Microbial Communities of Stored Product Mites: Variation by Species and Population

Abstract

Arthropod-associated microorganisms are important because they affect host fitness, protect hosts from pathogens, and influence the host’s ability to vector pathogens. Stored product mites (Astigmata) often establish large populations in various types of food items, damaging the food by direct feeding and introducing contaminants, including their own bodies, allergen-containing feces, and associated microorganisms. Here we access the microbial structure and abundance in rearing diets, eggs, feces fraction, and mite bodies of 16 mite populations belonging to three species (Carpoglyphus lactis, Acarus siro, and Tyrophagus putrescentiae) using quantitative PCR and 16S ribosomal RNA (rRNA) gene amplicon sequencing. The mite microbiomes had a complex structure dominated by the following bacterial taxa (OTUs): (a) intracellular symbionts of the genera Cardinium and Wolbachia in the mite bodies and eggs; (b) putative gut symbionts of the genera Solitalea, Bartonella, and Sodalis abundant in mite bodies and also present in mite feces; (c) feces-associated or environmental bacteria of the genera Bacillus, Staphylococcus, and Kocuria in the diet, mite bodies, and feces. Interestingly and counterintuitively, the differences between microbial communities in various conspecific mite populations were higher than those between different mite species. To explain some of these differences, we hypothesize that the intracellular bacterial symbionts can affect microbiome composition in mite bodies, causing differences between microbial profiles. Microbial profiles differed between various sample types, such as mite eggs, bodies, and the environment (spent growth medium—SPGM). Low bacterial abundances in eggs may result in stochastic effects in parent-offspring microbial transmission, except for the intracellular symbionts. Bacteria in the rearing diet had little effect on the microbial community structure in SPGM and mite bodies. Mite fitness was positively correlated with bacterial abundance in SPGM and negatively correlated with bacterial abundances in mite bodies. Our study demonstrates critical host-microbe interactions, affecting all stages of mite growth and leading to alteration of the environmental microbiome. Correlational evidence based on absolute quantitation of bacterial 16S rRNA gene copies suggests that mite-associated microorganisms are critical for modulating important pest properties of mites by altering population growth.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. 1.

    Chambers J, Bhushy Thind B, Dunn JA, Pearson DJ (1999) The importance of storage mite allergens in occupational and domestic environments. In: Robinson W, Rettich F, Rambo GW (eds) Proceedings of the 3rd International Conference on Urban Pests: Prague, 19–22 July 1999. Czech University of Agriculture, Prague, pp 559–569

    Google Scholar 

  2. 2.

    Zhao Y, Abbar S, Amoah B, Phillips TW, Schilling MW (2016) Controlling pests in dry-cured ham: a review. Meat Sci 111:183–191. https://doi.org/10.1016/j.meatsci.2015.09.009

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Athanassiou CG, Palyvos NE, Eliopoulos PA, Papadoulis GT (2001) Distribution and migration of insects and mites in flat storage containing wheat. Phytoparasitica 29:379–392. https://doi.org/10.1007/BF02981856

    Article  Google Scholar 

  4. 4.

    Hughes AM (1976) The mites of stored food and houses: technical bulletin 9 of the Ministry of Agriculture, Fisheries and Food2nd edn. Her Majesty’s Stationery Office, London

    Google Scholar 

  5. 5.

    Hubert J, Erban T, Nesvorna M, Stejskal V (2011) Emerging risk of infestation and contamination of dried fruits by mites in the Czech Republic. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 28:1129–1135. https://doi.org/10.1080/19440049.2011.584911

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Green WF, Woolcock AJ (1978) Tyrophagus putrescentiae: an allergenically important mite. Clin Allergy 8:135–144. https://doi.org/10.1111/j.1365-2222.1978.tb00458.x

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Sanchez-Borges M, Fernandez-Caldas E (2015) Hidden allergens and oral mite anaphylaxis: the pancake syndrome revisited. Curr Opin Allergy Clin Immunol 15:337–343. https://doi.org/10.1097/ACI.0000000000000175

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Hubert J, Stejskal V, Athanassiou CG, Throne JE (2018) Health hazards associated with arthropod infestation of stored products. Annu Rev Entomol 63:553–573. https://doi.org/10.1146/annurev-ento-020117-043218

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Cunnington AM (1965) Physical limits for complete development of the grain mite, Acarus siro L. (Acarina, Acaridae), in relation to its world distribution. J Appl Ecol 2:295–306. https://doi.org/10.2307/2401481

    Article  Google Scholar 

  10. 10.

