Molecular detection of Wolbachia endosymbiont in reptiles and their ectoparasites.
Ixodes ricinus
Lizard
Neotrombicula autumnalis
Snake
Wolbachia
Journal
Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571
Informations de publication
Date de publication:
Sep 2021
Sep 2021
Historique:
received:
21
05
2021
accepted:
30
06
2021
pubmed:
23
7
2021
medline:
14
10
2021
entrez:
22
7
2021
Statut:
ppublish
Résumé
Wolbachia, a maternally transmitted Gram-negative endosymbiont of onchocercid nematodes and arthropods, has a role in the biology of their host; thus it has been exploited for the filariasis treatment in humans. To assess the presence and prevalence of this endosymbiont in reptiles and their ectoparasites, blood and tail tissue as well as ticks and mites collected from them were molecularly screened for Wolbachia DNA using two sets of primers targeting partial 16S rRNA and Wolbachia surface protein (wsp) genes. Positive samples were screened for the partial 12S rRNA and cytochrome c oxidase subunit 1 (cox1) genes for filarioids. Of the different species of lizards (Podarcis siculus, Podarcis muralis and Lacerta bilineata) and snakes (Elaphe quatuorlineata and Boa constrictor constrictor) screened from three collection sites, only P. siculus scored positive for Wolbachia 16S rRNA. Among ectoparasites collected from reptiles (Ixodes ricinus ticks and Neotrombicula autumnalis, Ophionyssus sauracum and Ophionyssus natricis mites), I. ricinus (n = 4; 2.8%; 95% CI, 0.9-7) from P. siculus, N. autumnalis (n = 2 each; 2.8%; 95% CI, 0.9-6.5) from P. siculus and P. muralis and O. natricis (n = 1; 14.3%; 95% CI, 0.7-55.4) from Boa constrictor constrictor scored positive for Wolbachia DNA. None of the positive Wolbachia samples scored positive for filarioids. This represents the first report of Wolbachia in reptilian hosts and their ectoparasites, which follows a single identification in the intestinal cells of a filarioid associated with a gecko. This data could contribute to better understand the reptile filarioid-Wolbachia association and to unveil the evolutionary pattern of Wolbachia in its filarial host.
Identifiants
pubmed: 34292377
doi: 10.1007/s00436-021-07237-1
pii: 10.1007/s00436-021-07237-1
pmc: PMC8397688
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3255-3261Informations de copyright
© 2021. The Author(s).
Références
Anuradha R, George PJ, Kumar NP, Fay MP, Kumaraswami V, Nutman TB, Babu S (2012) Circulating microbial products and acute phase proteins as markers of pathogenesis in lymphatic filarial disease. PLoS Pathog 8(6):e1002749
pubmed: 22685406
pmcid: 3369944
Bandi C, Anderson TJC, Genchi C, Blaxter ML (1998) Phylogeny of Wolbachia pipientis in filarial nematodes. Proc R Soc Lond B 265:2407–2413
Bandi C, Trees AJ, Brattig NW (2001) Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet Parasitol 98:215–238
pubmed: 11516587
Bassini-Silva R, Jacinavicius FC, Mendoza-Roldan JA, Daemon E, Barros-Battesti DM (2017) Description of Blankaartia shatrovi n. sp. (Acari: Trombiculidae) from Brazil. J Med Entomol 54(1):82–90
pubmed: 28082634
Bezerra-Santos MA, Mendoza-Roldan JA, Thompson RA, Dantas-Torres F, Otranto D (2021) Illegal wildlife trade: a gateway to zoonotic infectious diseases. Trends in Parasitology 37(3):181–184
pubmed: 33454218
Brattig NW, Bazzocchi C, Kirschning CJ, Reiling N, Büttner DW, Ceciliani F, Geisinger F, Hochrein H, Ernst M, Wagner H, Bandi C (2004) The major surface protein of Wolbachia endosymbionts in filarial nematodes elicits immune responses through TLR2 and TLR4. J Immunol 173(1):437–445
pubmed: 15210803
Brown AM, Wasala SK, Howe DK, Peetz AB, Zasada IA, Denver DR (2016) Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts. Sci Rep 6(1):1–4
