Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-26T14:26:41.466Z Has data issue: false hasContentIssue false
  • English
  • Français

Symbiosis in an overlooked microcosm: a systematic review of the bacterial flora of mites

Published online by Cambridge University Press:  25 May 2015

KITTIPONG CHAISIRI ,
JOHN W. McGARRY ,
SERGE MORAND  and
BENJAMIN L. MAKEPEACE
KITTIPONG CHAISIRI
Affiliation:
Institute of Infection and Global Health, University of Liverpool, 146 Brownlow Hill, Liverpool L3 5RF, UK Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand
JOHN W. McGARRY
Affiliation:
School of Veterinary Science, University of Liverpool, 401 Great Newton Street, Liverpool L3 5RP, UK
SERGE MORAND
Affiliation:
CNRS CIRAD AGIRs, Centre d'Infectiologie Christophe Mérieux du Laos, Vientiane, Lao PDR
BENJAMIN L. MAKEPEACE*
Affiliation:
Institute of Infection and Global Health, University of Liverpool, 146 Brownlow Hill, Liverpool L3 5RF, UK
*
*Corresponding author. Institute of Infection and Global Health, University of Liverpool, 146 Brownlow Hill, Liverpool L3 5RF, UK. E-mail: blm1@liv.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

A dataset of bacterial diversity found in mites was compiled from 193 publications (from 1964 to January 2015). A total of 143 mite species belonging to the 3 orders (Mesostigmata, Sarcoptiformes and Trombidiformes) were recorded and found to be associated with approximately 150 bacteria species (in 85 genera, 51 families, 25 orders and 7 phyla). From the literature, the intracellular symbiont Cardinium, the scrub typhus agent Orientia, and Wolbachia (the most prevalent symbiont of arthropods) were the dominant mite-associated bacteria, with approximately 30 mite species infected each. Moreover, a number of bacteria of medical and veterinary importance were also reported from mites, including species from the genera Rickettsia, Anaplasma, Bartonella, Francisella, Coxiella, Borrelia, Salmonella, Erysipelothrix and Serratia. Significant differences in bacterial infection patterns among mite taxa were identified. These data will not only be useful for raising awareness of the potential for mites to transmit disease, but also enable a deeper understanding of the relationship of symbionts with their arthropod hosts, and may facilitate the development of intervention tools for disease vector control. This review provides a comprehensive overview of mite-associated bacteria and is a valuable reference database for future research on mites of agricultural, veterinary and/or medical importance.