    Hibberson CE, Vogelnest LJ (2014) Storage mite contamination of commercial dry dog food in south-eastern Australia. Aust Vet J 92:219–224. https://doi.org/10.1111/avj.12185

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Robertson PL (1946) Tyroglyphid mites in stored products in New Zealand. T Roy Soc N Z 76:185–207

    Google Scholar 

  12. 12.

    Smrz J, Catska V (1987) Food selection of the field population of Tyrophagus putrescentiae (Schrank) (Acari, Acarida). J Appl Entomol 104:329–335. https://doi.org/10.1111/j.1439-0418.1987.tb00533.x

    Article  Google Scholar 

  13. 13.

    Collins DA (2012) A review on the factors affecting mite growth in stored grain commodities. Exp Appl Acarol 56:191–208. https://doi.org/10.1007/s10493-012-9512-6

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Kavallieratos NG, Athanassiou CG, Guedes RNC, Drempela JD, Boukouvala MC (2017) Invader competition with local competitors: displacement or coexistence among the invasive khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), and two other major stored-grain beetles? Front Plant Sci 8:1837. https://doi.org/10.3389/fpls.2017.01837

    Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Shah JA, Vendl T, Aulicky R, Stejskal V (2020) Frass produced by the primary pest Rhyzopertha dominica supports the population growth of the secondary stored product pests Oryzaephilus surinamensis, Tribolium castaneum, and T. confusum. Bull Entomol Res (in press). https://doi.org/10.1017/S0007485320000425

  16. 16.

    Mason CJ, Campbell AM, Scully ED, Hoover K (2019) Bacterial and fungal midgut community dynamics and transfer between mother and brood in the Asian longhorned beetle (Anoplophora glabripennis), an invasive xylophage. Microb Ecol 77:230–242. https://doi.org/10.1007/s00248-018-1205-1

    Article  PubMed  Google Scholar 

  17. 17.

    Erban T, Rybanska D, Harant K, Hortova B, Hubert J (2016) Feces derived allergens of Tyrophagus putrescentiae reared on dried dog food and evidence of the strong nutritional interaction between the mite and Bacillus cereus producing protease bacillolysins and exo-chitinases. Front Physiol 7:53. https://doi.org/10.3389/fphys.2016.00053

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Hubert J, Nesvorna M, Sopko B, Smrz J, Klimov P, Erban T (2018) Two populations of mites (Tyrophagus putrescentiae) differ in response to feeding on feces-containing diets. Front Microbiol 9:2590. https://doi.org/10.3389/fmicb.2018.02590

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Tovey ER, Chapman MD, Platts-Mills TAE (1981) Mite faeces are a major source of house dust allergens. Nature 289:592–593. https://doi.org/10.1038/289592a0

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Stewart GA (1982) Isolation and characterization of the allergen Dpt 12 from Dermatophagoides pteronyssinus by chromatofocusing. Int Arch Allergy Appl Immunol 69:224–230. https://doi.org/10.1159/000233175

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Stewart GA, Lake FR (1991) Thompson PJ (1991) Faecally derived hydrolytic enzymes from Dermatophagoides pteronyssinus: physicochemical characterisation of potential allergens. Int Arch Allergy Appl Immunol 95:248–256. https://doi.org/10.1159/000235437

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Batard T, Hrabina A, Bi XZ, Chabre H, Lemoine P, Couret M-N, Faccenda D, Villet B, Harzic P, Andre F, Goh SY, Andre C, Chew FT, Moingeon P (2006) Production and proteomic characterization of pharmaceutical-grade Dermatophagoides pteronyssinus and Dermatophagoides farinae extracts for allergy vaccines. Int Arch Allergy Immunol 140:295–305. https://doi.org/10.1159/000093707

    Article  PubMed  Google Scholar 

  23. 23.

    Yella L, Morgan MS, Arlian LG (2013) Population growth and allergen accumulation of Dermatophagoides farinae cultured at 20 and 25 °C. Exp Appl Acarol 60:117–126. https://doi.org/10.1007/s10493-012-9626-x

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    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

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Hubert J, Doleckova-Maresova L, Hyblova J, Kudlikova I, Stejskal V, Mares M (2005) In vitro and in vivo inhibition of alpha-amylases of stored-product mite Acarus siro. Exp Appl Acarol 35:281–291. https://doi.org/10.1007/s10493-004-7834-8

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    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 (in Japanese with English summary)

    Article  Google Scholar 

  27. 27.

