Research progress on the interaction between intestinal nematodes and intestinal flora

doi:10.12140/j.issn.1000-7423.2024.05.012

Abstract

Abstract:

The intestinal flora is an important component of human intestinal microenvironment, playing important roles in digestion and absorption, nutrient metabolism, defense against pathogenic infections and regulation of autoimmune diseases. There are complex interactions between parasites residing in the host’s gut and the host’s gut microbiota, influencing the health of the host’s intestine and the onset and progression of related diseases. This article reviews the research progress on the interaction between host intestinal nematodes and intestinal flora, to provide scientific basis for a deeper understanding of the pathogenic mechanisms of related diseases.

Key words: Intestinal flora, Intestinal nematodes, Interaction

CLC Number:

R383.1

ZHANG Zhilan, YIN Sixuan, LV Fangli. Research progress on the interaction between intestinal nematodes and intestinal flora[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2024, 42(5): 642-647.

References 53

[1]	Papaiakovou M, Littlewood DTJ, Doyle SR, et al. Worms and bugs of the gut: the search for diagnostic signatures using barcoding, and metagenomics-metabolomics[J]. Parasit Vectors, 2022, 15(1): 118. doi: 10.1186/s13071-022-05225-7 pmid: 35365192
[2]	Kang WH, Jee SC. Enterobius vermicularis (pinworm) infection[J]. N Engl J Med, 2019, 381(1): e1.
[3]	Lin H, Yang GY. Strongyloidiasis of human and animals[J]. Chin J Zoonoses, 2016, 32(5): 477-484, 505. (in Chinese)
	(林海, 杨光友. 人和动物的类圆线虫病[J]. 中国人兽共患病学报, 2016, 32(5): 477-484, 505.)
[4]	Brooker S, Clements AC, Bundy DA. Global epidemiology, ecology and control of soil-transmitted helminth infections[J]. Adv Parasitol, 2006, 62: 221-261.
[5]	Horrocks V, King OG, Yip AYG, et al. Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization[J]. Microbiology (Reading), 2023, 169(8): 001377.
[6]	Cortés A, Peachey L, Scotti R, et al. Helminth-microbiota cross-talk: a journey through the vertebrate digestive system[J]. Mol Biochem Parasitol, 2019, 233: 111222.
[7]	Drew GC, Stevens EJ, King KC. Microbial evolution and transitions along the parasite-mutualist continuum[J]. Nat Rev Microbiol, 2021, 19(10): 623-638. doi: 10.1038/s41579-021-00550-7 pmid: 33875863
[8]	Hooper LV, Littman DR, MacPherson AJ. Interactions between the microbiota and the immune system[J]. Science, 2012, 336(6086): 1268-1273. doi: 10.1126/science.1223490 pmid: 22674334
[9]	Gause WC, Maizels RM. Macrobiota: helminths as active participants and partners of the microbiota in host intestinal homeostasis[J]. Curr Opin Microbiol, 2016, 32: 14-18.
[10]	Brosschot TP, Reynolds LA. The impact of a helminth-modified microbiome on host immunity[J]. Mucosal Immunol, 2018, 11(4): 1039-1046. doi: 10.1038/s41385-018-0008-5 pmid: 29453411
[11]	Kato Y, Komatsu S. ASABF, a novel cysteine-rich antibacterial peptide isolated from the nematode Ascaris suum. Purification, primary structure, and molecular cloning of cDNA[J]. J Biol Chem, 1996, 271(48): 30493-30498. doi: 10.1074/jbc.271.48.30493 pmid: 8940016
[12]	Marillier RG, Michels C, Smith EM, et al. IL-4/IL-13 independent goblet cell hyperplasia in experimental helminth infections[J]. BMC Immunol, 2008, 9: 11. doi: 10.1186/1471-2172-9-11 pmid: 18373844
[13]	Datta R, DeSchoolmeester ML, Hedeler C, et al. Identification of novel genes in intestinal tissue that are regulated after infection with an intestinal nematode parasite[J]. Infect Immun, 2005, 73(7): 4025-4033. pmid: 15972490
[14]	Sun SM, Wang XL, Wu XP, et al. Toll-like receptor activation by helminths or helminth products to alleviate inflammatory bowel disease[J]. Parasit Vectors, 2011, 4: 186. doi: 10.1186/1756-3305-4-186 pmid: 21943110
