肠道寄生虫与肠道微生物相互作用研究进展

doi:10.16431/j.cnki.1671-7236.2024.01.033

摘要/Abstract

摘要： 在脊椎动物的肠道内，存在着数量庞大、结构多样、动态变化的微生物群，它们对肠道的生理、代谢、免疫等具有重要的作用。在自然条件下，这些微生物和真核生物（如蠕虫、原生动物、真菌等）共同存在于脊椎动物肠道内。寄生虫与微生物群均可显著改变机体肠道生理与免疫环境，为它们之间的相互作用创造了机会。肠道微生物与寄生虫之间的相互作用会极大地影响感染的结果，进而对宿主的健康产生重要影响。如寄生虫感染会影响宿主与微生物的相互作用关系，从而促使或保护宿主免受细菌的侵害。另一方面，菌群又会影响寄生虫的定植、繁殖和毒性，使其沿着与宿主寄生性-互惠共生性的生存模式发展。这些相互作用的机理与结果是微生物学与寄生虫学之间交叉研究的前沿课题。笔者对近年来有关肠道寄生虫与肠道微生物间相互作用的最新研究成果进行了总结，并对其可能未考虑到的因素提出了自己的观点，旨在为肠道寄生虫病防控及肠道菌群研究提供参考。

关键词: 肠道寄生虫; 肠道微生物; 相互作用

Abstract: In the intestines of vertebrates, there are a large number of structurally diverse and dynamically changing microbiota, which play important roles in the physiology, metabolism, and immunity of the intestine.Under natural conditions, these microorganisms and eukaryotes (such as worms, protozoa, fungi, etc) co-exist in the vertebrate intestine.Both parasites and microbiota can significantly alter the intestinal physiology and immune environment, creating opportunities for interaction between them.The interaction between gut microbes and parasites can greatly affect the outcome of infection, which in turn has important implications for host health.For example, parasitic infections affect host-microbial interactions to promote or protect the host from bacteria.On the other hand, the flora affects the colonization, reproduction and toxicity of the parasite, causing it to develop along the survival pattern of parasitic-reciprocal symbiosis with the host.The mechanism and results of these interactions are frontier topics in the cross-research between microbiology and parasitology.This article summarizes the latest research results on the interaction between intestinal parasites and intestinal microbiota in recent years, and puts forward its own views on factors that may not be taken into account, aiming to provide reference for the prevention and control of intestinal parasitic diseases and the study of intestinal microbiota.

Key words: intestinal parasites; intestinal microorganisms; interaction

中图分类号:

S852.7

李思瑶, 侯斌, 玛丽雅其其格, 哈斯苏荣. 肠道寄生虫与肠道微生物相互作用研究进展[J]. 中国畜牧兽医, 2024, 51(1): 330-337.

LI Siyao, HOU Bin, MALI Yaqiqige, HASI Surong. Research Progress on the Interaction Between Intestinal Parasites and Intestinal Microorganisms[J]. China Animal Husbandry and Veterinary Medicine, 2024, 51(1): 330-337.

