Interaction of the Rhipicephalus microplus tick microbiota with the pathogen Anaplasma marginale
Keywords:
ticks, tick microbiota, Rhipicephalus microplus, Anaplasma marginale, anti-microbiota vaccinesAbstract
Introduction: Ticks transmit pathogens to their hosts. Manipulating their microbiota can be used to modify their physiology and affect their ability to transmit pathogens. This constitutes an alternative to chemical control that generates contamination and resistant ticks.
Objectives: To study the microbial community resident in Rhipicephalus microplus ticks over time and during their ontogeny and their interaction with the pathogenic bacterium Anaplasma marginale.
Methods: The presence of A. marginale was studied using end-point PCR or high-throughput real-time microfluidics. Using tick DNA, sequences of the 16S ribosomal RNA gene V4 variable region were obtained and taxonomically classified to generate microbial community phylogenies. The topology of these communities, their associations, and key taxa were determined through co-occurrence network analysis.
Results: The increase of A. marginale in R. microplus microbial communities correlated with a reduction in their diversity and, as a keystone taxon, induced community dysbiosis. It was most abundant in nymphs with well-structured connectivity and interactions. Pseudoalteromonas was a keystone taxon that correlated positively with A. marginale, while the endosymbiont Coxiella correlated negatively.
Conclusions: A. marginale modifies the microbial community of R. microplus to facilitate its colonization. Its greater abundance in nymphs suggests the more important role of this stage in the transmission of this pathogen. Key taxa that interact with A. marginale can be manipulated targets to decrease the vector capacity of R. microplus.
Downloads
References
1. Hopla CE, Durden LA, Keirans JE. Ectoparasites and classification. Rev Sci Tech. 1994;13(4):985-1017.
2. Jasiorowski HA. Opening statement for the FAO Expert Consultation on Revision of Strategies for the Control of Ticks and Tick-borne Diseases. Parassitologia. 1990;32(1):13-4.
3. Graf JF, Gogolewski R, Leach-Bing N, Sabatini GA, Molento MB, Bordin EL, et al. Tick control: an industry point of view. Parasitology. 2004;129 Suppl:S427-42.
4. Heath A, Levot GW. Parasiticide resistance in flies, lice and ticks in New Zealand and Australia: mechanisms, prevalence and prevention. N Z Vet J. 2015;63(4):199-210.
5. Wang J, Gao L, Aksoy, S. Microbiota in disease-transmitting vectors. Nature Reviews Microbiology. 2023;21(9):604-18.
6. Fogaça AC, Sousa G, Pavanelo DB, Esteves E, Martins LA, Urbanová V, Kopáček P, Daffre S. Tick Immune System: What Is Known, the Interconnections, the Gaps, and the Challenges. Frontiers in immunology. 2021;12: 628054.
7. 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 Frontiers in Cellular and Infection Microbiology. 2021;11:713466.
8. Mateos-Hernández L OD, Wu-Chuang A, Maye J, Bornères J, Versillé N, et al. Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner. Front Immunol 2021(12):704621.
9. Mateos-Hernandez L, Obregon D, Maye J, Borneres J, Versille N, de la Fuente J, Estrada-Peña A, Hodzic A, Simo L, Cabezas-Cruz A. Anti-Tick Microbiota Vaccine Impacts Ixodes ricinus Performance during Feeding. Vaccines. 2020;8(4).
10. Abraham NM, Liu L, Jutras BL, Yadav AK, Narasimhan S, Gopalakrishnan V, et al. Pathogen-mediated manipulation of arthropod microbiota to promote infection. Proc Natl Acad Sci U S A. 2017;114(5):E781-e90.
11. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Nature Biotechnology. 2019;37(8):852-7.
12. Katoh K, Misawa K, Kuma KI, Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fouriern transform. Nucleic Acids Research. 2002;30(14):3059-66.
13. Price MN, Dehal PS, Arkin AP. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5(3):e9490.
14. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and webbased tools Nucleic Acids Res. 2013;41(Database issue):D590-D6.
15. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Appl Environ Microbiol. 2006;72 (7):5069-72.
16. Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv 1992;61:1-10.