[15]	Walusimbi B, Lawson MAE, Nassuuna J, et al. The effects of helminth infections on the human gut microbiome: a systematic review and meta-analysis[J]. Front Microbiomes, 2023, 2: 1174034.
[16]	Cooper P, Walker AW, Reyes J, et al. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota[J]. PLoS One, 2013, 8(10): e76573.
[17]	Pryshliak OY, Protsyk AL, Semaniv MV, et al. Effect of probiotics on the intestinal microbiota of patients with giardiasis and ascariasis[J]. J Med Life, 2022, 15(10): 1278-1282. doi: 10.25122/jml-2022-0191 pmid: 36420289
[18]	Guernier V, Brennan B, Yakob L, et al. Gut microbiota disturbance during helminth infection: can it affect cognition and behaviour of children?[J]. BMC Infect Dis, 2017, 17(1): 58. doi: 10.1186/s12879-016-2146-2 pmid: 28073356
[19]	Ramírez-Carrillo E, Gaona O, Nieto J, et al. Disturbance in human gut microbiota networks by parasites and its implications in the incidence of depression[J]. Sci Rep, 2020, 10(1): 3680. doi: 10.1038/s41598-020-60562-w pmid: 32111922
[20]	Klomkliew P, Sawaswong V, Chanchaem P, et al. Gut bacteriome and metabolome of Ascaris lumbricoides in patients[J]. Sci Rep, 2022, 12(1): 19524. doi: 10.1038/s41598-022-23608-9 pmid: 36376367
[21]	Jenkins TP, Pritchard DI, Tanasescu R, et al. Experimental infection with the hookworm, Necator americanus, is associated with stable gut microbial diversity in human volunteers with relapsing multiple sclerosis[J]. BMC Biol, 2021, 19(1): 74.
[22]	Cantacessi C, Giacomin P, Croese J, et al. Impact of experimental hookworm infection on the human gut microbiota[J]. J Infect Dis, 2014, 210(9): 1431-1434. doi: 10.1093/infdis/jiu256 pmid: 24795483
[23]	Giacomin P, Zakrzewski M, Croese J, et al. Experimental hookworm infection and escalating gluten challenges are associated with increased microbial richness in celiac subjects[J]. Sci Rep, 2015, 5: 13797. doi: 10.1038/srep13797 pmid: 26381211
[24]	Chen HL, Mozzicafreddo M, Pierella E, et al. Dissection of the gut microbiota in mothers and children with chronic Trichuris trichiura infection in Pemba Island, Tanzania[J]. Parasit Vectors, 2021, 14(1): 62.
[25]	Lee SC, Tang MS, Lim YA, et al. Helminth colonization is associated with increased diversity of the gut microbiota[J]. PLoS Negl Trop Dis, 2014, 8(5): e2880.
[26]	Yang CN, Liang C, Lin CL, et al. Impact of Enterobius vermicularis infection and mebendazole treatment on intestinal microbiota and host immune response[J]. PLoS Negl Trop Dis, 2017, 11(9): e0005963.
[27]	Corthésy B. Multi-faceted functions of secretory IgA at mucosal surfaces[J]. Front Immunol, 2013, 4: 185. doi: 10.3389/fimmu.2013.00185 pmid: 23874333
[28]	Nguyen HT, Hongsrichan N, Intuyod K,et al. Strongyloides stercoralis infection induces gut dysbiosis in chronic kidney disease patients[J]. PLoS Negl Trop Dis, 2022, 16(9): e0010302.
[29]	Nguyen HT, Hongsrichan N, Intuyod K, et al. Investigation of gut microbiota and short-chain fatty acids in Strongyloides stercoralis-infected patients in a rural community[J]. Biosci Microbiota Food Health, 2022, 41(3): 121-129.
[30]	Jenkins TP, Formenti F, Castro C, et al. A comprehensive analysis of the faecal microbiome and metabolome of Strongyloides stercoralis infected volunteers from a non-endemic area[J]. Sci Rep, 2018, 8(1): 15651.
[31]	Rubel MA, Abbas A, Taylor LJ, et al. Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians[J]. Genome Biol, 2020, 21(1): 122. doi: 10.1186/s13059-020-02020-4 pmid: 32450885
[32]	Springer A, Wagner L, Koehler S, et al. Modulation of the porcine intestinal microbiota in the course of Ascaris suum infection[J]. Parasit Vectors, 2022, 15(1): 433. doi: 10.1186/s13071-022-05535-w pmid: 36397169
[33]	Wang YY, Liu F, Urban JF Jr, et al. Ascaris suum infection was associated with a worm-independent reduction in microbial diversity and altered metabolic potential in the porcine gut microbiome[J]. Int J Parasitol, 2019, 49(3/4): 247-256.