    Naqib A, Poggi S, Wang W, Hyde M, Kunstman K, Green SJ (2018) Making and sequencing heavily multiplexed, high-throughput 16S ribosomal RNA gene amplicon libraries using a flexible, two-stage PCR protocol. In: Raghavachari N, Garcia-Reyero N (eds) Gene expression analysis: methods in and protocols. Humana Press, New York, pp 149–169. https://doi.org/10.1007/978-1-4939-7834-2_7

    Chapter  Google Scholar 

  28. 28.

    Sakai M, Matsuka A, Komura T, Kanazawa S (2004) Application of a new PCR primer for terminal restriction fragment length polymorphism analysis of the bacterial communities in plant roots. J Microbiol Methods 59:81–89. https://doi.org/10.1016/j.mimet.2004.06.005

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    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. https://doi.org/10.1038/ismej.2012.8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    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 23 April 2020

  32. 32.

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Hubert J, Nesvorna M, Kopecky J, Erban T, Klimov P (2019) Population and culture age influence the microbiome profiles of house dust mites. Microb Ecol 77:1048–1066. https://doi.org/10.1007/s00248-018-1294-x

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Cole JR, Wang Q, Fish JA, Chai BL, McGarrell DM, Sun YN, 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

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Edgar RC (2016) SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences. bioRxiv. https://doi.org/10.1101/074161; https://www.biorxiv.org/content/10.1101/074161v1. Accessed 23 April 2020

  37. 37.

    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

    CAS  Article  Google Scholar 

  38. 38.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    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 

  40. 40.

    Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217. https://doi.org/10.1006/jmbi.2000.4042

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang J-M, Taly J-F, Notredame C (2011) T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39:W13–W17. https://doi.org/10.1093/nar/gkr245

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Rambaut A (2014) FigTree, a graphical viewer of phylogenetic trees: 2014-07-09 - v1.4.2. 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

  44. 44.

    Nesvorna M, Bittner V, Hubert J (2019) The mite Tyrophagus putrescentiae hosts population-specific microbiomes that respond weakly to starvation. Microb Ecol 77:488–501. https://doi.org/10.1007/s00248-018-1224-y

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Hammer O (2018). Past 3.x - the past of the future: current version (October 2018): 3.21. Natural History Museum, University of Oslo, Oslo, Norway. https://folk.uio.no/ohammer/past/. Accessed 23 April 2020

  46. 46.

    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 23 April 2020

  47. 47.

    Oksanen J (2019) Vegan: an introduction to ordination: processed with vegan 2.5-6 in R version 3.6.1 (2019-07-05) on August 31, 2019. https://cran.r-project.org/web/packages/vegan/vignettes/intro-vegan.pdf. Accessed 23 April 2020

  48. 48.

    Mair P, Wilcox R (2019) Package ‘WRS2’. June 6, 2019. https://cran.r-project.org/web/packages/WRS2/WRS2.pdf. Accessed 23 April 2020

  49. 49.

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

    Article  Google Scholar 

  50. 50.

    Zeleny D (2019) Analysis of community ecology data in R. DavidZeleny.net. https://www.davidzeleny.net/anadat-r/doku.php/en:start. Accessed 23 April 2020

  51. 51.

    PopGen (2018) Detecting multilocus adaptation using Redundancy Analysis (RDA). Population genetics in R. https://popgen.nescent.org/2018-03-27_RDA_GEA.html. Accessed 23 April 2020

  52. 52.

    Mair P, Wilcox R (2019) Robust statistical methods in R using the WRS2 package. J Stat Softw 20:1–32. https://doi.org/10.18637/jss.v000.i00; https://dornsife.usc.edu/assets/sites/239/docs/WRS2.pdf. Accessed 23 April 2020

  53. 53.

    Zele F, Santos I, Olivieri I, Weill M, Duron O, Magalhaes S (2018) Endosymbiont diversity and prevalence in herbivorous spider mite populations in South-Western Europe. FEMS Microbiol Ecol 94:fiy015. https://doi.org/10.1093/femsec/fiy015

    CAS  Article  Google Scholar 

  54. 54.

    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

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Erban T, Klimov P, Molva V, Hubert J (2020) Whole genomic sequencing and sex-dependent abundance estimation of Cardinium sp., a common and hyperabundant bacterial endosymbiont of the American house dust mite, Dermatophagoides farinae. Exp Appl Acarol 80:363–380. https://doi.org/10.1007/s10493-020-00475-5

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    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 

  57. 57.

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

    CAS  Article  PubMed  Google Scholar 

  58. 58.