参考文献

[1] GRAHAM A L, SCHROM E C 2 ND, METCALF C J E.The evolution of powerful yet perilous immune systems[J].Trends in Immunology, 2022, 43(2):117-131.
[2] ACHARYA S, DA'DARA A A, SKELLY P J.Schistosome immunomodulators[J].PLoS Pathogens, 2021, 17(12):e1010064.
[3] CARUSO R, LO B C, NUNEZ G.Host-microbiota interactions in inflammatory bowel disease[J].Nature Reviews.Immunology, 2020, 20(7):411-426.
[4] XUE J, AJUWON K M, FANG R.Mechanistic insight into the gut microbiome and its interaction with host immunity and inflammation[J].Animal Nutrition, 2020, 6(4):421-428.
[5] ZHENG D, LIWINSKI T, ELINAV E.Interaction between microbiota and immunity in health and disease[J].Cell Research, 2020, 30(6):492-506.
[6] FULHAM M, POWER M, GRAY R.Gut microbiota of endangered Australian sea lion pups is unchanged by topical ivermectin treatment for endemic hookworm infection[J].Frontiers in Microbiology, 2022, 13:1048013.
[7] 吴海丽.不同季节圈养岩羊肠道微生物的多样性分析[J].中国动物传染病学报, 2020, 28(4):71-78. WU H L.Analysis of the diversity of intestinal microorganisms in captive rock sheep in different seasons[J].Chinese Journal of Animal Infectious Diseases, 2020, 28(4):71-78.(in Chinese)
[8] SIAGIAN E F.Intestinal microflora vs protozoan parasites:From interaction to competition[J].South Asian Journal of Research in Microbiology, 2022, 13(1):36-46.
[9] GUSTAFASSON J K, JOHANSSON M E V.The role of goblet cells and mucus in intestinal homeostasis[J].Nature Reviews.Gastroenterology & Hepatology, 2022, 19(12):785-803.
[10] RODRIGUES V F, BAHIA M P S, CANDIDO N R et al.Acute infection with Strongyloides venezuelensis increases intestine production IL-10, reduces Th1/Th2/Th17 induction in colon and attenuates dextran sulfate sodium-induced colitis in BALB/c mice[J].Cytokine, 2018, 111:72-83.
[11] TAILFORD L E, CROST E H, KAVANAUGH D, et al.Mucin glycan foraging in the human gut microbiome[J].Frontiers in Genetics, 2015, 6:81.
[12] HASNAIN S Z, MCGUCKIN M A, GRENCIS R K, et al.Serine protease(s) secreted by the nematode Trichuris muris degrade the mucus barrier[J]. PLoS Neglected Tropical Diseases, 2012, 6(10):e1856.
[13] LEVKUT M, LEVKUTOVÁ M, GREŠÁKOVÁ L', et al.Production of intestinal mucins, sIgA, and metallothionein after administration of zinc and infection of Ascaridia galli in chickens:Preliminary data[J]. Life (Basel, Switzerland), 2022, 13(1):67.
[14] TSUBOKAWA D, ISHIWATA K, GOSO Y, et al.Interleukin-13/interleukin-4 receptor pathway is crucial for production of Sd^a-sialomucin in mouse small intestinal mucosa by Nippostrongylus brasiliensis infection[J]. Parasitology International, 2017, 66(6):731-734.
[15] OSAKUNOR D N M, MUNK P, MDULUZA T, et al.The gut microbiome but not the resistome is associated with urogenital schistosomiasis in preschool-aged children[J].Communications Biology, 2020, 3(1):155.
[16] RAMANAN D, BOWCUTT R, LEE S C, et al.Helminth infection promotes colonization resistance via type 2 immunity[J].Science (New York, N.Y.), 2016, 352(6285):608-612.
[17] JIN X, LIU Y, WANG J, et al.β-glucan-triggered Akkermansia muciniphila expansion facilitates the expulsion of intestinal helminth via TLR2 in mice[J].Carbohydrate Polymers, 2022, 275:118719.
[18] BSKA P, NORBURY L J.The role of the intestinal epithelium in the "Weep and Sweep" response during gastro-intestinal helminth infections[J].Animals, 2022, 12(2):175.
[19] SARDINHA-SILVA A, ALVES-FERREIRA E V C, GRIGG M E.Intestinal immune responses to commensal and pathogenic protozoa[J].Frontiers in Immunology, 2022, 13:963723.
[20] BROADHURST M J, LEUNG J M, KASHYAP V, et al.IL-22⁺ CD4⁺ T cells are associated with therapeutic Trichuris trichiura infection in an ulcerative colitis patient[J]. Science Translational Medicine, 2010, 2(60):60ra88.
[21] ZHANG W, ZHOU Q, LIU H, et al. Bacteroides fragilis strain ZY-312 facilitates colonic mucosa regeneration in colitis via motivating STAT3 signaling pathway induced by IL-22 from ILC3 secretion[J]. Frontiers in Immunology, 2023, 14:1156762.
