1887

Abstract

We determined the distribution of microbial endosymbionts as possible agents of parthenogenesis in Oribatida. We screened mites from 20 species of 14 families suspected to be parthenogenetic from the absence or rarity of males. Our research included parthenogenesis-inducing bacteria spp., spp., spp., and additionally , and microsporidia that can also manipulate host reproduction. We detected the endosymbionts by PCR-based methods and transmission electron microscopy (TEM) observation of fixed and stained preparations of host cells. We detected only in one Oribatida species, , by identifying genes using PCR. TEM observations confirmed infection by the endosymbiont in and its lack in other Oribatida species. Sequence analysis of and genes showed that the strain from was different from strains characterized in some insects, crustaceans (Isopoda), mites (Tetranychidae), springtails (Hexapoda) and roundworms (Nematoda). The analysis strongly suggested that the sp. strain found in did not belong to supergroups A, B, C, D, E, F, H or M. We found that the sequences of from were clearly distantly related to sequences from the bacteria of the other supergroups. This observation makes a unique host in terms of the distinction of the strain. The role of these micro-organisms in remains unknown and is an issue to investigate.

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2015-08-01
2019-12-11
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References

  1. Augustinos A.A., Santos-Garcia D., Dionyssopoulou E., Moreira M., Papapanagiotou A., Scarvelakis M., Doudoumis V., Ramos S., Aguiar A.F., other authors. ( 2011;). Detection and characterization of Wolbachia infections in natural populations of aphids: is the hidden diversity fully unraveled?. PLoS One 6: e28695 [CrossRef] [PubMed].
    [Google Scholar]
  2. Baker M.D., Vossbrinck C.R., Didier E.S., Maddox J.V., Shadduck J.A.. ( 1995;). Small subunit ribosomal DNA phylogeny of various microsporidia with emphasis on AIDS related forms. J Eukaryot Microbiol 42: 564–570 [CrossRef] [PubMed].
    [Google Scholar]
  3. Baldo L., Dunning Hotopp J.C.D., Jolley K.A., Bordenstein S.R., Biber S.A., Choudhury R.R., Hayashi C., Maiden M.C.J., Tettelin H., Werren J.H.. ( 2006;). Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72: 7098–7110 [CrossRef] [PubMed].
    [Google Scholar]
  4. Bandi C., Dunn A.M., Hurst G.D.D., Rigaud T.. ( 2001;). Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends Parasitol 17: 88–94 [CrossRef] [PubMed].
    [Google Scholar]
  5. Bing X.-L., Xia W.-Q., Gui J.-D., Yan G.-H., Wang X.-W., Liu S.-S.. ( 2014;). Diversity and evolution of the Wolbachia endosymbionts of Bemisia (Hemiptera: Aleyrodidae) whiteflies. Ecol Evol 4: 2714–2737 [CrossRef] [PubMed].
    [Google Scholar]
  6. Brown G.K., Martin A.R., Roberts T.K., Aitken R.J.. ( 2001;). Detection of Ehrlichia platys in dogs in Australia. Aust Vet J 79: 554–558 [CrossRef] [PubMed].
    [Google Scholar]
  7. Casiraghi M., Bordenstein S.R., Baldo L., Lo N., Beninati T., Wernegreen J.J., Werren J.H., Bandi C.. ( 2005;). Phylogeny of Wolbachia pipientis based on gltA, groEL ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology 151: 4015–4022 [CrossRef] [PubMed].
    [Google Scholar]
  8. Charlat S., Hurst G.D.D., Merçot H.. ( 2003;). Evolutionary consequences of Wolbachia infections. Trends Genet 19: 217–223 [CrossRef] [PubMed].
    [Google Scholar]
  9. Chrostek E., Marialva M.S.P., Esteves S.S., Weinert L.A., Martinez J., Jiggins F.M., Teixeira L.. ( 2013;). Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet 9: e1003896 [CrossRef] [PubMed].
    [Google Scholar]
  10. Cianciolo J.M., Norton R.A.. ( 2006;). The ecological distribution of reproductive mode in oribatid mites, as related to biological complexity. Exp Appl Acarol 40: 1–25 [CrossRef] [PubMed].
    [Google Scholar]
  11. Cordaux R., Bouchon D., Grève P.. ( 2011;). The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends Genet 27: 332–341 [CrossRef] [PubMed].
    [Google Scholar]
  12. Crainey J.L., Wilson M.D., Post R.J.. ( 2010;). Phylogenetically distinct Wolbachia gene and pseudogene sequences obtained from the African onchocerciasis vector Simulium squamosum. Int J Parasitol 40: 569–578 [CrossRef] [PubMed].
    [Google Scholar]
  13. Dabert M., Witalinski W., Kazmierski A., Olszanowski Z., Dabert J.. ( 2010;). Molecular phylogeny of acariform mites (Acari, Arachnida): strong conflict between phylogenetic signal and long-branch attraction artifacts. Mol Phylogenet Evol 56: 222–241 [CrossRef] [PubMed].
    [Google Scholar]
  14. Fukatsu T., Nikoh N.. ( 2000;). Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta. Homoptera). Appl Environ Microbiol 66: 643–650 [CrossRef] [PubMed].
