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Comparison of Microbiomes between Red Poultry Mite Populations (Dermanyssus gallinae): Predominance of Bartonella-like Bacteria

  • Invertebrate Microbiology
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Abstract

Blood feeding red poultry mites (RPM) serve as vectors of pathogenic bacteria and viruses among vertebrate hosts including wild birds, poultry hens, mammals, and humans. The microbiome of RPM has not yet been studied by high-throughput sequencing. RPM eggs, larvae, and engorged adult/nymph samples obtained in four poultry houses in Czechia were used for microbiome analyses by Illumina amplicon sequencing of the 16S ribosomal RNA (rRNA) gene V4 region. A laboratory RPM population was used as positive control for transcriptome analysis by pyrosequencing with identification of sequences originating from bacteria. The samples of engorged adult/nymph stages had 100-fold more copies of 16S rRNA gene copies than the samples of eggs and larvae. The microbiome composition showed differences among the four poultry houses and among observed developmental stadia. In the adults’ microbiome 10 OTUs comprised 90 to 99% of all sequences. Bartonella-like bacteria covered between 30 and 70% of sequences in RPM microbiome and 25% bacterial sequences in transcriptome. The phylogenetic analyses of 16S rRNA gene sequences revealed two distinct groups of Bartonella-like bacteria forming sister groups: (i) symbionts of ants; (ii) Bartonella genus. Cardinium, Wolbachia, and Rickettsiella sp. were found in the microbiomes of all tested stadia, while Spiroplasma eriocheiris and Wolbachia were identified in the laboratory RPM transcriptome. The microbiomes from eggs, larvae, and engorged adults/nymphs differed. Bartonella-like symbionts were found in all stadia and sampling sites. Bartonella-like bacteria was the most diversified group within the RPM microbiome. The presence of identified putative pathogenic bacteria is relevant with respect to human and animal health issues while the identification of symbiontic bacteria can lead to new control methods targeting them to destabilize the arthropod host.

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References

  1. Pritchard J, Kuster T, Sparagano O, Tomley F (2015) Understanding the biology and control of the poultry red mite Dermanyssus gallinae: a review. Avian Pathol 44:143–153. doi:10.1080/03079457.2015.1030589

    Article  PubMed  Google Scholar 

  2. Lucky AW, Sayers CP, Argus JD, Lucky A (2001) Avian mite bites acquired from a new source—pet gerbils: report of 2 cases and review of the literature. Arch Dermatol 137:167–170. doi:10.1001/pubs.Arch Dermatol.-ISSN-0003-987x-137-2-dob00013

    CAS  PubMed  Google Scholar 

  3. Cafiero MA, Camarda A, Circella E, Santagada G, Schino G, Lomuto M (2008) Pseudoscabies caused by Dermanyssus gallinae in Italian city dwellers: a new setting for an old dermatitis. J Eur Acad Dermatol Venereol 22:1382–1383. doi:10.1111/j.1468-3083.2008.02645.x

    Article  CAS  PubMed  Google Scholar 

  4. Sparagano OAE, George DR, Harrington DWJ, Giangaspero A (2014) Significance and control of the poultry red mite, Dermanyssus gallinae. Annu Rev Entomol 59:447–466. doi:10.1146/annurev-ento-011613-162101

    Article  CAS  PubMed  Google Scholar 

  5. Moro CV, De Luna CJ, Tod A, Guy JH, Sparagano OAE, Zenner L (2009) The poultry red mite (Dermanyssus gallinae): a potential vector of pathogenic agents. Exp Appl Acarol 48:93–104. doi:10.1007/s10493-009-9248-0

    Article  Google Scholar 

  6. Moro CV, Fravalo P, Amelot M, Chauve C, Zenner L, Salvat G (2007) Colonization and organ invasion in chicks experimentally infected with Dermanyssus gallinae contaminated by Salmonella enteritidis. Avian Pathol 36:307–311. doi:10.1080/03079450701460484

