别对肠道黏膜菌群的差异影响还不清楚。目的以江山乌猪为研究对象,探究性别差异对其肠道黏膜微生物组成及功能的影响。方法选取性成熟的雌性和雄性江山乌猪各8头,利用16S rRNA基因高通量测序技术分析回肠和结肠黏膜菌群。结果在回肠黏膜中,雄性江山乌猪菌群的Chao1指数和Shannon指数显著高于雌性(P<0.05),在结肠黏膜中,不同性别江山乌猪菌群Chao1指数和Shannon指数无显著差异(P>0.05)。菌群差异分析显示,回肠黏膜中,沙雷氏菌属(Serratia)和埃希氏志贺菌属(Escherichia_Shigella)在雌性组中的相对丰度显著高于雄性组(P<0.05),雄性组中Oscillospiraceae UCG-005、拟普雷沃氏菌属(Alloprevotella)、布劳特氏菌属(Blautia)和Prevotellaceae_NK3B31_group相对丰度显著高于雌性组(P<0.05);结肠黏膜中,雌性组中unclassified_MuribaculaceaeRikenellaceae_RC9_gut_group和Prevotellaceae UCG-003相对丰度显著高于雄性组(P<0.05),Oscillospiraceae UCG-005、Lachnospiraceae_NK4A136_group和unclassified_Lachnospiraceae在雄性组中相对丰度更高(P<0.05)。功能预测发现,雄性乌猪回肠黏膜菌群显著富集了氨基酸代谢、碳水化合物代谢和能量代谢等功能途径(P<0.05);结肠黏膜菌群主要富集了膜转运相关的ABC转运蛋白和信号转导相关的双组分系统等功能途径(P<0.05)。结论不同性别江山乌猪肠黏膜菌群结构及功能具有明显差异。这些结果揭示了不同性别江山乌猪肠道黏膜菌群的差异特征,为了解和挖掘我国地方畜禽品种肠道微生物资源提供部分参考。

    Abstract:

    The intestinal mucosal microbiota plays an important role in regulating the physiological functions of the host, and its structure and composition are modulated by multiple factors. The host sex is regarded as a key factor shaping the gut microbiota. However, the effects of different sexes on intestinal mucosal microbiota remain unclear. [Objective] To investigate the differences of the composition and functions of the intestinal mucosal microbiota between male and female Jiangshan Black pigs. [Methods] This study analyzed the ileal and colonic mucosal microbiota of eight sexually mature female and eight male Jiangshan Black pigs by 16S rRNA gene high-throughput sequencing. [Results] The Chao1 index and Shannon index of the ileal mucosal microbiota in male pigs were higher than that in female pigs (P<0.05). However, the two indexes of the colonic mucosal microbiota had no significant differences between the male and female pigs (P>0.05). The ileal mucosa of female pigs had higher relative abundance of Serratia and Escherichia_Shigella and lower relative abundance of Oscillospiraceae UCG-005, Alloprevotella, Blautia and Prevotellaceae_NK3B31_group than that of male pigs (P<0.05). The colonic mucosa of female pigs had higher relative abundance of unclassified_Muribaculaceae, Rikenellaceae_RC9_gut_group, and Prevotellaceae UCG-003 and lower relative abundance of Oscillospiraceae UCG-005, Lachnospiraceae_NK4A136_group, and unclassified_Lachnospiraceae than that of male pigs (P<0.05). Functional prediction results showed that the intestinal mucosal microbiota of male Jiangshan Black pigs was mainly enriched with functional pathways such as amino acid metabolism, carbohydrate metabolism, and energy metabolism (P<0.05), while the colonic mucosal microbiota was mainly enriched with functional pathways such as ABC transporters and two-component signal transduction systems (P<0.05). [Conclusion] The structure and function of intestinal mucosal microbiota were different between male and female Jiangshan Black pigs. The results provide references for understanding and excavating the intestinal microbial resources of local breeds of domesticated animals in China.

    参考文献
    [1] ADAK A, KHAN MR. An insight into gut microbiota and its functionalities[J]. Cellular and Molecular Life Sciences, 2019, 76(3): 473-493.
    [2] WANG JW, QIN CF, HE T, QIU K, SUN WJ, ZHANG X, JIAO N, ZHU WY, YIN JD. Alfalfa-containing diets alter luminal microbiota structure and short chain fatty acid sensing in the caecal mucosa of pigs[J]. Journal of Animal Science and Biotechnology, 2018, 9: 11.