Keywords

SymbiontsAcariallergyRickettsialesCardiniummicrobiota
Type
Review Article
Information
Parasitology , Volume 142 , Issue 9 , August 2015 , pp. 1152 - 1162
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arlian, L. G., Vyszenski-Moher, D. L. and Morgan, M. S. (2003). Mite and mite allergen removal during machine washing of laundry. Journal of Allergy and Clinical Immunology 111, 1269–1273.CrossRefGoogle ScholarPubMed
Baumann, P. (2005). Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review of Microbiology 59, 155–89.Google Scholar
Bitam, I. (2012). Vectors of rickettsiae in Africa. Ticks and Tick-borne Diseases 3, 381–385.CrossRefGoogle ScholarPubMed
Brännström, S., Hansson, I. and Chirico, J. (2010). Experimental study on possible transmission of the bacterium Erysipelothrix rhusiopathiae to chickens by the poultry red mite, Dermanyssus gallinae . Experimental and Applied Acarology 50, 299–307.CrossRefGoogle Scholar
Breeuwer, J. A. and Jacobs, G. (1996). Wolbachia: intracellular manipulators of mite reproduction. Experimental and Applied Acarology 20, 421–34.CrossRefGoogle ScholarPubMed
Brouqui, P. and Raoult, D. (2006). Arthropod-borne diseases in homeless. Annals of the New York Academy of Sciences 1078, 223–235.CrossRefGoogle ScholarPubMed
Chan, T. F., Ji, K. M., Yim, A. K., Liu, X. Y., Zhou, J. W., Li, R. Q., Yang, K. Y., Li, J., Li, M., Law, P. T., Wu, Y. L., Cai, Z. L., Qin, H., Bao, Y., Leung, R. K., Ng, P. K., Zou, J., Zhong, X. J., Ran, P. X., Zhong, N. S., Liu, Z. G. and Tsui, S. K. (2015). The draft genome, transcriptome, and microbiome of Dermatophagoides farinae reveal a broad spectrum of dust mite allergens. Journal of Allergy and Clinical Immunology 135, 539–548.Google Scholar
Chigira, A. and Miura, K. (2005). Detection of ‘Candidatus Cardinium’ bacteria from the haploid host Brevipalpus californicus (Acari: Tenuipalpidae) and effect on the host. Experimental and Applied Acarology 37, 107–116.CrossRefGoogle ScholarPubMed
Chirico, J., Eriksson, H., Fossum, O. and Jansson, D. (2003). The poultry red mite, Dermanyssus gallinae, a potential vector of Erysipelothrix rhusiopathiae causing erysipelas in hens. Medical and Veterinary Entomology 17, 232–234.CrossRefGoogle ScholarPubMed
Choi, Y. J., Lee, E. M., Park, J. M., Lee, K. M., Han, S. H., Kim, J. K., Lee, S. H., Song, H. J., Choi, M. S., Kim, I. S., Park, K. H. and Jang, W. J. (2007). Molecular detection of various rickettsiae in mites (Acari: Trombiculidae) in southern Jeolla Province, Korea. Microbiology and Immunology 51, 307–312.Google Scholar
Cottew, G. S. and Yeats, F. R. (1982). Mycoplasma and mites in the ears of clinically normal goats. Australian Veterinary Journal 59, 77–81.CrossRefGoogle ScholarPubMed
Crotti, E., Rizzi, A., Chouaia, B., Ricci, I., Favia, G., Alma, A., Sacchi, L., Bourtzis, K., Mandrioli, M., Cherif, A., Bandi, C. and Daffonchio, D. (2010). Acetic acid bacteria, newly emerging symbionts of insects. Applied and Environmental Microbiology 76, 6963–6970.Google Scholar
Di Blasi, E., Morse, S., Mayberry, J. R., Avila, L. J., Morando, M. and Dittmar, K. (2011). New Spiroplasma in parasitic Leptus mites and their Agathemera walking stick hosts from Argentina. Journal of Invertebrate Pathology 107, 225–228.Google Scholar
Dohany, A. L., Shirai, A., Robinson, D. M., Ram, S. and Huxsoll, D. L. (1978). Identification and antigenic typing of Rickettsia tsutsugamushi in naturally infected chiggers (Acarina: Trombiculidae) by direct immunofluorescence. The American Journal of Tropical Medicine and Hygiene 27, 1261–1264.Google Scholar
Dray, S. and Dufour, A. B. (2007). The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22, 1–20.Google Scholar
Duron, O., Hurst, G. D., Hornett, E. A., Josling, J. A. and Engelstadter, J. (2008). High incidence of the maternally inherited bacterium Cardinium in spiders. Molecular Ecology 17, 1427–1437.CrossRefGoogle ScholarPubMed
Enigl, M. and Schausberger, P. (2007). Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Experimental and Applied Acarology 42, 75–85.CrossRefGoogle ScholarPubMed