    Article  PubMed  Google Scholar 

  7. Moro CV, Thioulouse J, Chauve C, Normand P, Zenner L (2009) Bacterial taxa associated with the hematophagous mite Dermanyssus gallinae detected by 16S rRNA PCR amplification and TTGE fingerprinting. Res Microbiol 160:63–70. doi:10.1016/j.resmic.2008.10.006

    Article  Google Scholar 

  8. Rasmussen M (2016) Aerococcus: an increasingly acknowledged human pathogen. Clin Microbiol Infect 22:22–27. doi:10.1016/j.cmi.2015.09.026

    Article  CAS  PubMed  Google Scholar 

  9. De Luna CJ, Arkle S, Harrington D, George DR, Guy JH, Sparagano OAE (2008) The poultry red mite Dermanyssus gallinae as a potential carrier of vector-borne diseases. Ann N Y Acad Sci 1149:255–258. doi:10.1196/annals.1428.085

    Article  PubMed  Google Scholar 

  10. Huong CTT, Murano T, Uno Y, Usui T, Yamaguchi T (2014) Molecular detection of avian pathogens in poultry red mite (Dermanyssus gallinae) collected in chicken farms. J Vet Med Sci 76:1583–1587. doi:10.1292/jvms.14-0253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Circella E, Pugliese N, Todisco G, Cafiero MA, Sparagano OAE, Camarda A (2011) Chlamydia psittaci infection in canaries heavily infested by Dermanyssus gallinae. Exp Appl Acarol 55:329–338. doi:10.1007/s10493-011-9478-9

    Article  PubMed  Google Scholar 

  12. De Luna CJ, Moro CV, Guy JH, Zenner L, Sparagano OAE (2009) Endosymbiotic bacteria living inside the poultry red mite (Dermanyssus gallinae). Exp Appl Acarol 48:105–113. doi:10.1007/s10493-008-9230-2

    Article  PubMed  Google Scholar 

  13. Hodkinson BP, Grice EA (2015) Next-generation sequencing: a review of technologies and tools for wound microbiome research. Adv Wound Care (New Rochelle) 4:50–58. doi:10.1089/wound.2014.0542

    Article  Google Scholar 

  14. Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145. doi:10.1038/nbt1486

    Article  CAS  PubMed  Google Scholar 

  15. Mul M, van Niekerk T, Chirico J, Maurer V, Kilpinen O, Sparagano O, Thind B, Zoons J, Moore D, Bell B, Gjevre A-G, Chauve C (2009) Control methods for Dermanyssus gallinae in systems for laying hens: results of an international seminar. World Poultry Sci J 65:589–599. doi:10.1017/S0043933909000403

    Article  Google Scholar 

  16. Schicht S, Qi W, Poveda L, Strube C (2014) Whole transcriptome analysis of the poultry red mite Dermanyssus gallinae (de Geer, 1778). Parasitology 141:336–346. doi:10.1017/S0031182013001467

    Article  CAS  PubMed  Google Scholar 

  17. Hubert J, Erban T, Kamler M, Kopecky J, Nesvorna M, Hejdankova S, Titera D, Tyl J, Zurek L (2015) Bacteria detected in the honeybee parasitic mite Varroa destructor collected from beehive winter debris. J Appl Microbiol 119:640–654. doi:10.1111/jam.12899

    Article  CAS  PubMed  Google Scholar 

  18. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, pp. 115–175

    Google Scholar 

  19. Kopecky J, Perotti MA, Nesvorna M, Erban T, Hubert J (2013) Cardinium endosymbionts are widespread in synanthropic mite species (Acari: Astigmata). J Invertebr Pathol 112:20–23. doi:10.1016/j.jip.2012.11.001

    Article  CAS  PubMed  Google Scholar 

  20. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736. doi:10.1128/AEM.71.12.7724-7736.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741. doi:10.1128/AEM.00556-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. doi:10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  23. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi:10.1128/AEM.00062-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Pruesse E, Peplies J, Glockner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829. doi:10.1093/bioinformatics/bts252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi:10.1080/10635150390235520

    Article  PubMed  Google Scholar 

  27. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772. doi:10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Rodrigue N, Lartillot N (2014) Site-heterogeneous mutation-selection models within the PhyloBayes-MPI package. Bioinformatics 30:1020–1021. doi:10.1093/bioinformatics/btt729

