Skip to main content

Population and Culture Age Influence the Microbiome Profiles of House Dust Mites

Microbial Ecology volume 77, pages 1048–1066 (2019)Cite this article

Abstract

Interactions with microorganisms might enable house dust mites (HDMs) to derive nutrients from difficult-to-digest structural proteins and to flourish in human houses. We tested this hypothesis by investigating the effects of changes in the mite culture growth and population of two HDM species on HDM microbiome composition and fitness. Growing cultures of laboratory and industrial allergen-producing populations of Dermatophagoides farinae (DFL and DFT, respectively) and Dermatophagoides pteronyssinus (DPL and DPT, respectively) were sampled at four time points. The symbiotic microorganisms of the mites were characterized by DNA barcode sequencing and quantified by qPCR using universal/specific primers. The population growth of mites and nutrient contents of mite bodies were measured and correlated with the changes in bacteria in the HDM microbiome. The results showed that both the population and culture age significantly influenced the microbiome profiles. Cardinium formed 93% and 32% of the total sequences of the DFL and DFT bacterial microbiomes, respectively, but this bacterial species was less abundant in the DPL and DPT microbiomes. Staphylococcus abundance was positively correlated with increased glycogen contents in the bodies of mites, and increased abundances of Aspergillus, Candida, and Kocuria were correlated with increased lipid contents in the bodies of mites. The xerophilic fungus Wallemia accounted for 39% of the fungal sequences in the DPL microbiome, but its abundance was low in the DPT, DFL, and DFT microbiomes. With respect to the mite culture age, we made three important observations: the mite population growth from young cultures was 5–8-fold higher than that from old cultures; specimens from old cultures had greater abundances of fungi and bacteria in their bodies; and yeasts predominated in the gut contents of specimens from young cultures, whereas filamentous mycelium prevailed in specimens from old cultures. Our results are consistent with the hypothesis that mites derive nutrients through associations with microorganisms.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Colloff MJ (2009) Dust mites. CSIRO Publishing, Collingwood. https://doi.org/10.1007/978-90-481-2224-0

    Book  Google Scholar 

  2. Jacquet A (2011) The role of innate immunity activation in house dust mite allergy. Trends Mol. Med. 17:604–611. https://doi.org/10.1016/j.molmed.2011.05.014

    Article  CAS  PubMed  Google Scholar 

  3. Arlian LG (1991) House-dust-mite allergens: a review. Exp Appl Acarol 10:167–186. https://doi.org/10.1007/BF01198649

    Article  CAS  PubMed  Google Scholar 

  4. Calderon MA, Linneberg A, Kleine-Tebbe J, De Blay F, Hernandez Fernandez de Rojas D, Virchow JC, Demoly P (2015) Respiratory allergy caused by house dust mites: what do we truly know? J. Allergy Clin. Immunol. 136:38–48. https://doi.org/10.1016/j.jaci.2014.10.012

    Article  PubMed  Google Scholar 

  5. Vidal-Quist JC, Ortego F, Rombauts S, Castanera P, Hernandez-Crespo P (2017) Dietary shifts have consequences for the repertoire of allergens produced by the European house dust mite. Med. Vet. Entomol. 31:272–280. https://doi.org/10.1111/mve.12234

    Article  CAS  PubMed  Google Scholar 

  6. Colloff MJ (2009) Development, life histories and population dynamics. In: Colloff MJ (ed) Dust mites. CSIRO Publishing, Collingwood, pp 215–254. https://doi.org/10.1007/978-90-481-2224-0_5

    Chapter  Google Scholar 

  7. Arlian LG, Dippold JS (1996) Development and fecundity of Dermatophagoides farinae (Acari: Pyroglyphidae). J. Med. Entomol. 33:257–260. https://doi.org/10.1093/jmedent/33.2.257

    Article  CAS  PubMed  Google Scholar 

  8. Arlian LG, Rapp CM, Ahmed SG (1990) Development of Dermatophagoides pteronyssinus (Acari: Pyroglyphidae). J. Med. Entomol. 27:1035–1040. https://doi.org/10.1093/jmedent/27.6.1035

