Metagenomics Characterization of Ixodes ricinus Intestinal Microbiota as Major Vector of Tick-Borne Diseases in Domestic Animals
-
Manijeh Yousefi Behzadi
,
Atefeh Mehrabi
,
Mozhgan Ahmadinezhad
,
Mahdi Rohani
,
Saeid Reza Naddaf
,
Amin Bagheri
,
Masoomeh Shams-Ghahfarokhi
,
Ebrahim Maghsoudlou
,
Nooshin Mojahed
,
Leila Mounesan
,
Zahra Tahmasebi
,
Aria Sohrabi
,
Mostafa Salehi-Vasiri
,
Zahra Salehi
,
Mehdi Razzaghi-Abyaneh
Abstract
Background: Understanding the microbiota of disease vectors can help for developing new strategies to prevent the transmission of vector pathogens. Ixodes ricinus is one of the most notorious tick vectors with increasing importance in Iran and other parts of the world while there is limited data on its microbiota. This study aimed to use metagenomics for identifying the I. ricinus tick’s microbiota of Iran.
Methods: A total of 39 adult ticks were collected from Mazandaran (21 females), Gilan (17 females), and Golestan (1 male). Five tick pools prepared from 39 adults of I. ricinus were subjected to metagenomics analysis. The data were analyzed by targeting the V6 region of the 16S rRNA gene by Illumina 4000 Hiseq sequencing.
Results: Among hundreds of intestinal microbiota identified by metagenomics, various pathogenic microorganisms distributed in 30 genera and species including those responsible for tick-borne diseases resided in the genera Coxiella, Rickettsia, and Burkholderia were found.
Conclusion: Our results indicated that metagenomics identifies bacteria genera and species which cannot be easily recognized by routine methods. The presence of such pathogenic bacteria indicates the importance of possible zoonotic diseases in this region which could affect public health. These results further substantiate the importance of advanced metagenomics analyses to identify neglected tick-borne pathogens which enable researchers to provide efficient mapping roads for the management of emerging and re-emerging infectious diseases.
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4. Černý J, Lynn G, Hrnková J, Golovchenko M, Rudenko N, Grubhoffer L (2020) Man¬agement options for Ixodes ricinus-as¬so¬ciated pathogens: a review of prevention strategies. Int J Environ Res Publ Health. 17(6): 1830.
5. James M, Bowman A, Forbes K, Lewis F, McLeod J, Gilbert L (2013) Environ-men¬tal determinants of Ixodes ricinus ticks and the incidence of Borrelia burgdor¬feri sensu lato, the agent of Lyme bor¬reliosis, in Scotland. Parasitology. 140 (2): 237–246.
6. Alfredsson M, Olafsson E, Eydal M, Unnsteinsdot¬tir ER, Hansford K, Wint W, Alexander N, Medlock JM (2017) Surveil¬lance of Ixodes ricinus ticks (Ac-ari: Ixodi¬dae) in Iceland. Parasit Vec-tors. 10(1): 466.
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9. Choubdar N, Oshaghi MA, Rafinejad J, Pour¬mand MR, Maleki-Ravasan N, Salehi-Vaziri M, Telmadarraiy Z, Karim-ian F, Koosha M, Rahimi-Foroushani A, Masoo¬mi S, Arzamani K, Nejati J, Karami M, Mozaffari E, Salim-Abadi Y, Moradi-Asl E, Taghilou B, Shirani M (2019) Effect of meteorologi¬cal factors on Hyalomma species com¬position and their host preference, sea¬sonal preva-lence and infection status to crimean-congo haemorrhagic fe¬ver in Iran. J Ar-thropod Borne Dis. 13 (3): 268–283.
10. Seedorf H, Griffin NW, Ridaura VK, Reyes A, Cheng J, Rey FE, Smith MI, Simon GM, Scheffrahn RH, Woebken D, Spor¬mann AM, Van Treuren W, Ursell LK, Pirrung M, Robbins-Pianka A, Cantarel BL, Lombard V, Henrissat B, Knight R, Gordon JI (2014) Bacteria from diverse habitats colonize and com-pete in the mouse gut. Cell. 159(2): 253–266.
11. Eybpoosh S, Haghdoost AA, Mostafavi E, Bahrampour A, Azadmanesh K, Zolala F (2017) Molecular epidemiology of in¬fectious diseases. Electron Phys. 9(8): 5149.
12. Lange A (2021) Interactions between in-tes¬ti¬nal commensal bacteria and differ-ent hosts: two sides of the same story: PhD Thesis, Universität Tübingen.
13. Tabasi M, Eybpoosh S, Siadat SD, El-yasinia F, Soroush A, Bouzari S (2021) Modulation of the gut microbiota and se¬rum biomarkers after laparoscopic sleeve gastrectomy: a 1-year follow-up study. Obes Surg. 31: 1949–1956.