Fernandez-Soto, P., Perez-Sanchez, R. and Encinas-Grandes, A. (2001). Molecular detection of Ehrlichia phagocytophila genogroup organisms in larvae of Neotrombicula autumnalis (Acari: Trombiculidae) captured in Spain. Journal of Parasitology 87, 1482–1483.Google Scholar
Ferri, B. O., Barbuto, M., Martin, C., Lo, N., Uni, S., Landmann, F., Baccei, S. G., Guerrero, R., De Souza, L. S., Bandi, C., Wanji, S., Diagne, M. and Casiraghi, M. (2011). New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species. PLoS ONE 6, e20843.Google Scholar
Frances, S. P., Watcharapichat, P. and Phulsuksombati, D. (2001). Vertical transmission of Orientia tsutsugamushi in two lines of naturally infected Leptotrombidium deliense (Acari: Trombiculidae). Journal of Medical Entomology 38, 17–21.Google Scholar
Franzolin, M. R., Gambale, W., Cuero, R. G. and Correa, B. (1999). Interaction between toxigenic Aspergillus flavus Link and mites (Tyrophagus putrescentiae Schrank) on maize grains: effects on fungal growth and aflatoxin production. Journal of Stored Products Research 35, 215–224.Google Scholar
Giorgini, M., Monti, M. M., Caprio, E., Stouthamer, R. and Hunter, M. S. (2009). Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harboring the bacterial symbiont Cardinium . Heredity 102, 365–371.Google Scholar
Glowska, E., Dragun-Damian, A., Dabert, M. and Gerth, M. (2015). New Wolbachia supergroups detected in quill mites (Acari: Syringophilidae). Infection Genetics and Evolution 30, 140–146.CrossRefGoogle ScholarPubMed
Gotoh, T., Noda, H., Fujita, T., Iwadate, K., Higo, Y., Saito, S. and Ohtsuka, S. (2005). Wolbachia and nuclear-nuclear interactions contribute to reproductive incompatibility in the spider mite Panonychus mori (Acari: Tetranychidae). Heredity 94, 237–246.CrossRefGoogle Scholar
Gotoh, T., Noda, H. and Ito, S. (2007). Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98, 13–20.Google Scholar
Grabarev, P. A., Suroviatkin, A. V., Tikhonova, L., Mishchenko, O. A. and Potapenko, O. V. (2009). Experimental study of the inoculative transmission of Rickettsia typhi by gamasid mites (Gamasidae) Ornithonyssus bacoti . Meditsinskaia parazitologiia 2, 47–49.Google Scholar
Groot, T. V. and Breeuwer, J. A. (2006). Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species. Experimental and Applied Acarology 39, 257–271.Google Scholar
Gunduz, E. A. and Douglas, A. E. (2009) Symbiotic bacteria enable insect to utilise a nutritionally-inadequate diet. Proceedings of the Royal Society of London Series B-Biological Sciences 276, 987–991.Google Scholar
Halliday, R. B., O Connor, B. M. and Baker, A. S. (2000). Global diversity of mites. In Nature and Human Society: The Quest for a Sustainable World: Proceedings of the 1997 Forum on Biodiversity (ed. Raven, P. H. and Williams, T.), pp. 192–212. National Academy Press, Washington, DC.Google Scholar
Hogg, J. C. and Lehane, M. J. (1999). Identification of bacterial species associated with the sheep scab mite (Psoroptes ovis) by using amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 65, 4227–4229.CrossRefGoogle Scholar
Hogg, J. C. and Lehane, M. J. (2001). Microfloral diversity of cultured and wild strains of Psoroptes ovis infesting sheep. Parasitology 123, 441–446.CrossRefGoogle ScholarPubMed
Hong, X. Y., Gotoh, T. and Nagata, T. (2002). Vertical transmission of Wolbachia in Tetranychus kanzawai Kishida and Panonychus mori Yokoyama (Acari: Tetranychidae). Heredity 88, 190–196.Google Scholar
Hoy, M. A. and Jeyaprakash, A. (2005). Microbial diversity in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae) and its prey, Tetranychus urticae (Acari: Tetranychidae). Biological Control 32, 427–441.CrossRefGoogle Scholar
Hoy, M. A. and Jeyaprakash, A. (2008). Symbionts, including pathogens, of the predatory mite Metaseiulus occidentalis: current and future analysis methods. Experimental and Applied Acarology 46, 329–347.Google Scholar
Hubert, J., Stejskal, V., Munzbergova, Z., Kubatova, A., Vanova, M. and Zdarkova, E. (2004). Mites and fungi in heavily infested stores in the Czech Republic. Journal of Economic Entomology 97, 2144–2153.CrossRefGoogle ScholarPubMed