    [3] BISANZ JE, UPADHYAY V, TURNBAUGH JA, LY K, TURNBAUGH PJ. Meta-analysis reveals reproducible gut microbiome alterations in response to a high-fat diet[J]. Cell Host & Microbe, 2019, 26(2): 265-272.e4.
    [4] IANIRO G, TILG H, GASBARRINI A. Antibiotics as deep modulators of gut microbiota: between good and evil[J]. Gut, 2016, 65(11): 1906-1915.
    [5] KOVACS A, BEN-JACOB N, TAYEM H, HALPERIN E, IRAQI FA, GOPHNA U. Genotype is a stronger determinant than sex of the mouse gut microbiota[J]. Microbial Ecology, 2011, 61(2): 423-428.
    [6] VALERI F, ENDRES K. How biological sex of the host shapes its gut microbiota[J]. Frontiers in Neuroendocrinology, 2021, 61: 100912.
    [7] YOON K, KIM N. Roles of sex hormones and gender in the gut microbiota[J]. Journal of Neurogastroenterology and Motility, 2021, 27(3): 314-325.
    [8] SINHA T, VICH VILA A, GARMAEVA S, JANKIPERSADSING SA, IMHANN F, COLLIJ V, BONDER MJ, JIANG XF, GURRY T, ALM EJ, D'AMATO M, WEERSMA RK, SCHERJON S, WIJMENGA C, FU JY, KURILSHIKOV A, ZHERNAKOVA A. Analysis of 1135 gut metagenomes identifies sex-specific resistome profiles[J]. Gut Microbes, 2019, 10(3): 358-366.
    [9] ELDERMAN M, HUGENHOLTZ F, BELZER C, BOEKSCHOTEN M, van BEEK A, de HAAN B, SAVELKOUL H, de VOS P, FAAS M. Sex and strain dependent differences in mucosal immunology and microbiota composition in mice[J]. Biology of Sex Differences, 2018, 9(1): 26.
    [10] HE MZ, GAO J, WU JY, ZHOU YY, FU H, KE SL, YANG H, CHEN CY, HUANG LS. Host gender and androgen levels regulate gut bacterial taxa in pigs leading to sex-biased serum metabolite profiles[J]. Frontiers in Microbiology, 2019, 10: 1359.
    [11] MAFFEI S, FORINI F, CANALE P, NICOLINI G, GUIDUCCI L. Gut microbiota and sex hormones: crosstalking players in cardiometabolic and cardiovascular disease[J]. International Journal of Molecular Sciences, 2022, 23(13): 7154.
    [12] SANTOS-MARCOS JA, HARO C, VEGA-ROJAS A, ALCALA-DIAZ JF, MOLINA-ABRIL H, LEON-ACUÑA A, LOPEZ-MORENO J, LANDA BB, TENA-SEMPERE M, PEREZ-MARTINEZ P, LOPEZ-MIRANDA J, PEREZ-JIMENEZ F, CAMARGO A. Sex differences in the gut microbiota as potential determinants of gender predisposition to disease[J]. Molecular Nutrition & Food Research, 2019, 63(7): e1800870.
    [13] DONALDSON GP, LEE SM, MAZMANIAN SK. Gut biogeography of the bacterial microbiota[J]. Nature Reviews Microbiology, 2016, 14: 20-32.
    [14] ADHIKARI B, KIM SW, KWON YM. Characterization of microbiota associated with digesta and mucosa in different regions of gastrointestinal tract of nursery pigs[J]. International Journal of Molecular Sciences, 2019, 20(7): 1630.
    [15] AWAD WA, MANN E, DZIECIOL M, HESS C, SCHMITZ-ESSER S, WAGNER M, HESS M. Age-related differences in the luminal and mucosa-associated gut microbiome of broiler chickens and shifts associated with Campylobacter jejuni infection[J]. Frontiers in Cellular and Infection Microbiology, 2016, 6: 154.
    [16] 杨宇翔. 消化道微生物对猪和大鼠氨基酸代谢的影响[D]. 南京: 南京农业大学博士学位论文, 2016. YANG YX. Influence of gastrointestinal microbiota on amino acids metabolism in swine and rat[D]. Nanjing: Doctoral Dissertation of Nanjing Agricultural University, 2016(in Chinese).