    Article  CAS  PubMed  Google Scholar 

  9. Eraso E, Guisantes JA, Martinez J, Saenz-de-Santamaria M, Martinez A, Palacios R, Cisterna R (1997) Kinetics of allergen expression in cultures of house dust mites, Dermatophagoides pteronyssinus and D. farinae (Acari: Pyroglyphidae). J. Med. Entomol. 34:684–689. https://doi.org/10.1093/jmedent/34.6.684

    Article  CAS  PubMed  Google Scholar 

  10. Eraso E, Martinez J, Martinez A, Palacios R, Guisantes JA (1997) Quality parameters for the production of mite extracts. Allergol. Immunopathol. 25:113–117

    CAS  Google Scholar 

  11. Andersen A (1991) Nutritional value of yeast for Dermatophagoides pteronyssinus (Acari: Epidermoptidae) and the antigenic and allergenic composition of extracts during extended culturing. J. Med. Entomol. 28:487–491. https://doi.org/10.1093/jmedent/28.4.487

    Article  CAS  PubMed  Google Scholar 

  12. Eraso E, Martinez J, Garcia-Ortega P, Martinez A, Palacios R, Cisterna R, Guisantes JA (1998) Influence of mite growth culture phases on the biological standardization of allergenic extracts. J Investig Allergol Clin Immunol 8:201–206

    CAS  PubMed  Google Scholar 

  13. Klimov PB, OConnor B (2013) Is permanent parasitism reversible?—critical evidence from early evolution of house dust mites. Syst. Biol. 62:411–423. https://doi.org/10.1093/sysbio/syt008

    Article  PubMed  Google Scholar 

  14. OConnor BM (1979) Evolutionary origins of astigmatid mites inhabiting stored products. In: Rodriguez GJ (ed) Recent advances in acarology, vol. 1. Academic Press, New York, pp 273–278. https://doi.org/10.1016/b978-0-12-592201-2.50038-5

    Chapter  Google Scholar 

  15. Sugiura S, Ikeda H (2014) Keratin decomposition by trogid beetles: evidence from a feeding experiment and stable isotope analysis. Naturwissenschaften 101:187–196. https://doi.org/10.1007/s00114-013-1137-z

    Article  CAS  PubMed  Google Scholar 

  16. Brandwein M, Steinberg D, Meshner S (2016) Microbial biofilms and the human skin microbiome. NPJ Biofilms Microbiomes 2(3):3. https://doi.org/10.1038/s41522-016-0004-z

    Article  PubMed  PubMed Central  Google Scholar 

  17. Horak B (1987) Preliminary study on the concentration and species composition of bacteria, fungi and mites in samples of house dust from Silesia (Poland). Allergol. Immunopathol. 15:161–166

    CAS  Google Scholar 

  18. de Saint Georges-Gridelet D (1987) Vitamin requirements of the European house dust mite, Dermatophagoides pteronyssinus (Acari: Pyroglyphidae), in relation to its fungal association. J. Med. Entomol. 24:408–411. https://doi.org/10.1093/jmedent/24.4.408

    Article  PubMed  Google Scholar 

  19. Van Asselt L (1999) Interactions between domestic mites and fungi. Indoor Built Environ 8:216–220. https://doi.org/10.1159/000024644

    Article  Google Scholar 

  20. Naegele A, Reboux G, Scherer E, Roussel S, Millon L (2013) Fungal food choices of Dermatophagoides farinae affect indoor fungi selection and dispersal. Int. J. Environ. Health Res. 23:91–95. https://doi.org/10.1080/09603123.2012.699029

    Article  PubMed  Google Scholar 

  21. Luxton M (1972) Studies on the oribatid mites of a Danish beech wood soil. I. Nutritional biology. Pedobiologia 12:434–463

    Google Scholar 

  22. Erban T, Hubert J (2008) Digestive function of lysozyme in synanthropic acaridid mites enables utilization of bacteria as a food source. Exp Appl Acarol 44:199–212. https://doi.org/10.1007/s10493-008-9138-x

    Article  CAS  PubMed  Google Scholar 

  23. Sabree ZL, Moran NA (2014) Host-specific assemblages typify gut microbial communities of related insect species. SpringerPlus 3:138. https://doi.org/10.1186/2193-1801-3-138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annual Rev Entomol 60:17–34. https://doi.org/10.1146/annurev-ento-010814-020822

    Article  CAS  Google Scholar 

  25. 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. https://doi.org/10.3389/fmicb.2016.01046