Hubert, J., Kopecky, J., Perotti, M. A., Nesvorna, M., Braig, H. R., Sagova-Mareckova, M., Macovei, L. and Zurek, L. (2012). Detection and identification of species-specific bacteria associated with synanthropic mites. Microbial Ecology 63, 919–928.Google Scholar
Hubert, J., Nesvorna, M., Kopecky, J., Sagova-Mareckova, M. and Poltronieri, P. (2014). Carpoglyphus lactis (Acari: Astigmata) from various dried fruits differed in associated micro-organisms. Journal of Applied Microbiology 118, 470–484.Google Scholar
Hugenholtz, P., Goebel, B. M. and Pace, N. R. (1998). Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. Journal of Bacteriology 180, 4765–4774.Google Scholar
Iturbe-Ormaetxe, I., Walker, T. and O’ Neill, S. L. (2011). Wolbachia and the biological control of mosquito-borne disease. EMBO Reports 12, 508–518.CrossRefGoogle ScholarPubMed
Jeffery, J. A., Thi, Y. N., Nam, V. S., Nghia, L. T., Hoffmann, A. A., Kay, B. H. and Ryan, P. A. (2009) Characterizing the Aedes aegypti population in a Vietnamese village in preparation for a Wolbachia-based mosquito control strategy to eliminate dengue. PLoS Neglected Tropical Diseases 3, e552.CrossRefGoogle Scholar
Jensenius, M., Fournier, P. E. and Raoult, D. (2004). Rickettsioses and the international traveller. Clinical Infectious Diseases 39, 1493–1499.Google Scholar
Kabeya, H., Colborn, J. M., Bai, Y., Lerdthusnee, K., Richardson, J. H., Maruyama, S. and Kosoy, M. Y. (2010). Detection of Bartonella tamiae DNA in ectoparasites from rodents in Thailand and their sequence similarity with bacterial cultures from Thai patients. Vector-Borne and Zoonotic Diseases 10, 429–434.CrossRefGoogle ScholarPubMed
Kamani, J., Morick, D., Mumcuoglu, K. Y. and Harrus, S. (2013). Prevalence and diversity of Bartonella species in commensal rodents and ectoparasites from Nigeria, West Africa. PLoS Neglected Tropical Diseases 7, e2246.Google Scholar
Kelly, D. J., Dasch, G. A., Chan, T. C. and Ho, T. M. (1994). Detection and characterization of Rickettsia tsutsugamushi (Rickettsiales: Rickettsiaceae) in infected Leptotrombidium (Leptotrombidium) fletcheri chiggers (Acari: Trombiculidae) with the polymerase chain reaction. Journal of Medical Entomology 31, 691–9.CrossRefGoogle ScholarPubMed
Kettle, D. S. (1984). In Medical and Veterinary Entomology, Mackays of Chatham Ltd, Bristol.Google Scholar
Khuntirat, B., Lerdthusnee, K., Leepitakrat, W., Kengluecha, A., Wongkalasin, K., Monkanna, T., Mungviriya, S., Jones, J. W. and Coleman, R. E. (2003). Characterization of Orientia tsutsugamushi isolated from wild-caught rodents and chiggers in Northern Thailand. Annals of the New York Academy of Sciences 990, 205–212.Google Scholar
Kitaoka, M., Asanuma, K. and Otsuji, J. (1974). Transmission of Rickettsia orientalis to man by Leptotrombidium akamushi at a scrub typhus endemic area in Akita Prefecture, Japan. The American Journal of Tropical Medicine and Hygiene 23, 993–999.Google Scholar
Kocianova, E. (1989). Nest ectoparasites (gamasid mites) as vectors for Rickettsia under experimental conditions. Trudy Instituta Imeni Pastera 66, 89–94.Google Scholar
Kopecky, J., Nesvorna, M. and Hubert, J. (2014). Bartonella-like bacteria carried by domestic mite species. Experimental and Applied Acarology 64, 21–32.Google Scholar
Kosoy, M., Morway, C., Sheff, K. W., Bai, Y., Colborn, J., Chalcraft, L., Dowell, S. F., Peruski, L. F., Maloney, S. A., Baggett, H., Sutthirattana, S., Sidhirat, A., Maruyama, S., Kabeya, H., Chomel, B. B., Kasten, R., Popov, V., Robinson, J., Kruglov, A. and Petersen, L. R. (2008). Bartonella tamiae sp. nov., a newly recognized pathogen isolated from three human patients from Thailand. Journal of Clinical Microbiology 46, 772–775.Google Scholar
Krantz, G. W. and Walter, D. E. (2009). A Manual of Acarology, 3rd Edn. Texas Tech University Press, Texas, 807pp.Google Scholar
Lee, H. I., Shim, S. K., Song, B. G., Choi, E. N., Hwang, K. J., Park, M. Y., Park, C. and Shin, E. H. (2011). Detection of Orientia tsutsugamushi, the causative agent of scrub typhus, in a novel mite species, Eushoengastia koreaensis, in Korea. Vector-Borne and Zoonotic Diseases 11, 209–214.CrossRefGoogle Scholar