    [Google Scholar]
  15. Gerth M., Gansauge M.T., Weigert A., Bleidorn C.. ( 2014;). Phylogenomic analyses uncover origin and spread of the Wolbachia pandemic. Nat Commun 5: 5117 [CrossRef] [PubMed].
    [Google Scholar]
  16. Glaser R.L., Meola M.A.. ( 2010;). The native Wolbachia endosymbionts of Drosophila melanogaster Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One 5: e11977 [CrossRef] [PubMed].
    [Google Scholar]
  17. 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 [CrossRef] [PubMed].
    [Google Scholar]
  18. Haegeman A., Vanholme B., Jacob J., Vandekerckhove T.T.M., 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: 1045–1054 [CrossRef] [PubMed].
    [Google Scholar]
  19. Harris H.L., Brennan L.J., Keddie B.A., Braig H.R.. ( 2010;). Bacterial symbionts in insects: balancing life and death. Symbiosis 51: 37–53 [CrossRef].
    [Google Scholar]
  20. Hise A.G., Gillette-Ferguson I., Pearlman E.. ( 2004;). The role of endosymbiotic Wolbachia bacteria in filarial disease. Cell Microbiol 6: 97–104 [CrossRef] [PubMed].
    [Google Scholar]
  21. Hosokawa T., Koga R., Kikuchi Y., Meng X.Y., Fukatsu T.. ( 2010;). Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A 107: 769–774 [CrossRef] [PubMed].
    [Google Scholar]
  22. Hoy M.A., Jeyaprakash A.. ( 2008;). Symbionts, including pathogens, of the predatory mite Metaseiulus occidentalis: current and future analysis methods. Exp Appl Acarol 46: 329–347 [CrossRef] [PubMed].
    [Google Scholar]
  23. Hurst G.D.D., Jiggins F.M.. ( 2000;). Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis 6: 329–336 [CrossRef] [PubMed].
    [Google Scholar]
  24. Huson D.H., Bryant D.. ( 2006;). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267 [CrossRef] [PubMed].
    [Google Scholar]
  25. Liana M., Witaliński W.. ( 2010;). Microorganisms in the oribatid mite Hermannia gibba (C. L. Koch, 1839) (Acari: Oribatida: Hermanniidae). Biol Lett 47: 37–43 [CrossRef].
    [Google Scholar]
  26. Lindquist E.E.. ( 1984;). Current theories on the evolution of major groups of Acari and on their relationships with other groups of Arachnida, with consequent implications for their classification. . In Acarology VI, pp. 28–62. Edited by Griffith D. A., Bowman C. E.. Chichester: Ellis Horwood;.
    [Google Scholar]
  27. Lo N., Paraskevopoulos C., Bourtzis K., O'Neill S.L., Werren J.H., Bordenstein S.R., Bandi C.. ( 2007;). Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int J Syst Evol Microbiol 57: 654–657 [CrossRef] [PubMed].
    [Google Scholar]
  28. Lorenzo-Carballa M.O., Cordero-Rivera A.. ( 2009;). Thelytokous parthenogenesis in the damselfly Ischnura hastata (Odonata, Coenagrionidae): genetic mechanisms and lack of bacterial infection. Heredity (Edinb) 103: 377–384 [CrossRef] [PubMed].
    [Google Scholar]
  29. Luxton M.. ( 1972;). Studies on the oribatid mites of a Danish beech wood soil. I. Nutritional biology. Pedobiologia 12: 434–463.
    [Google Scholar]
  30. Martin O.Y., Puniamoorthy N., Gubler A., Wimmer C., Bernasconi M.V.. ( 2013;). Infections with Wolbachia, Spiroplasma, and Rickettsia in the Dolichopodidae and other Empidoidea. Infect Genet Evol 13: 317–330 [CrossRef] [PubMed].
    [Google Scholar]
  31. McNulty S.N., Foster J.M., Mitreva M., Dunning Hotopp J.C., Martin J., Fischer K., Wu B., Davis P.J., Kumar S., other authors. ( 2010;). Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS One 5: e11029 [CrossRef] [PubMed].
    [Google Scholar]
  32. Merçot H., Poinsot D.. ( 2009;). Infection by Wolbachia: from passengers to residents. C R Biol 332: 284–297 [CrossRef] [PubMed].
    [Google Scholar]
  33. Norton R.A., Palmer S.C.. ( 1991;). The distribution, mechanisms and evolutionary significance of parthenogenesis in oribatid mites. . In The Acari: Reproduction, Development and Life-History Strategies, pp. 107–136. Edited by Schuster R., Murphy W.. London: Chapman & Hall;.
    [Google Scholar]
  34. Norton R.A., Kethley J.B., Johnston D.E., O'Connor B.M.. ( 1993;). Phylogenetic perspectives on genetic systems and reproductive modes in mites. . In Evolution and Diversity of Sex Ratios, pp. 9–99. Edited by Wrensch D. L., Ebbert M. A.. New York: Chapman & Hall;.