17. Pielou EC. Species-diversity and pattern-diversity in the study of ecological succession J Theor Biol. 1966;10 (2):370-83.
18. Bray JR, Curtis, J. T. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs. 1957;27(4):326-49.
19. Friedman J, Alm EJ. Inferring correlation networks from genomic survey data. PLoS Computational Biology. 2012;8(9):e1002687.
20. Estrada-Peña A, Bouattour A, Camicas J, Walker A. Ticks of domestic animals in the Mediterranean region. A guide to identification of species. Zaragoza, España: University of Zaragoza. 2004.
21. Gondard MD S, Pinarello V, Aprelon R, Devillers E, Galon C, Pradel J, Vayssier-Taussat M, Albina E, Moutailler S. Upscaling the surveillance of tick-borne pathogens in the French Caribbean islands. Pathogens. 2020;9:176.
22. Mateos-Hernández L, Obregon D, Wu-Chuang A, Maye J, Bornères J, Versillé N, de La Fuente J, Díaz-Sánchez S, Bermúdez-Humarán LG, Torres-Maravilla E, Estrada-Peña A, Hodžić A, Šimo L, Cabezas-Cruz A. Anti-microbiota vaccines modulate the tick microbiome in a taxon-specific manner. Frontiers in immunology. 2021;12:704621.
23. Guizzo MG, Tirloni L, Gonzalez SA, Farber MD, Braz G, Parizi LF, Dedavid E Silva LA, Da Silva Vaz I, Oliveira PL. Coxiella endosymbiont of Rhipicephalus microplus modulates tick physiology with a major impact in blood feeding capacity. Front Microbiol 2022;13:868575.
24. Rialch A, Sankar M, Silamparasan M, Madhusoodan AP, Kharayat NS, Gautam S, Gurav AR, Thankappan S. Molecular detection of Coxiella-like endosymbionts in Rhipicephalus microplus from north India. Vet Parasitol: Reg Stud Rep 2022;36:100803.
25. Encinosa Guzmán PE, Fernández C, Cano Argüelles AL, Fuentes Castillo A, García Y, Rodríguez R, et al. Characterization of two Cuban colonies of Rhipicephalus microplus ticks. Veterinary Parasitology: Regional Studies and Reports. 2021;25:100591.
26. Duron O, Jourdain E, McCoy KD. Diversity and global distribution of the Coxiella intracellular bacterium in seabird ticks. Ticks Tick Borne Dis. 2014;5(5):557-63.
27. Hammer Ø, Harper DA. Past: paleontological statistics software package for educaton and data anlysis. Palaeontologia electronica. 2001;4(1):1.
28. Abuin-Denis L, Piloto-Sardiñas E, Maître A, Wu-Chuang A, Mateos-Hernández L, Obregon D, Cabezas-Cruz A. Exploring the impact of Anaplasma phagocytophilum on colonization resistance of Ixodes scapularis microbiota using network node manipulation. Current Research in Parasitology & Vector-Borne Diseases. 2024;5:100177.
29. Spragge F, Bakkeren E, Jahn MT, BN Araujo E, Pearson CF, Wang X, Foster KR. Microbiome diversity protects against pathogens by nutrient blocking. Science. 2023;382:6676 eadj3502.
30. Piloto-Sardiñas E, Foucault-Simonin A, Wu-Chuang A, Mateos-Hernández L, Marrero-Perera R, Abuin-Denis L, Roblejo-Arias L, Díaz-Corona C, Zaja Z, Kulisz J, Wozniak A, Moutailler S, Corona-González B, Cabezas-Cruz A. Dynamics of infections in cattle and Rhipicephalus microplus: A preliminary study. Pathogens. 2023;12(8):998.
31. Woolhouse MET, SM, Jennings A, Chase-Topping M Callaby R, Kiara H, Oosthuizen MC, Mbole-Kariuki MN, Conradie I, Handel IG, et al. Co-infections determine patterns of mortality in a population exposed to parasite infection. Sci Adv Virus Res. 2015(1):1400026.
32. Eriks IS, Stiller D, Palmer GH. Impact of persistent Anaplasma marginale rickettsemia on tick infection and transmission. J Clin Microbiol. 1993;31(8):2091-6.