Lerdthusnee, K., Khlaimanee, N., Monkanna, T., Sangjun, N., Mungviriya, S., Linthicum, K. J., Frances, S. P., Kollars, T. M. and Coleman, R. E. (2002). Efficiency of Leptotrombidium chiggers (Acari: Trombiculidae) at transmitting Orientia tsutsugamushi to laboratory mice. Journal of Medical Entomology 39, 521–525.CrossRefGoogle ScholarPubMed
Literak, I., Stekolnikov, A. A., Sychra, O., Dubska, L. and Taragelova, V. (2008). Larvae of chigger mites Neotrombicula spp. (Acari: Trombiculidae) exhibited Borrelia but no Anaplasma infections: a field study including birds from the Czech Carpathians as hosts of chiggers. Experimental and Applied Acarology 44, 307–314.Google Scholar
Liu, Y. X., Jia, N., Xing, Y. B., Suo, J. J., Du, M. M., Jia, N., Gao, Y., Xie, L. J., Liu, B. W. and Ren, S. W. (2013). Consistency of the key genotypes of Orientia tsutsugamushi in scrub typhus patients, rodents, and chiggers from a new endemic focus of Northern China. Cell Biochemistry and Biophysics 67, 1461–1466.Google Scholar
Lopatina, V., Vasileva, I. S., Gutova, V. P., Ershova, A. S., Burakova, O. V., Naumov, R. L. and Petrova, A. D. (1999). An experimental study of the capacity of the rat mite Ornithonyssus bacoti (Hirst, 1913) to ingest, maintain and transmit Borrelia . Meditsinskaia parazitologiia 2, 26–30.Google Scholar
Lu, M. H., Zhang, K. J. and Hong, X. Y. (2012). Tripartite associations among bacteriophage WO, Wolbachia, and host affected by temperature and age in Tetranychus urticae . Experimental and Applied Acarology 58, 207–220.Google Scholar
Lysy, J., Nosek, J., Vyrostekova, V. and Kovacik, J. (1979). Isolation of Francisella tularensis from mites Haemogamasus nidi and Laelaps hilaris in Western Slovakia. Zentralbl Bakteriol Orig A 244, 324–326.Google Scholar
Martin, O. Y., Gubler, A., Wimmer, C., Germann, C. and Bernasconi, M. V. (2012). Infections with Wolbachia and Spiroplasma in the Scathophagidae and other Muscoidea. Infection Genetics and Evolution 12, 315–323.Google Scholar
Martinson, V. G., Danforth, B. N., Minckley, R. L., Rueppell, O., Tingek, S. and Moran, N. A. (2011). A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology 20, 619–628.Google Scholar
Mathieson, B. R. F. and Lehane, M. J. (1996). Isolation of the Gram-negative bacterium, Serratia marcescens, from the sheep scab mite, Psoroptes ovis . Veterinary Record 138, 210–211.Google Scholar
Murillo, N., Aubert, J. and Raoult, D. (2014). Microbiota of Demodex mites from rosacea patients and controls. Microbial Pathogenesis 71–72, 37–40.Google Scholar
Netusil, J., Zakovska, A., Horvath, R., Dendis, M. and Janouskovcova, E. (2005). Presence of Borrelia burgdorferi sensu lato in mites parasitizing small rodents. Vector-borne and Zoonotic Diseases 5, 227–232.Google Scholar
Netusil, J., Zakovska, A., Vostal, K., Norek, A. and Stanko, M. (2013). The occurrence of Borrelia burgdorferi sensu lato in certain ectoparasites (Mesostigmata, Siphonaptera) of Apodemus flavicollis and Myodes glareolus in chosen localities in the Czech Republic. Acta Parasitologica 58, 337–341.Google Scholar
Novelli, V. M., Freitas-Astua, J., Segatti, N., Mineiro, J. L. C., Arthur, V., Bastianel, M., Hilf, M. E., Gottwald, T. R. and Machado, M. A. (2008). Effects of radiation (Cobalt-60) on the elimination of Brevipalpus phoenicis (Acari: Tenuipalpidae) Cardinium endosymbiont. Experimental and Applied Acarology 45, 147–153.CrossRefGoogle ScholarPubMed
Perrucci, S., Rossi, G., Fichi, G. and O'Brien, D. J. (2005). Relationship between Psoroptes cuniculi and the internal bacterium Serratia marcescens . Experimental and Applied Acarology 36, 199–206.CrossRefGoogle ScholarPubMed
Petrov, V. G. (1971). On the role of mite Ornithonyssus bacoti. Hirst in the preservation of the causal agent of tularemia and transmission to white mice. Parazitologiia 5, 7–14.Google Scholar
Pham, X. D., Otsuka, Y., Suzuki, H. and Takaoka, H. (2001). Detection of Orientia tsutsugamushi (Rickettsiales: rickettsiaceae) in unengorged chiggers (Acari: Trombiculidae) from Oita Prefecture, Japan, by nested polymerase chain reaction. Journal of Medical Entomology 38, 308–311.CrossRefGoogle ScholarPubMed
