Feces have been suggested as a major source of microorganisms for recolonization of the gut of stored product mites via coprophagy. The mites can host microorganisms that decrease their fitness, but their transmission is not known. To address the role of fecal microbiota on mite fitness, we performed an experimental study in which the surfaces of mite (Tyrophagus putrescentiae) eggs were sterilized. Mites eggs (15 per experimental box) were then hatched and grown on feedstock with and without feces. These experiments were conducted with four distinct T. putrescentiae populations (5L, 5K, 5N, and 5P), and mite population density after 21 day of cultivation was used to assess mite fitness and the impact of fecal microbiota on fitness. Population density was not affected by the presence of feces in two of the cultures (5L and 5K), while significant effects of feces were observed in the other cultures (5N and 5P). Mite culture microbial communities were analyzed using cultivation-independent next-generation amplicon sequencing of microbial 16S and 18S ribosomal RNA (rRNA) genes in the fitness influenced populations (5N and 5P). Several microbial taxa were associated with fecal treatments and reduced mite fitness, including Staphylococcus and Bartonella-like bacteria, and the fungal genera Yamadazyma, Candida, and Aspergillus. Although coprophagy is the transmission route mites used to obtain beneficial gut bacteria such as Bartonella-like organisms, the results of this study demonstrate that fecal-associated microorganisms can have negative effects on some populations of T. putrescentiae fitness, and this may counteract the positive effects of gut symbiont acquisition.

Crop Research Institute Prague Czechia

Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Prague Czechia

Genomics and Microbiome Core Facility Rush University Chicago IL United States

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Abbar S., Amoah B., Schilling M. W., Phillips T. W. (2016). Efficacy of selected food-safe compounds to prevent infestation of the ham mite, Tyrophagus putrescentiae (Schrank) (Acarina: Acaridae), on southern dry-cured hams. Pest Manag. Sci. 72 1604–1612. 10.1002/ps.4196 PubMed DOI

Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215 403–410. 10.1016/S0022-2836(05)80360-2 PubMed DOI

Anderson M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26 32–46. 10.1111/j.1442-9993.2001.01070.pp.x DOI

Aygun O., Yaman M., Durmaz H. (2007). A survey on occurrence of Tyrophagus putrescentiae (Acari: Acaridae) in surk, a traditional Turkish dairy product. J. Food Eng. 78 878–881. 10.1016/j.jfoodeng.2005.11.029 DOI

Baker A. S., Swan M. C. (2013). A puzzling domestic infestation of the storage mite Tyrophagus longior. J. Stored Prod. Res. 54 64–66. 10.1016/j.jspr.2013.05.004 DOI

Brazis P., Serra M., Selles A., Dethioux F., Biourge V., Puigdemont A. (2008). Evaluation of storage mite contamination of commercial dry dog food. Vet. Dermatol. 19 209–214. 10.1111/j.1365-3164.2008.00676.x PubMed DOI

Canfield M. S., Wrenn W. J. (2010). Tyrophagus putrescentiae mites grown in dog food cultures and the effect mould growth has on mite survival and reproduction. Vet. Dermatol. 21 58–63. 10.1111/j.1365-3164.2009.00778.x PubMed DOI

Clifford C. W., Fulk G. W. (1990). Association of diabetes, lash loss, and Staphylococcus aureus with infestation of eyelids by Demodex folliculorum (Acari: Demodicidae). J. Med. Entomol. 27 467–470. 10.1093/jmedent/27.4.467 PubMed DOI

Cole J. R., Wang Q., Fish J. A., Chai B. L., Mcgarrell D. M., Sun Y. N., et al. (2014). Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42 D633–D642. 10.1093/nar/gkt1244 PubMed DOI PMC

da Silva G. L., Esswein I. Z., Heidrich D., Dresch F., Maciel M. J., Pagani D. M., et al. (2019). Population growth of the stored product pest Tyrophaus putrescentiae (Acari: Acaridae) on environmentally and medically important fungi. Exp Appl Acarol 78 49–64. 10.1007/s10493-019-00370-8 PubMed DOI

Douglas A. E., Hart B. J. (1989). The significance of the fungus Aspergillus penicillioides to the house dust mite Dermatophagoides pteronyssinus. Symbiosis 7 105–116. PubMed