    Article  PubMed  PubMed Central  Google Scholar 

  26. 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. https://doi.org/10.1007/s10493-016-0080-z

    Article  PubMed  Google Scholar 

  27. Chan T-F, Ji K-M, Yim AK-Y, Liu X-Y, Zhou J-W, Li R-Q, Yang KY, Li J, Li M, Law PT-W, Wu Y-L, Cai Z-L, Qin H, Bao Y, Leung RK-K, Ng PK-S, Zou J, Zhong X-J, Ran P-X, Zhong N-S, Liu Z-G, Tsui SK-W (2015) The draft genome, transcriptome, and microbiome of Dermatophagoides farinae reveal a broad spectrum of dust mite allergens. J. Allergy Clin. Immunol. 135:539–548. https://doi.org/10.1016/j.jaci.2014.09.031

    Article  CAS  PubMed  Google Scholar 

  28. Waldron R, McGowan J, Gordon N, McCarthy C, Mitchell EB, Doyle S, Fitzpatrick DA (2017) Draft genome sequence of Dermatophagoides pteronyssinus, the European house dust mite. Genome Announc 5:e00789–e00717. https://doi.org/10.1128/genomeA.00789-17

    Article  PubMed  PubMed Central  Google Scholar 

  29. Erban T, Harant K, Hubert J (2017) Detailed two-dimensional gel proteomic mapping of the feces of the house dust mite Dermatophagoides pteronyssinus and comparison with D. farinae: reduced trypsin protease content in D. pteronyssinus and different isoforms. J. Proteome 162:11–19. https://doi.org/10.1016/j.jprot.2017.04.021

    Article  CAS  Google Scholar 

  30. Kim JY, Yi M, Hwang Y, Lee JY, Lee I-Y, Yong D, Yong T-S (2018) 16S rRNA profiling of the Dermatophagoides farinae core microbiome: Enterococcus and Bartonella. Clin. Exp. Allergy 48:607–610. https://doi.org/10.1111/cea.13104

    Article  CAS  PubMed  Google Scholar 

  31. Petrova-Nikitina AD, Antropova AB, Bilanenko EN, Mokeeva VL, Chekunova LN, Bulgakova TA, Zheltikova TM (2011) Population dynamics of mites of the family Pyroglyphidae and micromycetes in laboratory cultures. Entomol Rev 91:377–387. https://doi.org/10.1134/S0013873811030134

    Article  Google Scholar 

  32. 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. https://doi.org/10.1007/s00248-011-9969-6

    Article  CAS  PubMed  Google Scholar 

  33. 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. https://doi.org/10.1111/jam.12899

    Article  CAS  PubMed  Google Scholar 

  34. 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. https://doi.org/10.1371/journal.pone.0129996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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. https://doi.org/10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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. https://doi.org/10.1128/AEM.01043-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  38. Edgar RC (2016) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv. https://doi.org/10.1101/081257 https://www.biorxiv.org/content/early/2016/10/15/081257. Accessed 6 August 2017

  39. Sarikhani E, Sagova-Mareckova M, Omelka M, Kopecky J (2017) The effect of peat and iron supplements on the severity of potato common scab and bacterial community in tuberosphere soil. FEMS Microbiol. Ecol. 93:fiw206. https://doi.org/10.1093/femsec/fiw206

    Article  CAS  PubMed  Google Scholar 

  40. 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. https://doi.org/10.1093/nar/gkt1244

    Article  CAS  PubMed  Google Scholar 

  41. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:D590–D596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  PubMed  Google Scholar 

  42. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J. Mol. Biol. 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  43. 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 2017

    Google Scholar 

  44. 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. R Foundation for Statistical Computing, Vienna, Austria. http://CRAN.R-project.org/package=vegan. Accessed 6 August 2017

  45. R Development Core Team (2016) R: a language and environment for statistical computing, reference index version 3.3.1. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 6 August 2017

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

    Article  PubMed  PubMed Central  Google Scholar 

  47. Anderson MJ (2001) A new method for nonparametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  49. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632. https://doi.org/10.1890/07-0986.1

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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. https://doi.org/10.1128/AEM.00062-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  57. 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. https://doi.org/10.1093/oxfordjournals.molbev.a004221