[34]	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]. Front Cell Infect Microbiol, 2018, 8: 271.
[35]	Sieng S, Chen P, Wang N,et al. Toxocara canis-induced changes in host intestinal microbial communities[J]. Parasit Vectors, 2023, 16(1): 462. doi: 10.1186/s13071-023-06072-w pmid: 38115028
[36]	Walk ST, Blum AM, Ewing SAS, et al. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus[J]. Inflamm Bowel Dis, 2010, 16(11): 1841-1849.
[37]	Ramanan D, Bowcutt R, Lee SC, et al. Helminth infection promotes colonization resistance via type 2 immunity[J]. Science, 2016, 352(6285): 608-612. doi: 10.1126/science.aaf3229 pmid: 27080105
[38]	Rausch S, Midha A, Kuhring M, et al. Parasitic nematodes exert antimicrobial activity and benefit from microbiota-driven support for host immune regulation[J]. Front Immunol, 2018, 9: 2282. doi: 10.3389/fimmu.2018.02282 pmid: 30349532
[39]	Shimokawa C, Obi S, Shibata M, et al. Suppression of obesity by an intestinal helminth through interactions with intestinal microbiota[J]. Infect Immun, 2019, 87(6): e00042-19.
[40]	Su CW, Chen CY, Jiao LF, et al. Helminth-induced and Th2-dependent alterations of the gut microbiota attenuate obesity caused by high-fat diet[J]. Cell Mol Gastroenterol Hepatol, 2020, 10(4): 763-778. doi: S2352-345X(20)30105-3 pmid: 32629118
[41]	Houlden A, Hayes KS, Bancroft AJ, et al. Chronic Trichuris muris infection in C57BL/6 mice causes significant changes in host microbiota and metabolome: Effects reversed by pathogen clearance[J]. PLoS One, 2015, 10(5): e0125945.
[42]	Holm JB, Sorobetea D, Kiilerich P, et al. Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of lactobacilli[J]. PLoS One, 2015, 10(5): e0125495.
[43]	Rosa BA, Snowden C, Martin J, et al. Whipworm-associated intestinal microbiome members consistent across both human and mouse hosts[J]. Front Cell Infect Microbiol, 2021, 11: 637570.
[44]	Schachter J, Alvarinho de Oliveira D, da Silva CM, et al. Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation[J]. Infect Immun, 2020, 88(3): e00642-19.
[45]	Afrin T, Murase K, Kounosu A, et al. Sequential changes in the host gut microbiota during infection with the intestinal parasitic nematode Strongyloides venezuelensis[J]. Front Cell Infect Microbiol, 2019, 9: 217.
[46]	Pace F, Carvalho BM, Zanotto TM, et al. Helminth infection in mice improves insulin sensitivity via modulation of gut microbiota and fatty acid metabolism[J]. Pharmacol Res, 2018, 132: 33-46. doi: S1043-6618(17)31647-X pmid: 29653264
[47]	Fricke WF, Song Y, Wang AJ, et al. Erratum to: type 2 immunity-dependent reduction of segmented filamentous bacteria in mice infected with the helminthic parasite Nippostrongylus brasiliensis[J]. Microbiome, 2015, 3: 77.
[48]	Nobre V, Serufo JC, Carvalho ODOSS, et al. Alteration in the endogenous intestinal flora of Swiss Webster mice by experimental Angiostrongylus costaricensis infection[J]. Mem Inst Oswaldo Cruz, 2004, 99(7): 717-720.
[49]	Hayes KS, Bancroft AJ, Goldrick M, et al. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris[J]. Science, 2010, 328(5984): 1391-1394. doi: 10.1126/science.1187703 pmid: 20538949
[50]	Dea-Ayuela MA, Rama-Iñiguez S, Bolás-Fernandez F. Enhanced susceptibility to Trichuris muris infection of B10Br mice treated with the probiotic Lactobacillus casei[J]. Int Immunopharmacol, 2008, 8(1): 28-35.
[51]	Oliveira-Sequeira TCG, David ÉB, Ribeiro C, et al. Effect of Bifidobacterium animalis on mice infected with Strongyloides venezuelensis[J]. Rev Inst Med Trop Sao Paulo, 2014, 56(2): 105-109.
[52]	Jang S, Lakshman S, Beshah E, et al. Flavanol-rich cocoa powder interacts with Lactobacillus rhamnossus LGG to alter the antibody response to infection with the parasitic nematode Ascaris suum[J]. Nutrients, 2017, 9(10): 1113.
[53]	Thomas DJ, Husmann RJ, Villamar M,et al. Lactobacillus rhamnosus HN001 attenuates allergy development in a pig model[J]. PLoS One, 2011, 6(2): e16577.