Toxocara canis-induced changes in host intestinal microbial communities.
16S rRNA high-throughput sequencing
Intestinal flora
Toxocara canis
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
19 Dec 2023
19 Dec 2023
Historique:
received:
12
10
2023
accepted:
29
11
2023
medline:
20
12
2023
pubmed:
20
12
2023
entrez:
20
12
2023
Statut:
epublish
Résumé
Toxocara canis is a roundworm that resides in the gastrointestinal tract of dogs and causes various pathological changes. The dog's intestinal system consists of a diverse and dynamic bacterial community that has extensive effects on intestinal physiology, immunity and metabolics. In the case of intestinal parasites, interactions with the host intestinal flora are inevitable during the process of parasitism. We studied the role of T. canis in regulating the composition and diversity of the intestinal flora of the host by high-throughput sequencing of the 16S ribosomal RNA gene and various bioinformatics analyses. The α-diversity analysis showed that Toxocara canis infection resulted in a significant decrease in the abundance and diversity of host intestinal flora. The β-diversity analysis showed that the intestinal flora of infected dogs was similar to that carried by T. canis. Analysis of the microflora composition and differences at the phylum level showed that the ratio of Firmicutes to Bacteroidetes (F/B ratio) increased with T. canis infection. Analysis of species composition and differences at the genus level revealed that the proportion of some of the pathogenic bacteria, such as Clostridium sensu stricto and Staphylococcus, increased after T. canis infection. Toxocara canis infection affected the composition and diversity of the flora in the host intestinal tract. These results not only shed light on the potential mechanism of T. canis invasion and long-term survival in the intestinal tract, but also provide a new basis for the development of anthelmintic drugs.
Sections du résumé
BACKGROUND
BACKGROUND
Toxocara canis is a roundworm that resides in the gastrointestinal tract of dogs and causes various pathological changes. The dog's intestinal system consists of a diverse and dynamic bacterial community that has extensive effects on intestinal physiology, immunity and metabolics. In the case of intestinal parasites, interactions with the host intestinal flora are inevitable during the process of parasitism.
METHODS
METHODS
We studied the role of T. canis in regulating the composition and diversity of the intestinal flora of the host by high-throughput sequencing of the 16S ribosomal RNA gene and various bioinformatics analyses.
RESULTS
RESULTS
The α-diversity analysis showed that Toxocara canis infection resulted in a significant decrease in the abundance and diversity of host intestinal flora. The β-diversity analysis showed that the intestinal flora of infected dogs was similar to that carried by T. canis. Analysis of the microflora composition and differences at the phylum level showed that the ratio of Firmicutes to Bacteroidetes (F/B ratio) increased with T. canis infection. Analysis of species composition and differences at the genus level revealed that the proportion of some of the pathogenic bacteria, such as Clostridium sensu stricto and Staphylococcus, increased after T. canis infection.
CONCLUSIONS
CONCLUSIONS
Toxocara canis infection affected the composition and diversity of the flora in the host intestinal tract. These results not only shed light on the potential mechanism of T. canis invasion and long-term survival in the intestinal tract, but also provide a new basis for the development of anthelmintic drugs.
Identifiants
pubmed: 38115028
doi: 10.1186/s13071-023-06072-w
pii: 10.1186/s13071-023-06072-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
462Subventions
Organisme : National Natural Science Foundation of China
ID : U22A20363
Informations de copyright
© 2023. The Author(s).
Références
Hotez PJ. Human parasitology and parasitic diseases: heading towards 2050. Adv Parasitol. 2018;100:29–38.
doi: 10.1016/bs.apar.2018.03.002
pubmed: 29753341
Szwabe K, Blaszkowska J. Stray dogs and cats as potential sources of soil contamination with zoonotic parasites. Ann Agric Environ Med. 2017;24:39–43.
doi: 10.5604/12321966.1234003
pubmed: 28378987
Wright I, Stafford K, Coles G. The prevalence of intestinal nematodes in cats and dogs from Lancashire, north-west England. J Small Anim Pract. 2016;57:393–5.
doi: 10.1111/jsap.12478
pubmed: 27071856
Karo-Atar D, Gregorieff A, King IL. Dangerous liaisons: how helminths manipulate the intestinal epithelium. Trends Parasitol. 2023;39:414–22.
doi: 10.1016/j.pt.2023.03.012
pubmed: 37076358
Loke P, Harris NL. Networking between helminths, microbes, and mammals. Cell Host Microbe. 2023;31:464–71.
doi: 10.1016/j.chom.2023.02.008
pubmed: 37054669
Hasnain SZ, Gallagher AL, Grencis RK, Thornton DJ. A new role for mucins in immunity: insights from gastrointestinal nematode infection. Int J Biochem Cell Biol. 2013;45:364–74.
doi: 10.1016/j.biocel.2012.10.011
pubmed: 23107603
Tizard IR, Jones SW. The microbiota regulates immunity and immunologic diseases in dogs and cats. Vet Clin North Am Small Anim Pract. 2018;48:307–22.