Phasomkusolsil, S., Tanskul, P., Ratanatham, S., Watcharapichat, P., Phulsuksombati, D., Frances, S. P., Lerdthusnee, K. and Linthicum, K. J. (2009). Transstadial and transovarial transmission of Orientia tsutsugamushi in Leptotrombidium imphalum and Leptotrombidium chiangraiensis (Acari: Trombiculidae). Journal of Medical Entomology 46, 1442–1445.Google Scholar
Phasomkusolsil, S., Tanskul, P., Ratanatham, S., Watcharapichat, P., Phulsuksombati, D., Frances, S. P., Lerdthusnee, K. and Linthicum, K. J. (2012). Influence of Orientia tsutsugamushi infection on the developmental biology of Leptotrombidium imphalum and Leptotrombidium chiangraiensis (Acari: Trombiculidae). Journal of Medical Entomology 49, 1270–1275.Google Scholar
Pukall, R., Schumann, P., Schutte, C., Gols, R. and Dicke, M. (2006). Acaricomes phytoseiuli gen. nov., sp. nov., isolated from the predatory mite Phytoseiulus persimilis . International Journal of Systematic and Evolutionary Microbiology 56, 465–469.Google Scholar
R Development Core Team. (2008). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.Google Scholar
Ree, H. I., Lee, I. Y. and Cho, M. K. (1992). Study on vector mites of tsutsugamushi disease in Cheju Island, Korea. Kisaengchunghak Chapchi 30, 341–348.Google Scholar
Reeves, W. K., Dowling, A. P. and Dasch, G. A. (2006). Rickettsial agents from parasitic Dermanyssoidea (Acari: Mesostigmata). Experimental and Applied Acarology 38, 181–188.CrossRefGoogle ScholarPubMed
Reeves, W. K., Loftis, A. D., Szumlas, D. E., Abbassy, M. M., Helmy, I. M., Hanafi, H. A. and Dasch, G. A. (2007). Rickettsial pathogens in the tropical rat mite Ornithonyssus bacoti (Acari: Macronyssidae) from Egyptian rats (Rattus spp.). Experimental and Applied Acarology 41, 101–107.Google Scholar
Rivera, A., Cedillo, L., Hernandez, F., Romero, O. and Hernandez, M. A. (2013). Spiroplasma infectious agents of plants. European Journal of Experimental Biology 3, 583–591.Google Scholar
Roberts, L. W., Muul, I. and Robinson, D. M. (1977). Numbers of Leptotrombidium (Leptotrombidium) deliense (Acarina: Trombiculidae) and prevalence of Rickettsia tsutsugamushi in adjacent habitats of peninsular Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 8, 207–213.Google ScholarPubMed
Ros, V. D., Fleming, V. M., Feil, E. J. and Breeuwer, J. A. (2012). Diversity and recombination in Wolbachia and Cardinium from Bryobia spider mites. BMC Microbiology 12(Suppl 1), S13.CrossRefGoogle ScholarPubMed
Scarborough, C. L., Ferrari, J. and Godfray, H. C. J. (2005). Aphid protected from pathogen by endosymbiont. Science 310, 1781.Google Scholar
Schütte, C. and Dicke, M. (2008). Verified and potential pathogens of predatory mites (Acari: Phytoseiidae). Experimental and Applied Acarology 46, 307–328.Google Scholar
Schütte, C., Gols, R., Kleespies, R. G., Poitevin, O. and Dicke, M. (2008). Novel bacterial pathogen Acaricomes phytoseiuli causes severe disease symptoms and histopathological changes in the predatory mite Phytoseiulus persimilis (Acari, Phytoseiidae). Journal of Invertebrate Pathology 98, 127–135.Google Scholar
Seto, J., Suzuki, Y., Otani, K., Qiu, Y., Nakao, R., Sugimoto, C. and Abiko, C. (2013). Proposed vector candidate: Leptotrombidium palpale for Shimokoshi-type Orientia tsutsugamushi . Microbiology and Immunology 57, 111–117.Google Scholar
Shah, D. H., Lee, M. J., Park, J. H., Lee, J. H., Eo, S. K., Kwon, J. T. and Chae, J. S. (2005). Identification of Salmonella gallinarum virulence genes in a chicken infection model using PCR-based signature-tagged mutagenesis. Microbiology 151, 3957–3968.CrossRefGoogle Scholar
Shin, E. H., Roh, J. Y., Park, W. I., Song, B. G., Chang, K. S., Lee, W. G., Lee, H. I., Park, C., Park, M. Y. and Shin, E. (2014). Transovarial transmission of Orientia tsutsugamushi in Leptotrombidium palpale (Acari: Trombiculidae). PLoS ONE 9, e88453.Google Scholar
Shirai, A., Huxsoll, D. L., Dohany, A. L., Montrey, R. D., Werner, R. M. and Gan, E. (1982). Characterization of Rickettsia tsutsugamushi strains in two species of naturally infected, laboratory reared chiggers. The American Journal of Tropical Medicine and Hygiene 31, 395–402.CrossRefGoogle ScholarPubMed