    Article  CAS  PubMed  Google Scholar 

  58. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  59. 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. https://doi.org/10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  60. 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 6 August 2016

  61. Liang Q, Chen L, Fulco AJ (1995) An efficient and optimized PCR method with high fidelity for site-directed mutagenesis. PCR Methods Appl 4:269–274. https://doi.org/10.1101/gr.4.5.269

    Article  CAS  PubMed  Google Scholar 

  62. Kaufmann C, Brown MR (2008) Regulation of carbohydrate metabolism and flight performance by a hypertrehalosaemic hormone in the mosquito Anopheles gambiae. J. Insect Physiol. 54:367–377. https://doi.org/10.1016/j.jinsphys.2007.10.007

    Article  CAS  PubMed  Google Scholar 

  63. Van Handel E (1985) Rapid determination of glycogen and sugars in mosquitoes. J. Am. Mosq. Control Assoc. 1:299–301

    PubMed  Google Scholar 

  64. Kaufmann C (2014) Determination of lipid, glycogen and sugars in mosquitoes. In: Benedict M (ed) MR4 methods in Anopheles research, 4th edn. BEI Resources, Manassas, VA, USA. https://www.beiresources.org/Publications/MethodsinAnophelesResearch.aspx. Accessed 6 August 2016

  65. 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:e00128–e00117. https://doi.org/10.1128/AEM.00128-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Evans GO, Sheals JG, MacFarlane D (1961) The terrestrial Acari of the British Isles: an introduction to their morphology, biology and classification, vol. I. Introduction and biology. British Museum, London

    Google Scholar 

  67. Smrz J (1989) Internal anatomy of Hypochthonius rufulus (Acari: Oribatida). J. Morphol. 200:215–230. https://doi.org/10.1002/jmor.1052000210

    Article  PubMed  Google Scholar 

  68. Exbrayat J-M (2013) Histochemical and cytochemical methods of visualization1st edn. CRC Press, Boca Raton. https://doi.org/10.1201/b14967

    Book  Google Scholar 

  69. Bochkov AV, Klimov PB, Hestvik G, Saveljev AP (2014) Integrated Bayesian species delimitation and morphological diagnostics of chorioptic mange mites (Acariformes: Psoroptidae: Chorioptes). Parasitol. Res. 113:2603–2627. https://doi.org/10.1007/s00436-014-3914-9

    Article  PubMed  Google Scholar 

  70. Klimov PB, Bochkov AV, OConnor BM (2016) Phylogenetic position of the house dust mite subfamily Guatemalichinae (Acariformes: Pyroglyphidae) based on integrated molecular and morphological analyses and different measures of support. Cladistics 32:261–275. https://doi.org/10.1111/cla.12126

    Article  PubMed  Google Scholar 

  71. Klimov PB, Oconnor BM (2009) Improved tRNA prediction in the American house dust mite reveals widespread occurrence of extremely short minimal tRNAs in acariform mites. BMC Genomics 10:598. https://doi.org/10.1186/1471-2164-10-598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Webster LMI, Thomas RH, McCormack GP (2004) Molecular systematics of Acarus siro s. lat., a complex of stored food pests. Mol. Phylogenet. Evol. 32:817–822. https://doi.org/10.1016/j.ympev.2004.04.005

    Article  CAS  PubMed  Google Scholar 

  73. Dermauw W, Van Leeuwen T, Vanholme B, Tirry L (2009) The complete mitochondrial genome of the house dust mite Dermatophagoides pteronyssinus (Trouessart): a novel gene arrangement among arthropods. BMC Genomics 10:107. https://doi.org/10.1186/1471-2164-10-107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Beroiz B, Couso-Ferrer F, Ortego F, Chamorro MJ, Arteaga C, Lombardero M, Castanera P, Hernandez-Crespo P (2014) Mite species identification in the production of allergenic extracts for clinical use and in environmental samples by ribosomal DNA amplification. Med. Vet. Entomol. 28:287–296. https://doi.org/10.1111/mve.12052

    Article  CAS  PubMed  Google Scholar 

  75. Noge K, Mori N, Tanaka C, Nishida R, Tsuda M, Kuwahara Y (2005) Identification of astigmatid mites using the second internal transcribed spacer (ITS2) region and its application for phylogenetic study. Exp Appl Acarol 35:29–46. https://doi.org/10.1007/s10493-004-1953-0

