Volume 28, Number 9—September 2022
Research
Detection of Endosymbiont Candidatus Midichloria mitochondrii and Tickborne Pathogens in Humans Exposed to Tick Bites, Italy
Table 1
Tickborne bacteria | Target gene | Primers | Sequence, 5ˈ → 3ˈ | Base pairs | Reference |
---|---|---|---|---|---|
Coxiella burnetii | IS1111a | Trans1 | TATGTATCCACCGTAGCCAGT | 687 | (21) |
Trans2 |
CCCAACAACACCTCCTTATTC |
||||
Rickettsia spp. | gltA | CS 78F | GCAAGTATCGGTGAGGATGTAAT | 401 | (22) |
CS 323R |
GCTTCCTTAAAATTCAATAAATCAGGAT |
||||
Borrelia burgdorferi sensu lato complex | Flagellin | FLA1 | AGAGCAACTTACAGACGAAATTAAT | 482 | (23) |
FLA2 |
CAAGTCTATTTTGGAAAGCACCTAA |
||||
Anaplasmataceae | 16S rRNA | EHR 16SD | GGTACCYACAGAAGAAGTCC | 345 | (24) |
EHR 16SR | TAGCACTCATCGTTTACAGC |
References
- Dantas-Torres F, Chomel BB, Otranto D. Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol. 2012;28:437–46. DOIPubMedGoogle Scholar
- Madison-Antenucci S, Kramer LD, Gebhardt LL, Kauffman E. Emerging tick-borne diseases. Clin Microbiol Rev. 2020;33:e00083–18. DOIPubMedGoogle Scholar
- Mendoza-Roldan JA, Ravindran Santhakumari Manoj R, Latrofa MS, Iatta R, Annoscia G, Lovreglio P, et al. Role of reptiles and associated arthropods in the epidemiology of rickettsioses: A one health paradigm. PLoS Negl Trop Dis. 2021;15:
e0009090 . DOIPubMedGoogle Scholar - Silva-Rodríguez EA, Gálvez N, Swan GJF, Cusack JJ, Moreira-Arce D. Urban wildlife in times of COVID-19: What can we infer from novel carnivore records in urban areas? Sci Total Environ. 2021;765:
142713 . DOIPubMedGoogle Scholar - Sgroi G, Iatta R, Lia RP, D’Alessio N, Manoj RRS, Veneziano V, et al. Spotted fever group rickettsiae in Dermacentor marginatus from wild boars in Italy. Transbound Emerg Dis. 2021;68:2111–20. DOIPubMedGoogle Scholar
- Otranto D, Dantas-Torres F, Giannelli A, Latrofa MS, Cascio A, Cazzin S, et al. Ticks infesting humans in Italy and associated pathogens. Parasit Vectors. 2014;7:328. DOIPubMedGoogle Scholar
- Sgroi G, Iatta R, Lia RP, Napoli E, Buono F, Bezerra-Santos MA, et al. Tick exposure and risk of tick-borne pathogens infection in hunters and hunting dogs: a citizen science approach. Transbound Emerg Dis. 2022;69:e386–93. DOIPubMedGoogle Scholar
- Santino I, Cammarata E, Franco S, Galdiero F, Oliva B, Sessa R, et al. Multicentric study of seroprevalence of Borrelia burgdorferi and Anaplasma phagocytophila in high-risk groups in regions of central and southern Italy. Int J Immunopathol Pharmacol. 2004;17:219–23. DOIPubMedGoogle Scholar
- Toepp AJ, Willardson K, Larson M, Scott BD, Johannes A, Senesac R, et al. Frequent exposure to many hunting dogs significantly increases tick exposure. Vector Borne Zoonotic Dis. 2018;18:519–23. DOIPubMedGoogle Scholar
- Jansen A, La Scola B, Raoult D, Lierz M, Wichmann O, Stark K, et al. Antibodies against Rickettsia spp. in hunters, Germany. Emerg Infect Dis. 2008;14:1961–3. DOIPubMedGoogle Scholar
- Kmetiuk LB, Krawczak FS, Machado FP, Paploski IAD, Martins TF, Teider-Junior PI, et al. Ticks and serosurvey of anti-Rickettsia spp. antibodies in wild boars (Sus scrofa), hunting dogs and hunters of Brazil. PLoS Negl Trop Dis. 2019;13:
e0007405 . DOIPubMedGoogle Scholar - Sgroi G, Varcasia A, Dessì G, D’Alessio N, Pacifico L, Buono F, et al. Massive Taenia hydatigena cysticercosis in a wild boar (Sus scrofa) from Italy. Acta Parasitol. 2019;64:938–41. DOIPubMedGoogle Scholar
- Stavru F, Riemer J, Jex A, Sassera D. When bacteria meet mitochondria: The strange case of the tick symbiont Midichloria mitochondrii†. Cell Microbiol. 2020;22:
e13189 . DOIPubMedGoogle Scholar - Cafiso A, Sassera D, Romeo C, Serra V, Hervet C, Bandi C, et al. Midichloria mitochondrii, endosymbiont of Ixodes ricinus: evidence for the transmission to the vertebrate host during the tick blood meal. Ticks Tick Borne Dis. 2019;10:5–12. DOIPubMedGoogle Scholar
- Mariconti M, Epis S, Gaibani P, Dalla Valle C, Sassera D, Tomao P, et al. Humans parasitized by the hard tick Ixodes ricinus are seropositive to Midichloria mitochondrii: is Midichloria a novel pathogen, or just a marker of tick bite? Pathog Glob Health. 2012;106:391–6. DOIPubMedGoogle Scholar
- Serra V, Krey V, Daschkin C, Cafiso A, Sassera D, Maxeiner HG, et al. Seropositivity to Midichloria mitochondrii (order Rickettsiales) as a marker to determine the exposure of humans to tick bite. Pathog Glob Health. 2019;113:167–72. DOIPubMedGoogle Scholar
- Epis S, Sassera D, Beninati T, Lo N, Beati L, Piesman J, et al. Midichloria mitochondrii is widespread in hard ticks (Ixodidae) and resides in the mitochondria of phylogenetically diverse species. Parasitology. 2008;135:485–94. DOIPubMedGoogle Scholar
- Bazzocchi C, Mariconti M, Sassera D, Rinaldi L, Martin E, Cringoli G, et al. Molecular and serological evidence for the circulation of the tick symbiont Midichloria (Rickettsiales: Midichloriaceae) in different mammalian species. Parasit Vectors. 2013;6:350. DOIPubMedGoogle Scholar
- Serra V, Cafiso A, Formenti N, Verheyden H, Plantard O, Bazzocchi C, et al. Molecular and serological evidence of the presence of Midichloria mitochondrii in roe deer (Capreolus capreolus) in France. J Wildl Dis. 2018;54:597–600. DOIPubMedGoogle Scholar
- Berri M, Laroucau K, Rodolakis A. The detection of Coxiella burnetii from ovine genital swabs, milk and fecal samples by the use of a single touchdown polymerase chain reaction. Vet Microbiol. 2000;72:285–93. DOIPubMedGoogle Scholar
- Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, et al. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol. 2004;42:90–8. DOIPubMedGoogle Scholar
- Wójcik-Fatla A, Szymańska J, Wdowiak L, Buczek A, Dutkiewicz J. Coincidence of three pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti) in Ixodes ricinus ticks in the Lublin macroregion. Ann Agric Environ Med. 2009;16:151–8.PubMedGoogle Scholar
- Parola P, Roux V, Camicas JL, Baradji I, Brouqui P, Raoult D. Detection of ehrlichiae in African ticks by polymerase chain reaction. Trans R Soc Trop Med Hyg. 2000;94:707–8. DOIPubMedGoogle Scholar
- Nakamura T, Yamada KD, Tomii K, Katoh K. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics. 2018;34:2490–2. DOIPubMedGoogle Scholar
- Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3. DOIPubMedGoogle Scholar
- Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4. DOIPubMedGoogle Scholar
- Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35:518–22. DOIPubMedGoogle Scholar
- Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9. DOIPubMedGoogle Scholar
- Zhang J, Kapli P, Pavlidis P, Stamatakis A. A general species delimitation method with applications to phylogenetic placements. Bioinformatics. 2013;29:2869–76. DOIPubMedGoogle Scholar
- Balaban M, Sarmashghi S, Mirarab S. APPLES: scalable distance-based phylogenetic placement with or without alignments. Syst Biol. 2020;69:566–78. DOIPubMedGoogle Scholar
- Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49(W1):W293–6. DOIPubMedGoogle Scholar
- Sergeant ESG. Epitools epidemiological calculators. Ausvet. 2018 [cited 2022 Jan 14]. http://epitools.ausvet.com.au