Skaljac, M., Zanic, K., Hrncic, S., Radonjic, S., Perovic, T. and Ghanim, M. (2013). Diversity and localization of bacterial symbionts in three whitefly species (Hemiptera: Aleyrodidae) from the east coast of the Adriatic Sea. Bulletin of Entomological Research 103, 48–59.Google Scholar
Sonesson, A., Bartosik, J., Christiansen, J., Roscher, I., Nilsson, F., Schmidtchen, A. and Back, O. (2013). Sensitization to skin-associated microorganisms in adult patients with atopic dermatitis is of importance for disease severity. Acta Dermato-Venereologica 93, 340–345.Google Scholar
Stouthamer, R., Breeuwer, J. A. J. and Hurst, G. D. D. (1999). Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Review of Microbiology 53, 71–102.Google Scholar
Suh, E., Sim, C., Park, J. and Cho, K. (2014). Inter-population variation for Wolbachia induced reproductive incompatibility in the haplodiploid mite Tetranychus urticae . Experimental and Applied Acarology 65, 55–71.Google Scholar
Takahashi, T., Takagi, M., Yamamoto, K. and Nakamura, M. (2000). A serological survey on erysipelas in chickens by growth agglutination test. Journal of Veterinary Medicine B, Infectious Diseases and Veterinary Public Health 47, 797–9.Google Scholar
Takhampunya, R., Tippayachai, B., Promsathaporn, S., Leepitakrat, S., Monkanna, T., Schuster, A. L., Melendrez, M. C., Paris, D. H., Richards, A. L. and Richardson, J. H. (2014). Characterization based on the 56-kDa type-specific antigen gene of Orientia tsutsugamushi genotypes isolated from Leptotrombidium mites and the rodent host post-infection. The American Journal of Tropical Medicine and Hygiene 90, 139–146.CrossRefGoogle ScholarPubMed
Tamura, A., Makisaka, Y., Kadosaka, T., Enatsu, T., Okubo, K., Koyama, S., Yu, Q. and Urakami, H. (2000). Isolation of Orientia tsutsugamushi from Leptotrombidium fuji and its characterization. Microbiology and Immunology 44, 201–204.Google Scholar
Tang, V. H., Chang, B. J., Srinivasan, A., Mathaba, L. T., Harnett, G. B. and Stewart, G. A. (2013). Skin-associated Bacillus, staphylococcal and micrococcal species from the house dust mite, Dermatophagoides pteronyssinus and bacteriolytic enzymes. Experimental and Applied Acarology 61, 431–47.CrossRefGoogle ScholarPubMed
Taylor, G. P., Coghlin, P. C., Floate, K. D. and Perlman, S. J. (2011). The host range of the male-killing symbiont Arsenophonus nasoniae in filth fly parasitoids. Journal of Invertebrate Pathology 106, 371–379.Google Scholar
Thepparit, C., Sunyakumthorn, P., Guillotte, M. L., Popov, V. L., Foil, L. D. and Macaluso, K. R. (2011). Isolation of a rickettsial pathogen from a non-hematophagous arthropod. Plos ONE 6, e16396.Google Scholar
Tilak, R., Kunwar, R., Wankhade, U. B. and Tilak, V. W. (2011). Emergence of Schoengastiella ligula as the vector of scrub typhus outbreak in Darjeeling: has Leptotrombidium deliense been replaced? Indian Journal of Public Health 55, 92–99.CrossRefGoogle ScholarPubMed
Timofeeva, G. Y. (1964). Experimental study of the transmission and harbouring of the tularaemia agent by the mite Hirstonysus musculi Johnst. Medskaya Parazitology 33, 184–187.Google Scholar
Tinsley, M. C. and Majerus, M. E. N. (2006). A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132, 757–765.Google Scholar
Tsui, P. Y., Tsai, K. H., Weng, M. H., Hung, Y. W., Liu, Y. T., Hu, K. Y., Lien, J. C., Lin, P. R., Shaio, M. F., Wang, H. C. and Ji, D. D. (2007). Molecular detection and characterization of spotted fever group rickettsiae in Taiwan. The American Journal of Tropical Medicine and Hygiene 77, 883–890.Google Scholar
Urakami, H., Tamura, A., Tarasevich, I. V., Kadosaka, T. and Shubin, F. N. (1999). Decreased prevalence of Orientia tsutsugamushi in trombiculid mites and wild rodents in the Primorye region, Far East Russia. Microbiology and Immunology 43, 975–978.Google Scholar
Valiente-Moro, C., De Luna, C. J., Tod, A., Guy, J. H., Sparagano, O. A. E. and Zenner, L. (2009a). The poultry red mite (Dermanyssus gallinae): a potential vector of pathogenic agents. Experimental and Applied Acarology 48, 93–104.Google Scholar
