Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Babeisa duncani infection alters gut microbiota profile in hamsters

  • Shangdi Zhang (Lanzhou University Second Hospital) ;
  • Jinming Wang (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Xiaoyun Li (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Yanbo Wang (Lanzhou University Second Hospital) ;
  • Yueli Nian (Lanzhou University Second Hospital) ;
  • Chongge You (Lanzhou University Second Hospital) ;
  • Dekui Zhang (Lanzhou University Second Hospital) ;
  • Guiquan Guan (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences)
  • Received : 2022.10.13
  • Accepted : 2022.12.19
  • Published : 2023.02.28
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Abstract

The genus Babesia includes parasites that can induce human and animal babesiosis, which are common in tropical and subtropical regions of the world. The gut microbiota has not been examined in hamsters infected by Babesia duncani. Red blood cells infected with B. duncani were injected into hamsters through intraperitoneal route. To evaluate the changes in gut microbiota, DNAs were extracted from small intestinal contents, acquired from hamsters during disease development. Then, the V4 region of the 16S rRNA gene of bacteria was sequenced using the Illumina sequencing platform. Gut microbiota alternation and composition were assessed according to the sequencing data, which were clustered with >97.0% sequence similarity to create amplicon sequence variants (ASVs). Bacteroidetes and Firmicutes were made up of the major components of the gut microbiota in all samples. The abundance of Bacteroidetes elevated after B. duncani infection than the B. duncani-free group, while Firmicutes and Desulfobacterota declined. Alpha diversity analysis demonstrated that the shown ASVs were substantially decreased in the highest parasitemia group than B. duncani-free and lower parasitemia groups. Potential biomarkers were discovered by Linear discriminant analysis Effect Size (LEfSe) analysis, which demonstrated that several bacterial families (including Muribaculaceae, Desulfovibrionaceae, Oscillospiraceae, Helicobacteraceae, Clostridia UGG014, Desulfovibrionaceae, and Lachnospiraceae) were potential biomarkers in B. duncani-infected hamsters. This research demonstrated that B. duncani infectious can modify the gut microbiota of hamsters.

Keywords

Acknowledgement

This study was financially supported by the Science Fund for Creative Research Groups of Gansu Province (22JR5RA024), the Natural Science Foundation of Gansu (22JR5RA031), Gansu Natural Science Foundation (21JR11RA130), the Science and Technology Development Guiding Program of Lanzhou (2019ZD-55), Cuiying Scientific and Technological Program of Lanzhou University Second Hospital (CY2019-BJ05), the National Science Foundation of China (grant no. 31972701), ASTIP (grant no. CAAS-ASTIP-2016-LVRI), and NBCIS (grant no. CARS-37), the Leading Fund of Lanzhou Veterinary Research Institute (LVRI-SZJJ-202105), and the hatching program of SKLVEB (SKLVEB2021CGQD02).