Edgar R. (2018a). Taxonomy annotation and guide tree errors in 16S rRNA databases. PeerJ 6:e5030. 10.7717/peerj.5030 PubMed DOI PMC

Edgar R. C. (2018b). Accuracy of taxonomy prediction for 16S rRNA and fungal ITS sequences. PeerJ 6:e4652. 10.7717/peerj.4652 PubMed DOI PMC

Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10 996–998. 10.1038/nmeth.2604 PubMed DOI

Engel P., Moran N. A. (2013). The gut microbiota of insects – diversity in structure and function. FEMS Microbiol. Rev. 37 699–735. 10.1111/1574-6976.12025 PubMed DOI

Erban T., Rybanska D., Harant K., Hortova B., Hubert J. (2016b). 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. 10.3389/fphys.2016.00053 PubMed DOI PMC

Erban T., Klimov P. B., Smrz J., Phillips T. W., Nesvorna M., Kopecky J., et al. (2016a). Populations of stored product mite Tyrophagus putrescentiae differ in their bacterial communities. Front. Microbiol. 7:1046. 10.3389/fmicb.2016.01046 PubMed DOI PMC

Franzolin M. R., Gambale W., Cuero R. G., Correa B. (1999). Interaction between toxigenic Aspergillus flavus Link and mites (Tyrophagus putrescentiae Schrank) on maize grains: effects on fungal growth and aflatoxin production. J. Stored Prod. Res. 35 215–224. 10.1016/S0022-474X(99)00006-5 DOI

Garcia N. (2004). Efforts to control mites on Iberian ham by physical methods. Exp. Appl. Acarol. 32 41–50. 10.1023/b:appa.0000018165.80420.c9 PubMed DOI

Gihring T. M., Green S. J., Schadt C. W. (2012). Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes. Environ. Microbiol. 14 285–290. 10.1111/j.1462-2920.2011.02550.x PubMed DOI

Griffiths D. A., Hodson A. C., Christensen C. M. (1959). Grain storage fungi associated with mites. J. Econ. Entomol. 52 514–518. 10.1093/jee/52.3.514 DOI

Hammer O., Harper D. A. T., Ryan P. D. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4:4. Available online at: https://palaeo-electronica.org/2001_1/past/issue1_01.htm (accessed March 15, 2018).

Hay D. B., Hart B. J., Douglas A. E. (1992). Evidence refuting the contribution of the fungus Aspergillus penicillioides to the allergenicity of the house dust mite Dermatophagoides pteronyssinus. Int. Arch. Allergy Immunol. 97 86–88. 10.1159/000236100 PubMed DOI

Hay D. B., Hart B. J., Douglas A. E. (1993). Effects of the fungus Aspergillus penicillioides on the house dust mite Dermatophagoides pteronyssinus: an experimental re-evaluation. Med. Vet. Entomol. 7 271–274. 10.1111/j.1365-2915.1993.tb00687.x PubMed DOI

Hogg J. C., Lehane M. J. (1999). Identification of bacterial species associated with the sheep scab mite (Psoroptes ovis) by using amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 65 4227–4229. 10.1128/aem.65.9.4227-4229.1999 PubMed DOI PMC

Hosokawa T., Fukatsu T. (2020). Relevance of microbial symbiosis to insect behavior. Curr. Opin. Insect Sci. 39 91–100. 10.1016/j.cois.2020.03.004 PubMed DOI

Hubert J., Nesvorna M., Green S. J., Klimov P. B. (2021). Microbial communities of stored product mites: variation by species and population. Microb. Ecol. 81 506–522. 10.1007/s00248-020-01581-y PubMed DOI

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. 10.3389/fmicb.2018.02590 PubMed DOI PMC

Hubert J., Zilova M., Pekar S. (2001). Feeding preferences and gut contents of three panphytophagous oribatid mites (Acari: Oribatida). Eur. J. Soil Biol. 37 197–208. 10.1016/S1164-5563(01)01083-4 DOI

Jahnes B. C., Herrmann M., Sabree Z. L. (2019). Conspecific coprophagy stimulates normal development in a germ-free model invertebrate. PeerJ 7:e6914. 10.7717/peerj.6914 PubMed DOI PMC