    Article  CAS  PubMed  Google Scholar 

  29. Jow H, Hudelot C, Rattray M, Higgs PG (2002) Bayesian phylogenetics using an RNA substitution model applied to early mammalian evolution. Mol Biol Evol 19:1591–1601. doi:10.1093/oxfordjournals.molbev.a004221

    Article  CAS  PubMed  Google Scholar 

  30. Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:2286–2288. doi:10.1093/bioinformatics/btp368

    Article  CAS  PubMed  Google Scholar 

  31. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  32. Rambaut A (2007) FigTree, a graphical viewer of phylogenetic trees. Molecular evolution, phylogenetics and epidemiology: research, software and publications of Andrew Rambaut and members of his research group. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 27 July 2015

  33. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi:10.1038/ismej.2012.8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Aizenberg-Gershtein Y, Izhaki I, Santhanam R, Kumar P, Baldwin IT, Halpern M (2015) Pyridine-type alkaloid composition affects bacterial community composition of floral nectar. Sci Rep 5:11536. doi:10.1038/srep11536

    Article  PubMed  PubMed Central  Google Scholar 

  35. Earley ZM, Akhtar S, Green SJ, Naqib A, Khan O, Cannon AR, Hammer AM, Morris NL, Li X, Eberhardt JM, Gamelli RL, Kennedy RH, Choudhry MA (2015) Burn injury alters the intestinal microbiome and increases gut permeability and bacterial translocation. PLoS One 10:e0129996. doi:10.1371/journal.pone.0129996

    Article  PubMed  PubMed Central  Google Scholar 

  36. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642. doi:10.1093/nar/gkt1244

    Article  CAS  PubMed  Google Scholar 

  37. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. doi:10.1128/AEM.01043-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:4 http://palaeo-electronica.org/2001_1/past/issue1_01.htm. Accessed 6 August 2016

    Google Scholar 

  40. Ondov BD, Bergman NH, Phillippy AM (2011) Interactive metagenomic visualization in a web browser. BMC Bioinformatics 12:385. doi:10.1186/1471-2105-12-385

    Article  PubMed  PubMed Central  Google Scholar 

  41. Erban T, Ledvinka O, Nesvorna M, Hubert J (2017) Experimental manipulation shows a greater influence of population than dietary perturbation on the microbiome of Tyrophagus putrescentiae. Appl Environ Microbiol 83. doi:10.1128/AEM.00128-17

  42. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2016. vegan: Community Ecology Package. CRAN - The Comprehensive R Archive Network. http://CRAN.R-project.org/package=vegan. Accessed 6 August 2016

  43. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2016) gplots: Various R programming tools for plotting data. CRAN - The Comprehensive R Archive Network. https://CRAN.R-project.org/package=gplots. Accessed 6 August 2016

  44. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. doi:10.1111/j.1461-0248.2006.00926.x

    Article  PubMed  Google Scholar 

  45. White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5:e1000352. doi:10.1371/journal.pcbi.1000352

    Article  PubMed  PubMed Central  Google Scholar 

  46. Dorn-In S, Bassitta R, Schwaiger K, Bauer J, Holzel CS (2015) Specific amplification of bacterial DNA by optimized so-called universal bacterial primers in samples rich of plant DNA. J Microbiol Methods 113:50–56. doi:10.1016/j.mimet.2015.04.001

    Article  CAS  PubMed  Google Scholar 

  47. Hubert J, Kopecky J, Nesvorna M, Perotti MA, Erban T (2016) Detection and localization of Solitalea-like and Cardinium bacteria in three Acarus siro populations (Astigmata: Acaridae). Exp Appl Acarol 70:309–327. doi:10.1007/s10493-016-0080-z

  48. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. doi:10.1093/bioinformatics/bti610