    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 

  59. 59.

    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

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    Molva V, Bostlova M, Nesvorna M, Hubert J (2020) Do the microorganisms from laboratory culture spent growth medium affect house dust mite fitness and microbiome composition? Insect Sci 27:266–275. https://doi.org/10.1111/1744-7917.12636

    CAS  Article  PubMed  Google Scholar 

  61. 61.

    Nesvorna M, Sopko B, Hubert J (2020) Cardinium and Wolbachia are negatively correlated in the microbiome of various populations of stored product mite Tyrophagus putrescentiae. Int J Acarol 46:192–199. https://doi.org/10.1080/01647954.2020.1752305

    Article  Google Scholar 

  62. 62.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Lee J, Kim JY, M-h Y, Hwang Y, Lee I-Y, Nam S-H, Yong D, Yong T-S (2019) Comparative microbiome analysis of Dermatophagoides farinae, Dermatophagoides pteronyssinus, and Tyrophagus putrescentiae. J Allergy Clin Immunol 143:1620–1623. https://doi.org/10.1016/j.jaci.2018.10.062

    Article  PubMed  Google Scholar 

  64. 64.

    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. https://doi.org/10.1093/jee/tow089

    CAS  Article  PubMed  Google Scholar 

  65. 65.

    Hammer TJ, Janzen DH, Hallwachs W, Jaffe SP, Fierer N (2017) Caterpillars lack a resident gut microbiome. Proc Natl Acad Sci U S A 114:9641–9646. https://doi.org/10.1073/pnas.1707186114

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Murillo P, Klimov P, Hubert J, OConnor BM (2018) Investigating species boundaries using DNA and morphology in the mite Tyrophagus curvipenis (Acari: Acaridae), an emerging invasive pest, with a molecular phylogeny of the genus Tyrophagus. Exp Appl Acarol 75:167–189. https://doi.org/10.1007/s10493-018-0256-9

    Article  PubMed  Google Scholar 

  67. 67.

    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

    CAS  Article  PubMed  Google Scholar 

  68. 68.

    Swe PM, Zakrzewski M, Waddell R, Sriprakash KS, Fischer K (2019) High-throughput metagenome analysis of the Sarcoptes scabiei internal microbiota and in-situ identification of intestinal Streptomyces sp. Sci Rep 9:11744. https://doi.org/10.1038/s41598-019-47892-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Salem H, Florez L, Gerardo N, Kaltenpoth M (2015) An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc Biol Sci 282:20142957. https://doi.org/10.1098/rspb.2014.2957

    Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Onchuru TO, Martinez AJ, Ingham CS, Kaltenpoth M (2018) Transmission of mutualistic bacteria in social and gregarious insects. Curr Opin Insect Sci 28:50–58. https://doi.org/10.1016/j.cois.2018.05.002

    Article  PubMed  Google Scholar 

  71. 71.

    Zhu Y-X, Song Z-R, Song Y-L, Zhao D-S, Hong X-Y (2019) The microbiota in spider mite feces potentially reflects intestinal bacterial communities in the host. Insect Sci (in press). https://doi.org/10.1111/1744-7917.12716

  72. 72.

    Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A (2011) Bacterial communities of diverse Drosophila species: ecological context of a host–microbe model system. PLoS Genet 7:e1002272. https://doi.org/10.1371/journal.pgen.1002272

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. 73.

    Zindel R, Ofek M, Minz D, Palevsky E, Zchori-Fein E, Aebi A (2013) The role of the bacterial community in the nutritional ecology of the bulb mite Rhizoglyphus robini (Acari: Astigmata: Acaridae). FASEB J 27:1488–1497. https://doi.org/10.1096/fj.12-216242

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Martin Markovic for the help with manuscript formatting and Marie Bostlova and Natalie Hubertova for the valuable technical help.

Funding

JH and MN were supported by the Czech Science Foundation (GACR, grant no. GA19-09998S). PBK was supported by a grant from the Russian Science Foundation, project no. 19-14-00004.

Author information

Affiliations

Authors

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

(XLSX 267 kb)

ESM 2

(DOCX 1987 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hubert, J., Nesvorna, M., Green, S.J. et al. Microbial Communities of Stored Product Mites: Variation by Species and Population. Microb Ecol 81, 506–522 (2021). https://doi.org/10.1007/s00248-020-01581-y

Download citation

Keywords

  • Mite
  • Feeding
  • Feces
  • Eggs
  • Allergen
  • Symbionts
  • Cardinium
  • Wolbachia
  • Bartonella