    Article  CAS  PubMed  Google Scholar 

  76. Yang B, Cai J, Cheng X (2011) Identification of astigmatid mites using ITS2 and COI regions. Parasitol. Res. 108:497–503. https://doi.org/10.1007/s00436-010-2153-y

    Article  PubMed  Google Scholar 

  77. Griffiths DA, Cunnington AM (1971) Dermatophagoides microceras sp. n: a description and comparison with its sibling species, D. farinae Hughes, 1961. J. Stored Prod. Res. 7:1–14. https://doi.org/10.1016/0022-474X(71)90032-4

    Article  Google Scholar 

  78. Nakamura Y, Kawai S, Yukuhiro F, Ito S, Gotoh T, Kisimoto R, Yanase T, Matsumoto Y, Kageyama D, Noda H (2009) Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of “Candidatus Cardinium hertigii” based on detection of a new Cardinium group from biting midges. Appl. Environ. Microbiol. 75:6757–6763. https://doi.org/10.1128/AEM.01583-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Brody AR, McGrath JC, Wharton GW (1972) Dermatophagoides farinae: the digestive system. J N Y Entomol Soc 80:152–177

    Google Scholar 

  80. Wharton GW, Brody AR (1972) The peritrophic membrane of the mite, Dermatophagoides farinae: Acariformes. J. Parasitol. 58:801–804. https://doi.org/10.2307/3278321

    Article  CAS  PubMed  Google Scholar 

  81. Douglas AE, Hart BJ (1989) The significance of the fungus Aspergillus penicillioides to the house dust mite Dermatophagoides pteronyssinus. Symbiosis 7:105–116

    Google Scholar 

  82. Erban T, Hubert J (2010) Comparative analyses of proteolytic activities in seven species of synanthropic acaridid mites. Arch. Insect Biochem. Physiol. 75:187–206. https://doi.org/10.1002/arch.20388

    Article  CAS  PubMed  Google Scholar 

  83. Erban T, Hubert J (2010) Determination of pH in regions of the midguts of acaridid mites. J. Insect Sci. 10(42):1–12. https://doi.org/10.1673/031.010.4201

    Article  Google Scholar 

  84. Childs M, Bowman CE (1981) Lysozyme activity in six species of economically important astigmatid mites. Comp Biochem Physiol B 70:615–617. https://doi.org/10.1016/0305-0491(81)90305-9

    Article  Google Scholar 

  85. 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. https://doi.org/10.1016/j.jip.2012.11.001

    Article  CAS  PubMed  Google Scholar 

  86. Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol. Ecol. 13:2009–2016. https://doi.org/10.1111/j.1365-294X.2004.02203.x

    Article  CAS  PubMed  Google Scholar 

  87. Hubert J, Stejskal V, Nesvorna M, Aulicky R, Kopecky J, Erban T (2016) Differences in the bacterial community of laboratory and wild populations of the predatory mite Cheyletus eruditus (Acarina: Cheyletidae) and bacteria transmission from its prey Acarus siro (Acari: Acaridae). J. Econ. Entomol. 109:1450–1457. https://doi.org/10.1093/jee/tow032

    Article  CAS  PubMed  Google Scholar 

  88. Santos-Garcia D, Rollat-Farnier P-A, Beitia F, Zchori-Fein E, Vavre F, Mouton L, Moya A, Latorre A, Silva FJ (2014) The genome of Cardinium cBtQ1 provides insights into genome reduction, symbiont motility, and its settlement in Bemisia tabaci. Genome Biol Evol 6:1013–1030. https://doi.org/10.1093/gbe/evu077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Penz T, Schmitz-Esser S, Kelly SE, Cass BN, Muller A, Woyke T, Malfatti SA, Hunter MS, Horn M (2012) Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genet. 8:e1003012. https://doi.org/10.1371/journal.pgen.1003012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Zhang Y-K, Chen Y-T, Yang K, Hong X-Y (2016) A review of prevalence and phylogeny of the bacterial symbiont Cardinium in mites (subclass: Acari). Syst Appl Acarol 21:978–990. https://doi.org/10.11158/saa.21.7.11

    Article  Google Scholar 

  91. Gotoh T, Noda H, Ito S (2007) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98:13–20. https://doi.org/10.1038/sj.hdy.6800881