[22] FEI Y, LI S, WANG Z, et al.IRW (Ile-Arg-Trp) alleviates DSS-induced intestinal injury by remodeling gut microbiota and regulating fecal SCFA levels[J]. Nutrients, 2023, 15(4):953.
[23] ADALID R, FELIU C, SOMOANO A, et al.Ecological analysis of the helminth community of Microtus lusitanicus (Gerbe, 1879) (Rodentia) in Asturias (NW Spain)[J].Animals, 2021, 11(11):3055.
[24] CLEENEWERK L, GARSSEN J, HOGENKAMP A.Clinical use of Schistosoma mansoni antigens as novel immunotherapies for autoimmune disorders[J].Frontiers in Immunology, 2020, 11:1821.
[25] BHOJ P, TOGRE N, KHATRI V, et al.Harnessing immune evasion strategy of lymphatic filariae:A therapeutic approach against inflammatory and infective pathology[J].Vaccines, 2022, 10(8):1235.
[26] WOJTKOWIAK-GIERA A, DERDA M, WANDURSKA-NOWAK E, et al.Changes in the expression of TLR2 during the intestinal phase of trichinellosis[J].Journal of Veterinary Research, 2020, 64(2):269-274.
[27] LI Y, LIU W, GUAN X, et al.STAT6 and furin are successive triggers for the production of TGF-β by T cells[J].Journal of Immunology, 2018, 201(9):2612-2623.
[28] LI Y, GUAN X, LIU W, et al.Helminth-induced production of TGF-β and suppression of graft-versus-host disease is dependent on IL-4 production by host cells[J].Journal of Immunology (Baltimore, Md.:1950), 2018, 201(10):2910-2922.
[29] ATAGOZLI T, ELLIOTT D E, INCE M N.Helminth lessons in inflammatory bowel diseases (IBD)[J].Biomedicines, 2023, 11(4):1200.
[30] FRICKE W F, SONG Y, WANG A J, et al.Type 2 immunity-dependent reduction of segmented filamentous bacteria in mice infected with the helminthic parasite Nippostrongylus brasiliensis[J]. Microbiome, 2015, 3:40.
[31] BENSON A, PIFER R, BEHRENDT C L, et al.Gut commensal bacteria direct a protective immune response against Toxoplasma gondii[J].Cell Host & Microbe, 2009, 6(2):187-196.
[32] QUINTEROS S L, VON KRUSENSTIERN E, SNYDER N W, et al.The helminth derived peptide FhHDM-1 redirects macrophage metabolism towards glutaminolysis to regulate the pro-inflammatory response[J].Frontiers in Immunology, 2023, 14:1018076.
[33] CASARAVILLA C, PITTINI Á, RVCKERL D, et al.Activation of the NLRP3 inflammasome by particles from the Echinococcus granulosus laminated layer[J].Infection and Immunity, 2020, 88(9):e00190-20.
[34] CELIAS D P, CORVO I, SILVANE L, et al.Cathepsin L3 from Fasciola hepatica induces NLRP3 inflammasome alternative activation in murine dendritic cells[J].Frontiers in Immunology, 2019, 10:552.
[35] ELINAV E, STROWIG T, KAU A L, et al.NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis[J].Cell, 2011, 145(5):745-757.
[36] BAO C H, WANG C Y, LI G N, et al.Effect of mild moxibustion on intestinal microbiota and NLRP6 inflammasome signaling in rats with post-inflammatory irritable bowel syndrome[J].World Journal of Gastroenterology, 2019, 25(32):4696-4714.
[37] KONGSOMBOONVECH A K, GARCÍA-LÓPEZ L, NJUME F, et al.Variation in CD8 T cell IFNγ differentiation to strains of Toxoplasma gondii is characterized by small effect QTLs with contribution from ROP16[J].Frontiers in Cellular and Infection Microbiology, 2023, 13:1130965.
[38] MOREIRA-SOUZA A C A, NANINI H F, RANGEL T P, et al.P2X7 receptor modulation of the gut microbiota and the inflammasome determines the severity of Toxoplasma gondii-induced ileitis[J].Biomedicines, 2023, 11(2):555.
[39] STEAR M, PRESTON S, PIEDRAFITA D, et al.The immune response to nematode infection[J].International Journal of Molecular Sciences, 2023, 24(3):2283.
[40] MAO T, SU C W, JI Q, et al.Hyaluronan-induced alterations of the gut microbiome protects mice against Citrobacter rodentium infection and intestinal inflammation[J].Gut Microbes, 2021, 13(1):1972757.