14. Narasimhan S, Fikrig E (2015) Tick mi¬cro-biome: the force within. Trends Par-asitol. 31(7): 315–323.
15. Dantas-Torres F, Chomel BB, Otranto D (2021) Ticks and tick-borne diseases: a One Health perspective. Trends Parasi-tol. 28(10): 437–446.
16. Wilhelmsson P, Jaenson TG, Olsen B, Wal¬denström J, Lindgren P-E (2020) Migra¬tory birds as disseminators of ticks and the tick-borne pathogens Borrelia bacte¬ria and tick-borne encephalitis (TBE) vi¬rus: a seasonal study at Ottenby Bird Ob¬ser¬va¬tory in South-eastern Sweden. Par¬a¬sit Vectors. 13: 1–17.
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18. Wilhelmsson P, Pawełczyk O, Jaenson TG, Waldenström J, Olsen B, Forsberg P, Lind¬gren PE (2021) Three Babesia species in Ixodes ricinus ticks from migratory birds in Sweden. Parasit Vectors. 14(1): 183.
19. Pettersson JH-O (2013) The Origin of the Genus Flavivirus and the Ecology of Tick-Borne Pathogens, PhD Thesis, Acta Uni¬ver¬sitatis Upsaliensis.
20. Blanda V, Torina A, La Russa F, D'Ago-stino R, Randazzo K, Scimeca S, Giu-dice E, Caracappa S, Cascio A, de la Fuente J (2017) A retrospective study of the char¬acterization of Rickettsia species in ticks collected from humans. Ticks Tick Borne Dis. 8(4): 610–614.
21. Cutler SJ, Ruzic-Sabljic E, Potkonjak A (2017) Emerging borreliae–Expanding be¬yond Lyme borreliosis. Mol Cell Probes. 31: 22–27.
22. Mansfield KL, Cook C, Ellis RJ, Bell-Sakyi L, Johnson N, Alberdi P, de la Fuente J, Fooks AR (2017) Tick-borne pathogens induce differential expression of genes pro¬moting cell survival and host resistance in Ixodes ricinus cells. Parasit Vectors. 10(1): 81.
23. Reis C, Cote M, Le Rhun D, Lecuelle B, Levin ML, Vayssier-Taussat M, Bonnet SI (2011) Vector competence of the tick Ixodes ricinus for transmission of Bar-tonella birtlesii. PLoS Negl Trop Dis. 5(5): e1186.
24. Pajoro M, Pistone D, Varotto Boccazzi I, Mereghetti V, Bandi C, Fabbi M, Scat-torin F, Sassera D, Montagna M (2018) Molecular screening for bacterial path-ogens in ticks (Ixodes ricinus) collected on migratory birds captured in northern Italy. Folia Parasitol. 65: 2018.008.
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26. Song X, Zhong Z, Gao L, Weiss BL, Wang J (2022) Metabolic interactions between disease-transmitting vectors and their mi¬crobiota. Trends Parasitol. 38(8): 697–708.
27. Fukuda K, Ogawa M, Taniguchi H, Saito M (2016) Molecular approaches to stud-ying microbial communities: targeting the 16S ribosomal RNA gene. J UOEH. 38 (3): 223–232.
28. Mathison BA, Pritt BS (2014) Laboratory identification of arthropod ectoparasites. Clin Microbiol Rev. 27(1): 48–67.
29. Salehi Z, Shams-Ghahfarokhi M, Fattahi A, Ghazanfari M, Yazdanparast SA (2018) A head-to-head comparison of four cry¬o¬preservation protocols of dermatophyte species. Infect Epidemiol Microbiol. 4(3): 109–114.
30. Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next gen-eration sequencing data. PloS One. 7(2): e30619.
31. Okonechnikov K, Conesa A, García-Al-cal¬de F (2016) Qualimap 2: advanced multi-sample quality control for high-through¬put sequencing data. Bioinfor-matics. 32(2): 292-294.
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| Files | ||
| Issue | Vol 17 No 2 (2023) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v17i2.13620 | |
| Keywords | ||
| Tick-borne disease; Microbiota; Ixodes ricinus; Next-generation sequencing; Emerging pathogens | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Yousefi Behzadi M, Mehrabi A, Ahmadinezhad M, Rohani M, Naddaf SR, Bagheri A, Shams-Ghahfarokhi M, Maghsoudlou E, Mojahed N, Mounesan L, Tahmasebi Z, Sohrabi A, Salehi-Vasiri M, Salehi Z, Razzaghi-Abyaneh M. Metagenomics Characterization of Ixodes ricinus Intestinal Microbiota as Major Vector of Tick-Borne Diseases in Domestic Animals. J Arthropod Borne Dis. 2023;17(2):152–164.