doi: 10.1016/j.cvsm.2017.10.008
pubmed: 29198905
Lee SC, Tang MS, Lim YA, Choy SH, Kurtz ZD, Cox LM, et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl Trop Dis. 2014;8:e2880.
doi: 10.1371/journal.pntd.0002880
pubmed: 24851867
pmcid: 4031128
Morton ER, Lynch J, Froment A, Lafosse S, Heyer E, Przeworski M, et al. Variation in rural african gut microbiota is strongly correlated with colonization by Entamoeba and subsistence. PLoS Genet. 2015;11:e1005658.
doi: 10.1371/journal.pgen.1005658
pubmed: 26619199
pmcid: 4664238
Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Fölsch UR, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53:685–93.
doi: 10.1136/gut.2003.025403
pubmed: 15082587
pmcid: 1774050
Sepehri S, Kotlowski R, Bernstein CN, Krause DO. Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease. Inflamm Bowel Dis. 2007;13:675–83.
doi: 10.1002/ibd.20101
pubmed: 17262808
Yang CA, Liang C, Lin CL, Hsiao CT, Peng CT, Lin HC, et al. Impact of Enterobius vermicularis infection and mebendazole treatment on intestinal microbiota and host immune response. PLoS Negl Trop Dis. 2017;11:e0005963.
doi: 10.1371/journal.pntd.0005963
pubmed: 28945752
pmcid: 5629029
Kupritz J, Angelova A, Nutman TB, Gazzinelli-Guimaraes PH. Helminth-induced human gastrointestinal dysbiosis: a systematic review and meta-analysis reveals insights into altered taxon diversity and microbial gradient collapse. MBio. 2021;12:e0289021.
doi: 10.1128/mBio.02890-21
pubmed: 34933444
Easton AV, Raciny-Aleman M, Liu V, Ruan E, Marier C, Heguy A, et al. Immune response and microbiota profiles during coinfection with Plasmodium vivax and soil-transmitted helminths. MBio. 2020;11:e01705-e1720.
doi: 10.1128/mBio.01705-20
pubmed: 33082257
pmcid: 7587435
Dominguez-Bello MG, Blaser MJ, Ley RE, Knight R. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology. 2011;140:1713–9.
doi: 10.1053/j.gastro.2011.02.011
pubmed: 21530737
Barko PC, Mcmichael MA, Swanson KS, Williams DA. The gastrointestinal microbiome: a review. J Vet Intern Med. 2017;32:9–25.
doi: 10.1111/jvim.14875
pubmed: 29171095
pmcid: 5787212
Berrilli F, Di Cave D, Cavallero S, D’Amelio S. Interactions between parasites and microbial communities in the human gut. Front Cell Infect Microbiol. 2012;2:141.
doi: 10.3389/fcimb.2012.00141
pubmed: 23162802
pmcid: 3499702
Rosa BA, Supali T, Gankpala L, Djuardi Y, Sartono E, Zhou Y, et al. Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia. Microbiome. 2018;6:33.
doi: 10.1186/s40168-018-0416-5
pubmed: 29486796
pmcid: 6389212
Cooper P, Walker AW, Reyes J, Chico M, Salter SJ, Vaca M, et al. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLoS ONE. 2013;8:e76573.
doi: 10.1371/journal.pone.0076573
pubmed: 24124574
pmcid: 3790696
Zhong H, Penders J, Shi Z, Ren H, Cai K, Fang C, et al. Impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age children. Microbiome. 2019;7:2.
doi: 10.1186/s40168-018-0608-z
pubmed: 30609941
pmcid: 6320620
Whitman WB, Oren A, Chuvochina M, da Costa MS, Garrity GM, Rainey FA, et al. Proposal of the suffixota to denote phyla. Addendum to “Proposal to include the rank of phylum in the International Code of Nomenclature of Prokaryotes.” Int J Syst Evol Microbiol. 2018;68:967–9.
doi: 10.1099/ijsem.0.002593
pubmed: 29458499
Jeske O, Jogler M, Petersen J, Sikorski J, Jogler C. From genome mining to phenotypic microarrays: Planctomycetes as source for novel bioactive molecules. Antonie Van Leeuwenhoek. 2013;104:551–67.
doi: 10.1007/s10482-013-0007-1
pubmed: 23982431
Boedeker C, Schüler M, Reintjes G, Jeske O, van Teeseling MC, Jogler M, et al. Determining the bacterial cell biology of Planctomycetes. Nat Commun. 2017;8:14853.
doi: 10.1038/ncomms14853
pubmed: 28393831
pmcid: 5394234
Guo P, Zhang K, Ma X, He P. Clostridium species as probiotics: potentials and challenges. J Anim Sci Biotechnol. 2020;11:24.
doi: 10.1186/s40104-019-0402-1
pubmed: 32099648
pmcid: 7031906
Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, Bell J, Jones RN, et al. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997–1999. Clin Infect Dis. 2001;32:S114–32.
doi: 10.1086/320184
pubmed: 11320452