[41] LEUNG J M, BUDISCHAK S A, CHUNG THE H, et al.Rapid environmental effects on gut nematode susceptibility in rewilded mice[J].PLoS Biology, 2018, 16(3):e2004108.
[42] ROBERTSON A, SALL J, VENZON M, et al.Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching[J].bioRxiv, 2023, Doi:10.1101/2023.03.13.532458.
[43] RAJAMANIKAM A, ISA M N M, SAMUDI C, et al.Gut bacteria influence Blastocystis sp.phenotypes and may trigger pathogenicity[J].PLoS Neglected Tropical Diseases, 2023, 17(3):e0011170.
[44] HENRIQUEZ F L, MOONEY R, BANDEL T, et al.Paradigms of protist/bacteria symbioses affecting human health:Acanthamoeba species and Trichomonas vaginalis[J].Frontiers in Microbiology, 2021, 11:616213.
[45] ABOELSOUED D, ABDEL MEGEED K N.Diagnosis and control of cryptosporidiosis in farm animals[J].Journal of Parasitic Diseases, 2022, 46(4):1133-1146.
[46] BAUTISTA-GARFIAS C R, GÓMEZ M B, AGUILAR B R, et al.The treatment of mice with Lactobacillus casei induces protection against Babesia microti infection[J].Parasitology Research, 2005, 97(6):472-477.
[47] BAUTISTA C R, SANDOVAL A, AGUILAR B R.Effect of high- and low-molecular-weight components of Lactobacillus casei on resistance against Babesia microti in NIH mice[J].Annals of the New York Academy of Sciences, 2008, 1149:152-154.
[48] SHUKLA G, DEVI P, SEHGAL R.Effect of Lactobacillus casei as a probiotic on modulation of giardiasis[J].Digestive Diseases and Sciences, 2008, 53(10):2671-2679.
[49] MARTÍNEZ-GÓMEZ F, IXTA-RODRÍGUEZ O, AGUILAR-FIGUEROA B, et al.Lactobaciilus casei ssp.rhamnosus enhances non specific protection against Plasmodium chabaudi AS in mice[J].Salud Publica de Mexico, 2006, 48(6):498-503.
[50] BAUTISTA-GARFIAS C R, IXTA-RODRÍGUEZ O, MARTÍNEZ-GÓMEZ F, et al.Effect of viable or dead Lactobacillus casei organisms administered orally to mice on resistance against Trichinella spiralis infection[J].Parasite (Paris, France), 2001, 8(2 Suppl):S226-228.
[51] KATO I, TANAKA K, YOKOKURA T.Lactic acid bacterium potently induces the production of interleukin-12 and interferon-gamma by mouse splenocytes[J].International Journal of Immunopharmacology, 1999, 21(2):121-131.
[52] MIDHA A, JANEK K, NIEWIENDA A, et al.The intestinal roundworm Ascaris suum releases antimicrobial factors which interfere with bacterial growth and biofilm formation[J].Frontiers in Cellular and Infection Microbiology, 2018, 8:271.
[53] WHITE E C, HOULDEN A, BANCROFT A J, et al.Manipulation of host and parasite microbiotas:Survival strategies during chronic nematode infection[J].Science Advances, 2018, 4(3):eaap7399.
[54] BENSON A K, KELLY S A, LEGGE R, et al.Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors[J].Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(44):18933-18938.
[55] GOODRICH J K, DAVENPORT E R, WATERS J L, et al.Cross-species comparisons of host genetic associations with the microbiome[J].Science (New York, N.Y.), 2016, 352(6285):532-535.
[56] LING F, STEINEL N, WEBER J, et al.The gut microbiota response to helminth infection depends on host sex and genotype[J].The ISME Journal, 2020, 14(5):1141-1153.
[57] AYABINA D V, CLARK J, BAYLEY H, et al.Gender-related differences in prevalence, intensity and associated risk factors of Schistosoma infections in Africa:A systematic review and meta-analysis[J].PLoS Neglected Tropical Diseases, 2021, 15(11):e0009083.
[58] ŚWISŁOCKA M, BORKOWSKA A, MATOSIUK M, et al.Sex-biased polyparasitism in moose (Alces alces) based on molecular analysis of faecal samples[J].International Journal for Parasitology.Parasites and Wildlife, 2020, 13:171-177.
[59] WESOŁOWSKA A.Sex-the most underappreciated variable in research:Insights from helminth-infected hosts[J].Veterinary Research, 2022, 53(1):94.
[60] BORDES F, PONLET N, DE BELLOCQ J G, et al.Is there sex-biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections[J].Oecologia, 2012, 170(1):123-135.