Valiente-Moro, C., Thioulouse, J., Chauve, C., Normand, P. and Zenner, L. (2009b). Bacterial taxa associated with the hematophagous mite Dermanyssus gallinae detected by 16S rRNA PCR amplification and TTGE fingerprinting. Research in Microbiology 160, 63–70.CrossRefGoogle ScholarPubMed
Valiente-Moro, C., Thioulouse, J., Chauve, C. and Zenner, L. (2011). Diversity, geographic distribution, and habitat-specific variations of microbiota in natural populations of the chicken mite, Dermanyssus gallinae . Journal of Medical Entomology 48, 788–796.Google Scholar
Wales, A. D., Carrique-Mas, J. J., Rankin, M., Bell, B., Thind, B. B. and Davies, R. H. (2010). Review of the carriage of zoonotic bacteria by arthropods, with special reference to Salmonella in mites, flies and litter beetles. Zoonoses and Public Health 57, 299–314.Google Scholar
Weeks, A. R. and Breeuwer, J. A. (2001). Wolbachia-induced parthenogenesis in a genus of phytophagous mites. Proceedings of the Royal Society B: Biological Sciences 268, 2245–2251.Google Scholar
Weeks, A. R., Velten, R. and Stouthamer, R. (2003). Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proceedings of the Royal Society B: Biological Sciences 270, 1857–1865.Google Scholar
Yu, M. Z., Zhang, K. J., Xue, X. F. and Hong, X. Y. (2011). Effects of Wolbachia on mtDNA variation and evolution in natural populations of Tetranychus urticae Koch. Insect Molecular Biology 20, 311–321.Google Scholar
Yun, J. H., Roh, S. W., Whon, T. W., Jung, M. J., Kim, M. S., Park, D. S., Yoon, C., Nam, Y. D., Kim, Y. J., Choi, J. H., Kim, J. Y., Shin, N. R., Kim, S. H., Lee, W. J. and Baea, J. W. (2014). Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied and Environmental Microbiology 80, 5254–5264.Google Scholar
Zeman, P., Stika, V., Skalka, B., Bartik, M., Dusbabek, F. and Lavickova, M. (1982). Potential role of Dermanyssus gallinae De Geer, 1778 in the circulation of the agent of pullurosis-typhus in hens. Folia Parasitology (Praha) 29, 371–374.Google Scholar
Zemskaya, A. A. and Pchelnika, A. A. (1968). On the infection of various species of Gamasidae mites with Rickettsia burnetii in natural foci of Q fever. Zhurnal Mikrobiologii Epidemiologii I Immunobiologii 45, 130–132.Google Scholar
Zhang, Y. K., Ding, X. L., Rong, X. and Hong, X. Y. (2015). How do hosts react to endosymbionts? A new insight into the molecular mechanisms underlying the Wolbachia–host association. Insect Molecular Biology 24, 1–12.Google Scholar
Zhao, D. X., Chen, D. S., Ge, C., Gotoh, T. and Hong, X. Y. (2013 a). Multiple infections with Cardinium and two strains of Wolbachia in the spider mite Tetranychus phaselus Ehara: revealing new forces driving the spread of Wolbachia . PLoS ONE 8, e54964.Google Scholar
Zhao, D. X., Zhang, X. F. and Hong, X. Y. (2013 b). Host–symbiont interactions in spider mite Tetranychus truncates doubly infected with Wolbachia and Cardinium . Environmental Entomology 42, 445–452.Google Scholar
Zhu, L. Y., Zhang, K. J., Zhang, Y. K., Ge, C., Gotoh, T. and Hong, X. Y. (2012). Wolbachia strengthens Cardinium-induced cytoplasmic incompatibility in the spider mite Tetranychus piercei McGregor. Current Microbiology 65, 516–523.CrossRefGoogle ScholarPubMed
Zindel, R., Ofek, M., Minz, D., Palevsky, E., Zchori-Fein, E. and Aebi, A. (2013). The role of the bacterial community in the nutritional ecology of the bulb mite Rhizoglyphus robini (Acari: Astigmata: Acaridae). The FASEB Journal 27, 1488–1497.Google Scholar
Zucchi, T. D., Prado, S. S. and Consoli, F. L. (2012). The gastric caeca of pentatomids as a house for Actinomycetes. BMC Microbiology 12, 101.Google Scholar
Zuevskii, A. P. (1976). Role of gamasids in the epizootiology of tularemia. Parazitologiia 10, 531–5.Google Scholar
Zug, R. and Hammerstein, P. (2012). Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE 7, e38544.Google Scholar
Supplementary material: PDF

Chaisiri supplementary material

Table S1

Download Chaisiri supplementary material(PDF)
PDF 179.6 KB
Supplementary material: PDF

Chaisiri supplementary material

Table S2

Download Chaisiri supplementary material(PDF)
PDF 435.1 KB
Supplementary material: File

Chaisiri supplementary material

Table S3

Download Chaisiri supplementary material(File)
File 46.6 KB