    Article  CAS  PubMed  Google Scholar 

  49. Duron O (2013) Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts. Heredity 111:330–337. doi:10.1038/hdy.2013.56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Matsuura Y, Kikuchi Y, Meng XY, Koga R, Fukatsu T (2012) Novel clade of alphaproteobacterial endosymbionts associated with stinkbugs and other arthropods. Appl Environ Microbiol 78:4149–4156. doi:10.1128/AEM.00673-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE (2009) Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci U S A 106:21236–21241. doi:10.1073/pnas.0907926106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Anderson KE, Russell JA, Moreau CS, Kautz S, Sullam KE, Hu Y, Basinger U, Mott BM, Buck N, Wheeler DE (2012) Highly similar microbial communities are shared among related and trophically similar ant species. Mol Ecol 21:2282–2296. doi:10.1111/j.1365-294X.2011.05464.x

    Article  PubMed  Google Scholar 

  53. Hu Y, Lukasik P, Moreau CS, Russell JA (2014) Correlates of gut community composition across an ant species (Cephalotes varians) elucidate causes and consequences of symbiotic variability. Mol Ecol 23:1284–1300. doi:10.1111/mec.12607

    Article  PubMed  Google Scholar 

  54. Bonasio R, Zhang G, Ye C, Mutti NS, Fang X, Qin N, Donahue G, Yang P, Li Q, Li C, Zhang P, Huang Z, Berger SL, Reinberg D, Wang J, Liebig J (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329:1068–1071. doi:10.1126/science.1192428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Stoll S, Gadau J, Gross R, Feldhaar H (2007) Bacterial microbiota associated with ants of the genus Tetraponera. Biol J Linn Soc 90:399–412. doi:10.1111/j.1095-8312.2006.00730.x

    Article  Google Scholar 

  56. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 20:619–628. doi:10.1111/j.1365-294X.2010.04959.x

    Article  PubMed  Google Scholar 

  57. Kesnerova L, Moritz R, Engel P (2016) Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. Int J Syst Evol Microbiol 66:414–421. doi:10.1099/ijsem.0.000736

    Article  CAS  PubMed  Google Scholar 

  58. Hubert J, Kopecky J, Perotti MA, Nesvorna M, Braig HR, Sagova-Mareckova M, Macovei L, Zurek L (2012) Detection and identification of species-specific bacteria associated with synanthropic mites. Microb Ecol 63:919–928. doi:10.1007/s00248-011-9969-6

    Article  CAS  PubMed  Google Scholar 

  59. Hubert J, Nesvorna M, Kopecky J, Sagova-Mareckova M, Poltronieri P (2015) Carpoglyphus lactis (Acari: Astigmata) from various dried fruits differed in associated micro-organisms. J Appl Microbiol 118:470–484. doi:10.1111/jam.12714

    Article  CAS  PubMed  Google Scholar 

  60. Kopecky J, Nesvorna M, Hubert J (2014) Bartonella-like bacteria carried by domestic mite species. Exp Appl Acarol 64:21–32. doi:10.1007/s10493-014-9811-1

    Article  CAS  PubMed  Google Scholar 

  61. Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, Nomicos E, Polley EC, Komarow HD, Comparative Sequence Program NISC, Murray PR, Turner ML, Segre JA (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859. doi:10.1101/gr.131029.111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Tsuchida T, Koga R, Fujiwara A, Fukatsu T (2014) Phenotypic effect of “Candidatus Rickettsiella viridis,” a facultative symbiont of the pea aphid (Acyrthosiphon pisum), and its interaction with a coexisting symbiont. Appl Environ Microbiol 80:525–533. doi:10.1128/AEM.03049-13

    Article  PubMed  PubMed Central  Google Scholar 

  63. Lukasik P, van Asch M, Guo H, Ferrari J, Godfray HCJ (2013) Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett 16:214–218. doi:10.1111/ele.12031

    Article  PubMed  Google Scholar 

  64. Moquin SA, Garcia JR, Brantley SL, Takacs-Vesbach CD, Shepherd UL (2012) Bacterial diversity of bryophyte-dominant biological soil crusts and associated mites. J Arid Environ 87:110–117. doi:10.1016/j.jaridenv.2012.05.004