    [17] ARIKE L, SEIMAN A, van der POST S, RODRIGUEZ PIÑEIRO AM, ERMUND A, SCHÜTTE A, BÄCKHED F, JOHANSSON MEV, HANSSON GC. Protein turnover in epithelial cells and mucus along the gastrointestinal tract is coordinated by the spatial location and microbiota[J]. Cell Reports, 2020, 30(4): 1077-1087.e3.
    [18] SCHROEDER BO, BIRCHENOUGH GMH, PRADHAN M, NYSTRÖM EEL, HENRICSSON M, HANSSON GC, BÄCKHED F. Obesity-associated microbiota contributes to mucus layer defects in genetically obese mice[J]. Journal of Biological Chemistry, 2020, 295(46): 15712-15726.
    [19] PICKARD JM, ZENG MY, CARUSO R, NÚÑEZ G. Gut microbiota: role in pathogen colonization, immune responses, and inflammatory disease[J]. Immunological Reviews, 2017, 279(1): 70-89.
    [20] CALLAHAN BJ, McMURDIE PJ, ROSEN MJ, HAN AW, JOHNSON AJA, HOLMES SP. DADA2: high-resolution sample inference from Illumina amplicon data[J]. Nature Methods, 2016, 13: 581-583.
    [21] AMATO KR, YEOMAN CJ, KENT A, RIGHINI N, CARBONERO F, ESTRADA A, GASKINS HR, STUMPF RM, YILDIRIM S, TORRALBA M, GILLIS M, WILSON BA, NELSON KE, WHITE BA, LEIGH SR. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes[J]. The ISME Journal, 2013, 7(7): 1344-1353.
    [22] MERGA Y, CAMPBELL BJ, RHODES JM. Mucosal barrier, bacteria and inflammatory bowel disease: possibilities for therapy[J]. Digestive Diseases, 2014, 32(4): 475-483.
    [23] KOLIADA A, MOSEIKO V, ROMANENKO M, LUSHCHAK O, KRYZHANOVSKA N, GURYANOV V, VAISERMAN A. Sex differences in the phylum-level human gut microbiota composition[J]. BMC Microbiology, 2021, 21(1): 131.
    [24] 杨雄威. 华南野猪(Sus scrofa chirodontus)的食性和肠道微生物多样性初步研究[D]. 贵阳: 贵州大学硕士学位论文, 2021. YANG XW. A preliminary study on feeding habits and intestinal microbial diversity of sus scrofa chirodontus in Guizhou Province, china[D]. Guiyang: Master's Thesis of Guizhou University, 2021(in Chinese).
    [25] HARADA N, HANAOKA R, HANADA K, IZAWA T, INUI H, YAMAJI R. Hypogonadism alters cecal and fecal microbiota in male mice[J]. Gut Microbes, 2016, 7(6): 533-539.
    [26] PETRY AL, PATIENCE JF, KOESTER LR, HUNTLEY NF, BEDFORD MR, SCHMITZ-ESSER S. Xylanase modulates the microbiota of ileal mucosa and digesta of pigs fed corn-based arabinoxylans likely through both a stimbiotic and prebiotic mechanism[J]. PLoS One, 2021, 16(1): e0246144.
    [27] LI WX, ZHANG YP, MAO W, WANG CS, YIN SX. Functional potential differences between Firmicutes and Proteobacteria in response to manure amendment in a reclaimed soil[J]. Canadian Journal of Microbiology, 2020, 66(12): 689-697.
    [28] TANES C, BITTINGER K, GAO Y, FRIEDMAN ES, NESSEL L, PALADHI UR, CHAU L, PANFEN E, FISCHBACH MA, BRAUN J, XAVIER RJ, CLISH CB, LI HZ, BUSHMAN FD, LEWIS JD, WU GD. Role of dietary fiber in the recovery of the human gut microbiome and its metabolome[J]. Cell Host & Microbe, 2021, 29(3): 394-407.e5.
    [29] KAUR A, CHEN TT, GREEN SJ, MUTLU E, MARTIN BR, RUMPAGAPORN P, PATTERSON JA, KESHAVARZIAN A, HAMAKER BR. Physical inaccessibility of a resistant starch shifts mouse gut microbiota to butyrogenic Firmicutes[J]. Molecular Nutrition & Food Research, 2019, 63(7): e1801012.
    [30] KONIKOFF T, GOPHNA U. Oscillospira: a central, enigmatic component of the human gut microbiota[J]. Trends in Microbiology, 2016, 24(7): 523-524.