    Article  CAS  PubMed  Google Scholar 

  92. Hodgson RK (1976) Sex ratio and sex determination in the American house dust mite, Dermataphagoides farinae. Ann Entomol Soc Am 69:1085–1086. https://doi.org/10.1093/aesa/69.6.1085

    Article  Google Scholar 

  93. Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJM (2016) Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J 10:655–664. https://doi.org/10.1038/ismej.2015.142

    Article  CAS  PubMed  Google Scholar 

  94. Kopecky J, Nesvorna M, Mareckova-Sagova M, Hubert J (2014) The effect of antibiotics on associated bacterial community of stored product mites. PLoS One 9:e112919. https://doi.org/10.1371/journal.pone.0112919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Chigira A, Miura K (2005) Detection of ‘Candidatus Cardinium’ bacteria from the haploid host Brevipalpus californicus (Acari: Tenuipalpidae) and effect on the host. Exp Appl Acarol 37:107–116. https://doi.org/10.1007/s10493-005-0592-4

    Article  PubMed  Google Scholar 

  96. 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. https://doi.org/10.1016/j.jaci.2005.09.046

    Article  CAS  PubMed  Google Scholar 

  97. Hubert J, Erban T, Kopecky J, Sopko B, Nesvorna M, Lichovnikova M, Schicht S, Strube C, Sparagano O (2017) Comparison of microbiomes between red poultry mite populations (Dermanyssus gallinae): predominance of Bartonella-like bacteria. Microb. Ecol. 74:947–960. https://doi.org/10.1007/s00248-017-0993-z

    Article  PubMed  Google Scholar 

  98. Segers FHID, Kesnerova L, Kosoy M, Engel P (2017) Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME J 11:1232–1244. https://doi.org/10.1038/ismej.2016.201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. 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. https://doi.org/10.1099/ijsem.0.000736

    Article  CAS  PubMed  Google Scholar 

  100. Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, Nomicos E, Polley EC, Komarow HD, NISC Comparative Sequence Program, 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. https://doi.org/10.1101/gr.131029.111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:260–270. https://doi.org/10.1038/nrg3182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Tang VH, Chang BJ, Srinivasan A, Mathaba LT, Harnett GB, Stewart GA (2013) Skin-associated Bacillus, staphylococcal and micrococcal species from the house dust mite, Dermatophagoides pteronyssinus and bacteriolytic enzymes. Exp Appl Acarol 61:431–447. https://doi.org/10.1007/s10493-013-9712-8

    Article  CAS  PubMed  Google Scholar 

  103. Merk K, Borelli C, Korting HC (2005) Lactobacilli—bacteria–host interactions with special regard to the urogenital tract. Int J Med Microbiol 295:9–18. https://doi.org/10.1016/j.ijmm.2004.11.006

    Article  CAS  PubMed  Google Scholar 

  104. Inada N, Shoji J, Yamagami S (2017) Atopic keratoconjunctivitis complicated by Kocuria koreensis keratitis: the first case. Allergy Asthma Clin Immunol 13(6):6. https://doi.org/10.1186/s13223-017-0178-9

    Article  PubMed  PubMed Central  Google Scholar 

  105. Hay DB, Hart BJ, Pearce RB, Kozakiewicz Z, Douglas AE (1992) How relevant are house dust mite–fungal interactions in laboratory culture to the natural dust system? Exp Appl Acarol 16:37–47. https://doi.org/10.1007/BF01201491

    Article  CAS  PubMed  Google Scholar 

  106. Lustgraaf B (1978) Ecological relationships between xerophilic fungi and house-dust mites (Acarida: Pyroglyphidae). Oecologia 33:351–359. https://doi.org/10.1007/BF00348118

    Article  CAS  PubMed  Google Scholar 

  107. Simon D, Straumann A, Dahinden C, Simon H-U (2013) Frequent sensitization to Candida albicans and profilins in adult eosinophilic esophagitis. Allergy 68:945–948. https://doi.org/10.1111/all.12157

    Article  CAS  PubMed  Google Scholar 

  108. Avula-Poola S, Morgan MS, Arlian LG (2012) Diet influences growth rates and allergen and endotoxin contents of cultured Dermatophagoides farinae and Dermatophagoides pteronyssinus house dust mites. Int. Arch. Allergy Immunol. 159:226–234. https://doi.org/10.1159/000336026