References

  1. Gray J, Zintl A, Hildebrandt A, Hunfeld KP, Weiss L. Zoonotic babesiosis: overview of the disease and novel aspects of pathogen identity. Ticks Tick Borne Dis 2010;1(1):3-10. https://doi.org/10.1016/j.ttbdis.2009.11.003
  2. Cornillot E, Hadj-Kaddour K, Dassouli A, Noel B, Ranwez V, et al. Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti. Nucleic Acids Res 2012; 40(18):9102-9114. https://doi.org/10.1093/nar/gks700
  3. Skrabalo Z, Deanovic Z. Piroplasmosis in man; report of a case. Doc Med Geogr Trop 1957;9(1):11-16.
  4. Scholtens RG, Braff EH, Healey GA, Gleason N. Gleason. A case of babesiosis in man in the United States. Am J Trop Med Hyg 1968;17(6):810-813. https://doi.org/10.4269/ajtmh.1968.17.810
  5. Wang J, Zhang S, Yang J, Liu J, Zhang D, et al. Babesia divergens in human in Gansu province, China. Emerg Microbes Infect 2019;8(1):959-961. https://doi.org/10.1080/22221751.2019.1635431
  6. Kim JY, Cho SH, Joo HN, Tsuji M, Cho SR, et al. First case of human babesiosis in Korea: detection and characterization of a novel type of Babesia sp. (KO1) similar to ovine Babesia. J Clin Microbiol 2007;45(6):2084-2087. https://doi.org/10.1128/JCM.01334-06
  7. Shih CM, Liu LP, Chung WC, Ong SJ, Wang CC. Human babesiosis in Taiwan: asymptomatic infection with a Babesia microti-like organism in a Taiwanese woman. J Clin Microbiol 1997;35(2):450-454. https://doi.org/10.1128/jcm.35.2.450-454. 1997
  8. Quick RE, Herwaldt BL, Thomford JW, Garnett ME, Eberhard ML, et al. Babesiosis in Washington State: a new species of Babesia? Ann Intern Med 1993;119(4):284-290. https://doi.org/10.7326/0003-4819-119-4-199308150-00006
  9. Scott JD, Scott CM. Human babesiosis caused by Babesia duncani has widespread distribution across Canada. Healthcare (Basel) 2018;6(2):49. https://doi.org/10.3390/healthcare6020049
  10. Villarino NF, LeCleir GR, Denny JE, Dearth SP, Harding CL, et al. Composition of the gut microbiota modulates the severity of malaria. Proc Natl Acad Sci U S A 2016;113(8):2235-2240.https://doi.org/10.1073/pnas.1504887113
  11. Kamada N, Chen GY, Inohara N, Nunez G. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol 2013;14(7):685-690. https://doi.org/10.1038/ni.2608
  12. Fan ZG, Li X, Fu HY, Zhou LM, Gong FL, et al. Gut microbiota reconstruction following host infection with blood-stage Plasmodium berghei ANKA strain in a murine model. Curr Med Sci 2019;39(6):883-889. https://doi.org/10.1007/s11596-019-2119-y
  13. Wei N, Cao J, Zhang H, Zhou Y, Zhou J. The tick microbiota dysbiosis promote tick-borne pathogen transstadial transmission in a Babesia microti-infected mouse model. Front Cell Infect Microbiol 2021;11:713466. https://doi.org/10.3389/fcimb.2021.713466
  14. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019;37(8): 852-857. https://doi.org/10.1038/s41587-019-0209-9
  15. Abrams Y. Complications of coinfection with Babesia and Lyme disease after splenectomy. J Am Board Fam Med 2008; 21(1):75-77. https://doi.org/10.3122/jabfm.2008.01.060182
  16. Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, SouzaNeto JA, et al. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 2011; 332(6031):855-858. https://doi.org/10.1126/science.1201618
  17. Dong Y, Manfredini F, Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 2009;5(5):e1000423. https://doi.org/10.1371/ journal.ppat.1000423
  18. Azambuja P, Garcia ES, Ratcliffe NA. Gut microbiota and parasite transmission by insect vectors. Trends Parasitol 2005; 21(12):568-572. https://doi.org/10.1016/j.pt.2005.09.011
  19. Yilmaz B, Portugal S, Tran TM, Gozzelino R, Ramos S, et al. Gut microbiota elicits a protective immune response against malaria transmission. Cell 2014;159(6):1277-1289. https://doi.org/10.1016/j.cell.2014.10.053
  20. Taniguchi T, Miyauchi E, Nakamura S, Hirai M, Suzue K, et al. Plasmodium berghei ANKA causes intestinal malaria associated with dysbiosis. Sci Rep 2015;5:15699. https://doi.org/10.1038/srep15699
  21. Guan W, Yang S, Zhao Y, Cheng W, Song X, et al. Observation of the gut microbiota profile in C57BL/6 mice induced by Plasmodium berghei ANKA infection. Front Cell Infect Microbiol 2021;11:680383. https://doi.org/10.3389/fcimb.2021.680383
  22. Johnson EL, Heaver SL, Walters WA, Ley RE. Microbiome and metabolic disease: revisiting the bacterial phylum Bacteroidetes. J Mol Med (Berl) 2017;95(1):1-8. https://doi.org/10.1007/s00109-016-1492-2
  23. Raimondi S, Musmeci E, Candeliere F, Amaretti A, Rossi M. Identification of mucin degraders of the human gut microbiota. Sci Rep 2021;11(1):11094. https://doi.org/10.1038/s41598-021-90553-4
  24. Shimizu Y, Nakamura K, Kikuchi M, Ukawa S, Nakamura K, et al. Lower human defensin 5 in elderly people compared to middle-aged is associated with differences in the intestinal microbiota composition: the DOSANCO health study. Geroscience 2022;44(2):997-1009. https://doi.org/10.1007/s11357-021-00398-y