Casiraghi M, Bain O, Guerrero R, Martin C, Pocacqua V, Gardner SL, Franceschi A, Bandi C (2004) Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. Int J Parasitol 34(2):191–203
pubmed: 15037105
Casiraghi M, Bordenstein SR, Baldo L, Lo N, Beninati T, Wernegreen JJ, Werren JH, Bandi C (2005) Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology 151(12):4015–4022
pubmed: 16339946
Casiraghi M, Favia G, Cancrini G, Bartoloni A, Bandi C (2001) Molecular identification of Wolbachia from the filarial nematode Mansonella ozzardi. Parasitol Res 87(5):417–420
pubmed: 11403387
Chomczynski P (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 15(3):532–534
pubmed: 7692896
Fenn K, Conlon C, Jones M, Quail MA, Holroyd NE, Parkhill J, Blaxter M (2006) Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathog 2(10):e94
pubmed: 17040125
pmcid: 1599763
Ferri E, Bain O, Barbuto M, Martin C, Lo N, Uni S, Landmann F, Baccei SG, Guerrero R, de Souza Lima S, Bandi C (2011) New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species. PloS one 6(6):e20843
pubmed: 21731626
pmcid: 3120775
Glowska E, Dragun-Damian A, Dabert M, Gerth M (2015) New Wolbachia supergroups detected in quill mites (Acari: Syringophilidae). Infect Genet Evol 30:140–146
pubmed: 25541519
Haegeman A, Vanholme B, Jacob J, Vandekerckhove TT, Claeys M, Borgonie G, Gheysen G (2009) An endosymbiotic bacterium in a plant-parasitic nematode: member of a new Wolbachia supergroup. Int J Parasitol 39(9):1045–1054
pubmed: 19504759
Jacinavicius FDC, Bassini-Silva R, Mendoza-Roldan JA, Muñoz-Leal S, Hingst-Zaher E, Ochoa R, Barros-Battesti DM (2018) A contribution to the knowledge of Quadraseta brasiliensis Goff and Gettinger, 1989 (Trombidiformes: Trombiculidae), with description of the deutonymph instar. Acarologia 58(2):442–456
Jacobson ER, Garner MM (eds) (2020) Infectious diseases and pathology of reptiles: color atlas and text, diseases and pathology of reptiles, vol 1. CRC Press. https://doi.org/10.1201/9780429155567
Jeyaprakash A, Hoy MA (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 9(4):393–405
pubmed: 10971717
Keiser PB, Coulibaly Y, Kubofcik J, Diallo AA, Klion AD, Traoré SF, Nutman TB (2008) Molecular identification of Wolbachia from the filarial nematode Mansonella perstans. Mol Biochem Parasitol 160(2):123–128
pubmed: 18538871
pmcid: 2497444
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120
pubmed: 7463489
Kramer L, Passeri B, Corona S, Simoncini L, Casiraghi M (2003) Immunohistochemical/immunogold detection and distribution of the endosymbiont Wolbachia of Dirofilaria immitis and Brugia pahangi using a polyclonal antiserum raised against WSP (Wolbachia surface protein). Parasitol Res 89(5):381–386
pubmed: 12632152
Kremer N, Voronin D, Charif D, Mavingui P, Mollereau B, Vavre F (2009) Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog. 5(10):e1000630
pubmed: 19851452
pmcid: 2759286
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
pubmed: 29722887
pmcid: 5967553
Landmann F, Bain O, Martin C, Uni S, Taylor MJ, Sullivan W (2012) Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biol Open 1(6):536–47
pubmed: 23213446
pmcid: 3509449
Lefoulon E, Bain O, Makepeace BL, d’Haese C, Uni S, Martin C, Gavotte L (2016) Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts. PeerJ 4:e1840
pubmed: 27069790
pmcid: 4824920
Lefoulon E, Clark T, Guerrero R, Cañizales I, Cardenas-Callirgos JM, Junker K, Vallarino-Lhermitte N, Makepeace BL, Darby AC, Foster JM, Martin C (2020) Diminutive, degraded but dissimilar: Wolbachia genomes from filarial nematodes do not conform to a single paradigm. Microb Genom 6(12):e000487