    [31] HOSOMI K, SAITO M, PARK J, MURAKAMI H, SHIBATA N, ANDO M, NAGATAKE T, KONISHI K, OHNO H, TANISAWA K, MOHSEN A, CHEN YA, KAWASHIMA H, NATSUME-KITATANI Y, OKA Y, SHIMIZU H, FURUTA M, TOJIMA Y, SAWANE K, SAIKA A, et al. Oral administration of Blautia wexlerae ameliorates obesity and type 2 diabetes via metabolic remodeling of the gut microbiota[J]. Nature Communications, 2022, 13: 4477.
    [32] BIDDLE A, STEWART L, BLANCHARD J, LESCHINE S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities[J]. Diversity, 2013, 5(3): 627-640.
    [33] LI SS, GUO JD, LIU RM, ZHANG FZ, WEN SA, LIU Y, REN WC, ZHANG XX, SHANG YY, GAO MQ, LU J, PANG Y. Predominance of Escherichia-Shigella in gut microbiome and its potential correlation with elevated level of plasma tumor necrosis factor alpha in patients with tuberculous meningitis[J]. Microbiology Spectrum, 2022, 10(6): e0192622.
    [34] 郭仕辉, 余永涛, 万佳宏, 毛彦妮, 张浩东, 张津慎, 田新岳, 赵清梅. 变形菌门与哺乳动物结肠肠道菌群失调相关研究进展[J]. 中国微生态学杂志, 2022, 34(4): 479-484. GUO SH, YU YT, WAN JH, MAO YN, ZHANG HD, ZHANG JS, TIAN XY, ZHAO QM. Progress in research on the relationship between Proteobacteria and the imbalance of mammalian colonic intestinal flora[J]. Chinese Journal of Microecology, 2022, 34(4): 479-484(in Chinese).
    [35] ZHANG CG, LIU HF, SUN L, WANG Y, CHEN XD, DU J, SJÖLING Å, YAO JH, WU SR. An overview of host-derived molecules that interact with gut microbiota[J]. iMeta, 2023, 2(2): e88.
    [36] 石宝明, 鲍嘉欣, 赵轩. 中国地方猪种肠道微生物功能发掘与利用的研究进展[J]. 动物营养学报, 2022, 34(10): 6281-6290. SHI BM, BAO JX, ZHAO X. Research progress on exploitation and utilization of intestinal microbial function in Chinese native pigs[J]. Chinese Journal of Animal Nutrition, 2022, 34(10): 6281-6290(in Chinese).
    [37] GAO H, BAI L, JIANG YM, HUANG W, WANG LL, LI SG, ZHU GD, WANG DQ, HUANG ZH, LI XS, CAO J, JIANG LB, JACOBS-LORENA M, ZHAN S, WANG SB. A natural symbiotic bacterium drives mosquito refractoriness to Plasmodium infection via secretion of an antimalarial lipase[J]. Nature Microbiology, 2021, 6: 806-817.
    [38] APPLE JK, MAXWELL CV, BROWN DC, FRIESEN KG, MUSSER RE, JOHNSON ZB, ARMSTRONG TA. Effects of dietary lysine and energy density on performance and carcass characteristics of finishing pigs fed ractopamine[J]. Journal of Animal Science, 2004, 82(11): 3277-3287.
    [39] GAO J, XU K, LIU HN, LIU G, BAI MM, PENG C, LI TJ, YIN YL. Impact of the gut microbiota on intestinal immunity mediated by tryptophan metabolism[J]. Frontiers in Cellular and Infection Microbiology, 2018, 8: 13.
    [40] BEIS K. Structural basis for the mechanism of ABC transporters[J]. Biochemical Society Transactions, 2015, 43(5): 889-893.
    [41] PASQUA M, COLUCCIA M, EGUCHI Y, OKAJIMA T, GROSSI M, PROSSEDA G, UTSUMI R, COLONNA B. Roles of two-component signal transduction systems in Shigella virulence[J]. Biomolecules, 2022, 12(9): 1321.
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吴娴,毕海洋,武永淑,李向臣,张亚南. 江山乌猪肠道黏膜菌群组成及其功能的性别差异[J]. 微生物学报, 2024, 64(4): 1249-1262

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  • 收稿日期:2023-11-06
  • 最后修改日期:2024-01-10
  • 录用日期:2024-01-10
  • 在线发布日期: 2024-03-30
  • 出版日期: 2024-04-04
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