- Körner S, Makert GR, Ulbert S, Pfeffer M, Mertens-Scholz K. The prevalence of Coxiella burnetii in hard ticks in Europe and their role in Q fever transmission revisited—a systematic review. Front Vet Sci. 2021;8:
655715 . DOIPubMedGoogle Scholar - Gürtler L, Bauerfeind U, Blümel J, Burger R, Drosten C, Gröner A, et al. Coxiella burnetii—pathogenic agent of Q (query) fever. Transfus Med Hemother. 2014;41:60–72. DOIPubMedGoogle Scholar
- Mediannikov O, Matsumoto K, Samoylenko I, Drancourt M, Roux V, Rydkina E, et al. Rickettsia raoultii sp. nov., a spotted fever group rickettsia associated with Dermacentor ticks in Europe and Russia. Int J Syst Evol Microbiol. 2008;58:1635–9. DOIPubMedGoogle Scholar
- Parola P, Rovery C, Rolain JM, Brouqui P, Davoust B, Raoult D. Rickettsia slovaca and R. raoultii in tick-borne Rickettsioses. Emerg Infect Dis. 2009;15:1105–8. DOIPubMedGoogle Scholar
- Li H, Zhang PH, Huang Y, Du J, Cui N, Yang ZD, et al. Isolation and identification of Rickettsia raoultii in human cases: a surveillance study in 3 medical centers in China. Clin Infect Dis. 2018;66:1109–15. DOIPubMedGoogle Scholar
- Jia N, Zheng YC, Ma L, Huo QB, Ni XB, Jiang BG, et al. Human infections with Rickettsia raoultii, China. Emerg Infect Dis. 2014;20:866–8. DOIPubMedGoogle Scholar
- Mendoza-Roldan JA, Colella V, Lia RP, Nguyen VL, Barros-Battesti DM, Iatta R, et al. Borrelia burgdorferi (sensu lato) in ectoparasites and reptiles in southern Italy. Parasit Vectors. 2019;12:35. DOIPubMedGoogle Scholar
- Sgroi G, Iatta R, Veneziano V, Bezerra-Santos MA, Lesiczka P, Hrazdilová K, et al. Molecular survey on tick-borne pathogens and Leishmania infantum in red foxes (Vulpes vulpes) from southern Italy. Ticks Tick Borne Dis. 2021;12:
101669 . DOIPubMedGoogle Scholar - Collares-Pereira M, Couceiro S, Franca I, Kurtenbach K, Schäfer SM, Vitorino L, et al. First isolation of Borrelia lusitaniae from a human patient. J Clin Microbiol. 2004;42:1316–8. DOIPubMedGoogle Scholar
- Aguero-Rosenfeld ME, Wormser GP. Lyme disease: diagnostic issues and controversies. Expert Rev Mol Diagn. 2015;15:1–4. DOIPubMedGoogle Scholar
- Budachetri K, Kumar D, Crispell G, Beck C, Dasch G, Karim S. The tick endosymbiont Candidatus Midichloria mitochondrii and selenoproteins are essential for the growth of Rickettsia parkeri in the Gulf Coast tick vector. Microbiome. 2018;6:141. DOIPubMedGoogle Scholar
- Cafiso A, Bazzocchi C, De Marco L, Opara MN, Sassera D, Plantard O. Molecular screening for Midichloria in hard and soft ticks reveals variable prevalence levels and bacterial loads in different tick species. Ticks Tick Borne Dis. 2016;7:1186–92. DOIPubMedGoogle Scholar
- Buysse M, Duron O. Multi-locus phylogenetics of the Midichloria endosymbionts reveals variable specificity of association with ticks. Parasitology. 2018;145:1969–78. DOIPubMedGoogle Scholar
- Matsumoto K, Izri A, Dumon H, Raoult D, Parola P. First detection of Wolbachia spp., including a new genotype, in sand flies collected in Marseille, France. J Med Entomol. 2008;45:466–9. DOIPubMedGoogle Scholar
- Fraihi W, Fares W, Perrin P, Dorkeld F, Sereno D, Barhoumi W, et al. An integrated overview of the midgut bacterial flora composition of Phlebotomus perniciosus, a vector of zoonotic visceral leishmaniasis in the Western Mediterranean Basin. PLoS Negl Trop Dis. 2017;11:
e0005484 . DOIPubMedGoogle Scholar - Dantas-Torres F, Otranto D. Best practices for preventing vector-borne diseases in dogs and humans. Trends Parasitol. 2016;32:43–55. DOIPubMedGoogle Scholar
1These authors contributed equally to this article.
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