    Article  CAS  PubMed  Google Scholar 

  109. Vidal-Quist JC, Ortego F, Lombardero M, Castanera P, Hernandez-Crespo P (2015) Allergen expression in the European house dust mite Dermatophagoides pteronyssinus throughout development and response to environmental conditions. Med. Vet. Entomol. 29:137–146. https://doi.org/10.1111/mve.12102

    Article  CAS  PubMed  Google Scholar 

  110. Colloff MJ (1987) Effects of temperature and relative humidity on development times and mortality of eggs from laboratory and wild populations of the European house-dust mite Dermatophagoides pteronyssinus (Acari: Pyroglyphidae). Exp Appl Acarol 3:279–289. https://doi.org/10.1007/BF01193165

    Article  CAS  PubMed  Google Scholar 

  111. Hart BJ, Crowther D, Wilkinson T, Biddulph P, Ucci M, Pretlove S, Ridley I, Oreszczyn T (2007) Reproduction and development of laboratory and wild house dust mites (Acari: Pyroglyphidae) and their relationship to the natural dust ecosystem. J. Med. Entomol. 44:568–574. https://doi.org/10.1093/jmedent/44.4.568

    Article  CAS  PubMed  Google Scholar 

  112. Matsumoto K (1965) Studies on environmental factors for breeding of grain mites VII. Relationship between reproduction of mites and kind of carbohydrates in the diet. Med Entomol Zool 16:118–122. https://doi.org/10.7601/mez.16.118

    Article  Google Scholar 

  113. Smrz J, Trelova M (1995) The association of bacteria and some soil mites (Acari: Oribatida and Acaridida). Acta Zool Fennica 196:120–123

    Google Scholar 

  114. Smrz J (2002) Microanatomical and microbiological characteristics of the quiescent state of Scutovertex minutus (Acari: Oribatida). Exp Appl Acarol 27:103–112. https://doi.org/10.1023/A:1021527904766

    Article  PubMed  Google Scholar 

  115. Smrz J (2003) Microanatomical and biological aspects of bacterial associations in Tyrophagus putrescentiae (Acari: Acaridida). Exp Appl Acarol 31:105–113. https://doi.org/10.1023/B:APPA.0000005111.05959.d6

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Barry OConnor and the anonymous reviewers for providing useful comments on earlier drafts of this manuscript. We thank Marie Bostlova, Martin Markovic, Bc. Vit Molva, and Jan Hubert Jr. for their technical assistance; Prof. Krzysztof Solarz for the laboratory mite culture; and RNDr. Alexandr Zgarbovsky for the industrial allergen-producing mite cultures.

Funding

JH, TE, and MN were supported by the Czech Science Foundation (GACR) as part of Project No. 17-12068S. PBK was supported by the Russian Science Foundation (Project No. 16-14-10109), the Ministry of Education and Science of the Russian Federation (No. 6.1933.2014/K Project Code 1933), and the Russian Foundation for Basic Research (No. 15-04-0s5185-a).

Author information

Authors and Affiliations

  1. Crop Research Institute, Drnovska 507/73, CZ-16106, Prague 6-Ruzyne, Czechia

    Jan Hubert, Marta Nesvorna, Jan Kopecky & Tomas Erban

  2. Department of Ecology and Evolutionary Biology, University of Michigan, 3600 Varsity Drive, Ann Arbor, MI, 48109-2228, USA

    Pavel Klimov

  3. Institute of Biology, University of Tyumen, Pirogova 3, Tyumen, Russia, 625043

    Pavel Klimov

Authors
  1. Jan Hubert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marta Nesvorna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jan Kopecky
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tomas Erban
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pavel Klimov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jan Hubert.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

Electronic Supplementary Material

ESM 1

(DOCX 766 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hubert, J., Nesvorna, M., Kopecky, J. et al. Population and Culture Age Influence the Microbiome Profiles of House Dust Mites. Microb Ecol 77, 1048–1066 (2019). https://doi.org/10.1007/s00248-018-1294-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-018-1294-x

Keywords

  • Nutrition
  • Bacteria
  • Fungi
  • Yeasts
  • Gut
  • Symbiosis
  • Diet
  • Dermatophagoides pteronyssinus
  • Dermatophagoides farinae