    Article  Google Scholar 

  65. Moro CV, Thioulouse J, Chauve C, Zenner L (2011) Diversity, geographic distribution, and habitat-specific variations of microbiota in natural populations of the chicken mite, Dermanyssus gallinae. J Med Entomol 48:788–796. doi:10.1603/ME10113

    Article  PubMed  Google Scholar 

  66. Erban T, Klimov PB, Smrz J, Phillips TW, Nesvorna M, Kopecky J, Hubert J (2016) Populations of stored product mite Tyrophagus putrescentiae differ in their bacterial communities. Front Microbiol 7:1046. doi:10.3389/fmicb.2016.01046

    Article  PubMed  PubMed Central  Google Scholar 

  67. Hubert J, Kopecky J, Sagova-Mareckova M, Nesvorna M, Zurek L, Erban T (2016) Assessment of bacterial communities in thirteen species of laboratory-cultured domestic mites (Acari: Acaridida). J Econ Entomol 109:1887–1896. doi:10.1093/jee/tow089

    Article  PubMed  Google Scholar 

  68. Regier Y, O’Rourke F, Kempf VA (2016) Bartonella spp.—a chance to establish one health concepts in veterinary and human medicine. Parasit Vectors 9:261. doi:10.1186/s13071-016-1546-x

    Article  PubMed  PubMed Central  Google Scholar 

  69. Reeves WK, Dowling APG, Dasch GA (2006) Rickettsial agents from parasitic Dermanyssoidea (Acari: Mesostigmata). Exp Appl Acarol 38:181–188. doi:10.1007/s10493-006-0007-1

    Article  PubMed  Google Scholar 

  70. Klangthong K, Promsthaporn S, Leepitakrat S, Schuster AL, McCardle PW, Kosoy M, Takhampunya R (2015) The distribution and diversity of Bartonella species in rodents and their ectoparasites across Thailand. PLoS One 10:e0140856. doi:10.1371/journal.pone.0140856

    Article  PubMed  PubMed Central  Google Scholar 

  71. Melter O, Arvand M, Votypka J, Hulinska D (2012) Bartonella quintana transmission from mite to family with high socioeconomic status. Emerg Infect Dis 18:163–165. doi:10.3201/eid1801.110186

    Article  PubMed  PubMed Central  Google Scholar 

  72. Larson HK, Goffredi SK, Parra EL, Vargas O, Pinto-Tomas AA, McGlynn TP (2014) Distribution and dietary regulation of an associated facultative Rhizobiales-related bacterium in the omnivorous giant tropical ant, Paraponera clavata. Naturwissenschaften 101:397–406. doi:10.1007/s00114-014-1168-0

    Article  CAS  PubMed  Google Scholar 

  73. Valerio CR, Murray P, Arlian LG, Slater JE (2005) Bacterial 16S ribosomal DNA in house dust mite cultures. J Allergy Clin Immunol 116:1296–1300. doi:10.1016/j.jaci.2005.09.046

    Article  CAS  PubMed  Google Scholar 

  74. Kosoy M, Hayman DTS, Chan K-S (2012) Bartonella bacteria in nature: where does population variability end and a species start? Infect Genet Evol 12:894–904. doi:10.1016/j.meegid.2012.03.005

    Article  PubMed  Google Scholar 

  75. Tsai Y-L, Chang C-C, Chuang S-T, Chomel BB (2011) Bartonella species and their ectoparasites: selective host adaptation or strain selection between the vector and the mammalian host? Comp Immunol Microbiol Infect Dis 34:299–314. doi:10.1016/j.cimid.2011.04.005

    Article  PubMed  Google Scholar 

  76. Mediannikov O, Sekeyova Z, Birg M-L, Raoult D (2010) A novel obligate intracellular gamma-proteobacterium associated with ixodid ticks, Diplorickettsia massiliensis, gen. nov., sp. nov. PLoS One 5:e11478. doi:10.1371/journal.pone.0011478