33. Nair ASR R, Lakshmanan B, Sreekumar C, Kumar SS, Raju R, Tresamol PV, Vimalkumar MB Saseendranath MR. Bovine carriers of Anaplasma marginale and Anaplasma bovis in South India. Trop Biomed. 2013;30:105-12.
34. Wei Z, Yang T, Friman VP, Xu Y, Shen Q, Jousset A. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nature communications. 2015;6:8413.
35. Piloto‐Sardiñas E, Abuin‐Denis L, Maitre A, Foucault‐Simonin A, Corona‐González B, Díaz‐Corona C, Roblejo-Arias L, Mateos-Hernández L, Marrero-Perera R, Obregon D, Svobodová K, Wu-Chuang A, Cabezas‐Cruz A. Dynamic nesting of Anaplasma marginale in the microbial communities of Rhipicephalus microplus. Ecology and Evolution. 2024;14(4):e11228.
36. Abuin-Denis L, Piloto-Sardiñas E, Maitre A, Wu-Chuang A, Mateos-Hernández L, Paulino PG, Bello Y, Ledesma Bravo F, Alvarez Gutierrez A, Rodríguez R, Fuentes Castillo A, Méndez L, Foucault-Simonin A, Obregon D, Estrada-García MP, Rodríguez-Mallon A, Cabezas-Cruz A. Differential nested patterns of Anaplasma marginale and Coxiella-like endosymbiont across Rhipicephalus microplus ontogeny. Microbiological Research. 2024:127790.
37. Maitre A, Wu-Chuang A, Mateos-Hernández L, Piloto-Sardiñas E, Foucault-Simonin A, Cicculli V, Moutailler S, Paoli JC, Falchi A, Obregón D, Cabezas-Cruz A. Rickettsial pathogens drive microbiota assembly in Hyalomma marginatum and Rhipicephalus bursa ticks. Molecular Ecology. 2023;32(16):4660-76.
38. Duron O, Binetruy F, Noël V, Cremaschi J, McCoy KD, Arnathau C, Chevillon C. Evolutionary changes in symbiont community structure in ticks. Molecular ecology. 2017;26(11):2905-21.
39. Pavanelo DB P-SE, Maitre A, Abuin-Denis L, Kopa´ cˇ ek P, Cabezas Cruz A and Fogac¸a AC. Arthropod microbiota: shaping pathogen establishment and enabling control. Front Arachn Sci. 2023;2:1297733.
40. Duron O, Gottlieb Y. Convergence of nutritional symbioses in obligate blood feeders. Trends Parasitol. 2020;36(10):816-25.
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Lianet Abuin Denis, Elianne Piloto Sardiñas, Belkis Corona González, Alina Rodríguez Mallon, Alejandro Cabezas Cruz, Lourdes Mateos-Hernández, Alejandra Wu-Chuang, Dasiel Obregón, Apolline Maitre, Angélique Foucault-Simonin, Roxana Marrero-Perera, Lisset Roblejo Arias, Cristian Díaz-Corona, Mario Pablo Estrada García, Luis Méndez Mellor, Karolína Svobodová, Alier Fuentes Castillo, Rafmary Rodríguez Fernández, Frank Luis Ledesma, Patrícia Gonzaga Paulino, Yamil Bello Soto, Anays Álvarez Gutiérrez
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The journal Anales de la Academia de Ciencias de Cuba protects copyright, and operates with a Creative Commons License 4.0 (Creative Commons Attribution-NonCommercial License 4.0). By publishing in it, authors allow themselves to copy, reproduce, distribute, publicly communicate their work and generate derivative works, as long as the original author is cited and acknowledged. They do not allow, however, the use of the original work for commercial or lucrative purposes.
The authors authorize the publication of their writings, retaining the authorship rights, and assigning and transferring to the magazine all the rights protected by the intellectual property laws that govern in Cuba, which imply editing to disseminate the work.
Authors may establish additional agreements for the non-exclusive distribution of the version of the work published in the journal (for example, placing it in an institutional repository or publishing it in a book), with recognition of having been first published in this journal.
To learn more, see https://creativecommons.org