    [Google Scholar]
  35. Perrot-Minnot M.J., Norton R.A.. ( 1997;). Obligate thelytoky in oribatid mites: no evidence for Wolbachia inducement. Can Entomol 129: 691–698 [CrossRef].
    [Google Scholar]
  36. Posada D., Crandall K.A.. ( 1998;). modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818 [CrossRef] [PubMed].
    [Google Scholar]
  37. Ritter S., Michalski S.G., Settele J., Wiemers M., Fric Z.F., Sielezniew M., Šašić M., Rozier Y., Durka W.. ( 2013;). Wolbachia infections mimic cryptic speciation in two parasitic butterfly species, Phengaris teleius P. nausithous (Lepidoptera: Lycaenidae). PLoS One 8: e78107 [CrossRef] [PubMed].
    [Google Scholar]
  38. Ros V.I.D., Fleming V.M., Feil E.J., Breeuwer J.A.J.. ( 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: 1036–1043 [CrossRef] [PubMed].
    [Google Scholar]
  39. Russell J.E., Stouthamer R.. ( 2011;). The genetics and evolution of obligate reproductive parasitism in Trichogramma pretiosum infected with parthenogenesis-inducing Wolbachia. Heredity (Edinb) 106: 58–67 [CrossRef] [PubMed].
    [Google Scholar]
  40. Russell J.A., Funaro C.F., Giraldo Y.M., Goldman-Huertas B., Suh D., Kronauer D.J.C., Moreau C.S., Pierce N.E.. ( 2012;). A veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review. PLoS One 7: e51027 [CrossRef] [PubMed].
    [Google Scholar]
  41. Sacchi L., Genchi M., Clementi E., Negri I., Alma A., Ohler S., Sassera D., Bourtzis K., Bandi C.. ( 2010;). Bacteriocyte-like cells harbour Wolbachia in the ovary of Drosophila melanogaster (Insecta, Diptera) and Zyginidia pullula (Insecta, Hemiptera). Tissue Cell 42: 328–333 [CrossRef] [PubMed].
    [Google Scholar]
  42. Saridaki A., Bourtzis K.. ( 2010;). Wolbachia: more than just a bug in insects genitals. Curr Opin Microbiol 13: 67–72 [CrossRef] [PubMed].
    [Google Scholar]
  43. Serbus L.R., Casper-Lindley C., Landmann F., Sullivan W.. ( 2008;). The genetics and cell biology of Wolbachia–host interactions. Annu Rev Genet 42: 683–707 [CrossRef] [PubMed].
    [Google Scholar]
  44. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. ( 2011;). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739 [CrossRef] [PubMed].
    [Google Scholar]
  45. Taylor G.P., Coghlin P.C., Floate K.D., Perlman S.J.. ( 2011;). The host range of the male-killing symbiont Arsenophonus nasoniae in filth fly parasitioids. J Invertebr Pathol 106: 371–379 [CrossRef] [PubMed].
    [Google Scholar]
  46. Teixeira L., Ferreira A., Ashburner M.. ( 2008;). The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6: e2 [CrossRef] [PubMed].
    [Google Scholar]
  47. Thao M.L., Baumann P.. ( 2004;). Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Curr Microbiol 48: 140–144 [CrossRef] [PubMed].
    [Google Scholar]
  48. Thompson J.D., Higgins D.G., Gibson T.J.. ( 1994;). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680 [CrossRef] [PubMed].
    [Google Scholar]
  49. Tiawsirisup S., Sripatranusorn S., Oraveerakul K., Nuchprayoon S.. ( 2008;). Distribution of mosquito (Diptera: Culicidae) species and Wolbachia (Rickettsiales: Rickettsiaceae) infections during the bird immigration season in Pathumthani province, central Thailand. Parasitol Res 102: 731–735 [CrossRef] [PubMed].
    [Google Scholar]
  50. Webb L., Carl M., Malloy D.C., Dasch G.A., Azad A.F.. ( 1990;). Detection of murine typhus infection in fleas by using the polymerase chain reaction. J Clin Microbiol 28: 530–534 [PubMed].
    [Google Scholar]
  51. Weeks A.R., Velten R., Stouthamer R.. ( 2003;). Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc Biol Sci 270: 1857–1865 [CrossRef] [PubMed].
    [Google Scholar]
  52. Weigmann G.. ( 2006;). Hornmilben (Oribatida). . In [ Die Tierwelt Deutschlands., Vol. 76 Goecke & Evers, Keltern.
    [Google Scholar]
  53. Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J.. ( 1991;). 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697–703 [PubMed].
    [Google Scholar]
  54. Xue X., Li S.-J., Ahmed M.Z., De Barro P.J., Ren S.-X., Qiu B.L.. ( 2012;). Inactivation of Wolbachia reveals its biological roles in whitefly host. PLoS One 7: e48148 [CrossRef] [PubMed].
    [Google Scholar]
  55. Zchori-Fein E., Perlman S.J.. ( 2009;). Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:–2016 [CrossRef] [PubMed].
    [Google Scholar]
  56. Zhou W., Rousset F., O'Neill S.. ( 1998;). Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci 265: 509–515 [CrossRef] [PubMed].
    [Google Scholar]
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