    Article  PubMed  PubMed Central  Google Scholar 

  77. Kattar MM, Cookson BT, Carlson LDC, Stiglich SK, Schwartz MA, Nguyen TT, Daza R, Wallis CK, Yarfitz SL, Coyle MB (2001) Tsukamurella strandjordae sp. nov., a proposed new species causing sepsis. J Clin Microbiol 39:1467–1476. doi:10.1128/JCM.39.4.1467-1476.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Almehmi A, Pfister AK, McCowan R, Matulis S (2004) Implantable cardioverter-defibrillator infection caused by Tsukamurella. W V Med J 100:185–186

    PubMed  Google Scholar 

  79. Kucerova Z, Stejskal V (2009) Morphological diagnosis of the eggs of stored-products mites. Exp Appl Acarol 49:173–183. doi:10.1007/s10493-009-9256-0

    Article  PubMed  Google Scholar 

  80. Ma W-J, Vavre F, Beukeboom LW (2014) Manipulation of arthropod sex determination by endosymbionts: diversity and molecular mechanisms. Sex Dev 8:59–73. doi:10.1159/000357024

    Article  CAS  PubMed  Google Scholar 

  81. Pietri JE, DeBruhl H, Sullivan W (2016) The rich somatic life of Wolbachia. MicrobiologyOpen 5:923–936. doi:10.1002/mbo3.390

    Article  PubMed  PubMed Central  Google Scholar 

  82. Chirico J, Eriksson H, Fossum O, Jansson D (2003) The poultry red mite, Dermanyssus gallinae, a potential vector of Erysipelothrix rhusiopathiae causing erysipelas in hens. Med Vet Entomol 17:232–234. doi:10.1046/j.1365-2915.2003.00428.x

    Article  CAS  PubMed  Google Scholar 

  83. Eriksson H, Brannstrom S, Skarin H, Chirico J (2010) Characterization of Erysipelothrix rhusiopathiae isolates from laying hens and poultry red mites (Dermanyssus gallinae) from an outbreak of erysipelas. Avian Pathol 39:505–509. doi:10.1080/03079457.2010.518313

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the project of the Ministry of Agriculture of the Czech Republic RO0417 and by COST Action FA1404 (COREMI) (http://www.coremi.eu/home.html). Computational resources were supplied by the Ministry of Education, Youth and Sports of the Czech Republic under the Projects CESNET (Project No. LM2015042) and CERIT-Scientific Cloud (Project No. LM2015085) provided within the program Projects of Large Research, Development and Innovations Infrastructures. We thank Vlastislav Machandr for his kind help with sample collection and Martin Markovic for technical assistance.

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Authors and Affiliations

  1. Crop Research Institute, Drnovska 507/73, Prague 6-Ruzyne, 161 06, Czechia

    Jan Hubert, Tomas Erban, Jan Kopecky, Bruno Sopko & Marta Nesvorna

  2. Department of Medical Chemistry and Clinical Biochemistry, 2nd Faculty of Medicine, Charles University and Motol University Hospital, V Uvalu 84/1, Prague, 5150 06, Czechia

    Bruno Sopko

  3. Faculty of AgriSciences, Mendel University in Brno, Zemedelska 1665/1, Brno, 61 300, Czechia

    Martina Lichovnikova

  4. Institute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, Buenteweg 17, 30559, Hannover, Germany

    Sabine Schicht & Christina Strube

  5. Vice-Chancellor Office, Centre for Applied Biological and Exercise Sciences, Coventry University, Priory Street, Coventry, CV1 5FB, UK

    Olivier Sparagano

Authors
  1. Jan Hubert
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  2. Tomas Erban
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  3. Jan Kopecky
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  4. Bruno Sopko
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  5. Marta Nesvorna
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  6. Martina Lichovnikova
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  7. Sabine Schicht
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  8. Christina Strube
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  9. Olivier Sparagano
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Corresponding author

Correspondence to Jan Hubert.

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The authors declare no conflict of interest.

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Hubert, J., Erban, T., Kopecky, J. et al. Comparison of Microbiomes between Red Poultry Mite Populations (Dermanyssus gallinae): Predominance of Bartonella-like Bacteria. Microb Ecol 74, 947–960 (2017). https://doi.org/10.1007/s00248-017-0993-z

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  • DOI: https://doi.org/10.1007/s00248-017-0993-z

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