Lefoulon E, Clark T, Borveto F, Perriat-Sanguinet M, Moulia C, Slatko BE, Gavotte L (2020b) Pseudoscorpion Wolbachia symbionts: diversity and evidence for a new supergroup S. BMC Microbiol 20(1):1–5
Lefoulon E, Gavotte L, Junker K, Barbuto M, Uni S, Landmann F, Laaksonen S, Saari S, Nikander S, de Souza LS, Casiraghi M (2012) A new type F Wolbachia from Splendidofilariinae (Onchocercidae) supports the recent emergence of this supergroup. Int J Parasitol 42(11):1025–1036
pubmed: 23041355
Manoj RRS, Latrofa MS, Epis S, Otranto D (2021) Wolbachia: endosymbiont of onchocercid nematodes and their vectors. Parasit Vectors 14(1):1–24
Martin AR, Brown GK, Dunstan RH, Roberts TK (2005) Anaplasma platys: an improved PCR for its detection in dogs. Exp Parasitol 109(3):176–180
pubmed: 15713449
Martin C, Gavotte L (2010) The bacteria Wolbachia in filariae, a biological Russian dolls’ system: new trends in antifilarial treatments. Parasite 17(2):79–89
pubmed: 20597434
Martinez J, Tolosana I, Ok S, Smith S, Snoeck K, Day JP, Jiggins FM (2017) Symbiont strain is the main determinant of variation in Wolbachia-mediated protection against viruses across Drosophila species. Mol Ecol 26(15):4072–4084
pubmed: 28464440
pmcid: 5966720
Mendoza-Roldan J, Ribeiro SR, Castilho-Onofrio V, Grazziotin FG, Rocha B, Ferreto-Fiorillo B, Pereira JS, Benelli G, Otranto D, Barros-Battesti DM (2020) Mites and ticks of reptiles and amphibians in Brazil. Acta Trop 208:105515
pubmed: 32407792
Mendoza-Roldan JA, Colella V, Lia RP, Nguyen VL, Barros-Battesti DM, Iatta R, Dantas-Torres F, Otranto D (2019) Borrelia burgdorferi (sensu lato) in ectoparasites and reptiles in southern Italy. Parasit Vectors 12(1):1–9
Mendoza-Roldan JA, Ravindran Santhakumari Manoj R, Latrofa MS, Iatta R, Annoscia G, Lovreglio P, Stufano A, Dantas-Torres F, Davoust B, Laidoudi Y, Mediannikov O, Otranto D (2021) Role of reptiles and associated arthropods in the epidemiology of rickettsioses: a one health paradigm. PLoS Negl Trop Dis 15(2):e0009090
pubmed: 33596200
pmcid: 7888606
Mendoza-Roldan JA, Mendoza-Roldan MA, Otranto D (2021b) Reptile vector-borne diseases of zoonotic concern. Int J Parasitol Parasites Wildl 15:132–142
Otranto D, Sakru N, Testini G, Gürlü VP, Yakar K, Lia RP, Dantas-Torres F, Bain O (2011) First evidence of human zoonotic infection by Onchocerca lupi (Spirurida, Onchocercidae). Am J Trop Med Hyg 84(1):55–58
pubmed: 21212202
pmcid: 3005520
Rasgon JL, Scott TW (2004) Phylogenetic characterization of Wolbachia symbionts infecting Cimex lectularius L. and Oeciacus vicarius Horvath (Hemiptera: Cimicidae). J Med Entomol 41(6):1175–1178
pubmed: 15605657
Ros VI, Fleming VM, Feil EJ, Breeuwer JA (2009) How diverse is the genus Wolbachia? Multiple-gene sequencing reveals a putatively new Wolbachia supergroup recovered from spider mites (Acari: Tetranychidae). Appl Environ Microbiol 75(4):1036–1043
pubmed: 19098217
Shiny C, Krushna NS, Archana B, Farzana B, Narayanan RB (2009) Serum antibody responses to Wolbachia surface protein in patients with human lymphatic filariasis. Microbiol Immunol 53(12):685–693
pubmed: 19954456
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
pubmed: 24132122
pmcid: 3840312
Taylor MJ, Hoerauf A (1999) Wolbachia bacteria of filarial nematodes. Parasitol Today 15(11):437–442
pubmed: 10511685
Taylor MJ (2003) Wolbachia in the inflammatory pathogenesis of human filariasis. Ann N Y Acad Sci 990(1):444–449
pubmed: 12860672
Werren JH, Windsor D, Guo LR (1995) Distribution of Wolbachia among neotropical arthropods. Proc Royal Soc B P Roy Soc B-Bol Sci 262(1364):197–204.
Zhou W, Rousset F, O'Neill S (1998) Phylogeny and PCR–based classification of Wolbachia strains using wsp gene sequences. Proc Royal Soc B P Roy Soc B-Bol Sci 265(1395):509–515.