Karamipour N., Fathipour Y., Mehrabadi M. (2016). Gammaproteobacteria as essential primary symbionts in the striped shield bug, Graphosoma lineatum (Hemiptera: Pentatomidae). Sci. Rep. 6:33168. 10.1038/srep33168 PubMed DOI PMC

Klimov P., Molva V., Nesvorna M., Pekar S., Shcherbachenko E., Erban T., et al. (2019). Dynamics of the microbial community during growth of the house dust mite Dermatophagoides farinae in culture. FEMS Microbiol. Ecol. 95:fiz153. 10.1093/femsec/fiz153 PubMed DOI

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. 10.1371/journal.pone.0112919 PubMed DOI PMC

Kozich J. J., Westcott S. L., Baxter N. T., Highlander S. K., Schloss P. D. (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. 10.1128/Aem.01043-13 PubMed DOI PMC

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

Legendre P., Anderson M. J. (1999). Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol. Monogr. 69 1–24. 10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2 DOI

Levinson H. Z., Levinson A. R., Muller K. (1991a). The adaptive function of ammonia and guanine in the biocoenotic association between ascomycetes and flour mites (Acarus siro L.). Naturwissenschaften 78 174–176. 10.1007/BF01136207 DOI

Levinson H. Z., Levinson A. R., Muller K. (1991b). Functional adaptation of two nitrogenous waste products in evoking attraction and aggregation of flour mites (Acarus siro L.). Anz. Schadlingskde Pflanzenschutz Umweltschutz 64 55–60. 10.1007/BF01909743 DOI

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. Jpn. J. Sanit. Zool. 16 118–122. (in Japanese with English summary), 10.7601/mez.16.118 DOI

Molva V., Nesvorna M., Hubert J. (2019). Feeding interactions between microorganisms and the house dust mites Dermatophagoides pteronyssinus and Dermatophagoides farinae (Astigmata: Pyroglyphidae). J. Med. Entomol. 56, 1669–1677. 10.1093/jme/tjz089 PubMed DOI

Mueller D. K., Kelley P. J., VanRyckeghem A. R. (2006). “Mold mites Tyrophagus putrescentiae (Schrank) in stored products,” in Proceedings of the 9th International Working Conference on Stored Product Protection, 15 to 18 October 2006, Campinas, Sao Paulo, Brazil, eds Lorini I., Bacaltchuk B., Beckel H., Deckers D., Sundfeld E., dos Santos J. P., et al. (Passo Fundo: Brazilian Post-harvest Association - ABRAPOS; ), 1117–1122.

Nalepa C. A., Bignell D. E., Bandi C. (2001). Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera. Insect. Soc. 48 194–201. 10.1007/PL00001767 DOI

Naqib A., Poggi S., Wang W., Hyde M., Kunstman K., Green S. J. (2018). “Making and sequencing heavily multiplexed, high-throughput 16S ribosomal RNA gene amplicon libraries using a flexible, two-stage PCR protocol,” in Gene Expression Analysis: Methods and Protocols, eds Raghavachari N., Garcia-Reyero N. (New York, NY: Humana Press; ), 149–169. 10.1007/978-1-4939-7834-2_7 PubMed DOI

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. 10.1007/s00248-018-1224-y PubMed DOI

Nesvorna M., Pekar S., Shcherbachenko E., Molva V., Erban T., Green S. J., et al. (2021). Microbiome variation during culture growth of the European house dust mite, Dermatophagoides pteronyssinus. FEMS Microbiol. Ecol. 97:fiab039. 10.1093/femsec/fiab039 PubMed DOI

Oksanen J. (2017). vegan v2.4-2: Community Ecology Package. RDocumentation. Available online at: https://www.rdocumentation.org/packages/vegan/versions/2.4-2 (accessed March 15, 2018).

Oliveira A. M., MacKellar A., Hume L., Huntley J. F., Thoday K. L., van den Broek A. H. M. (2006). Immune responses to Staphylococcus aureus and Psoroptes ovis in sheep infected with P. ovis — the sheep scab mite. Vet. Immunol. Immunopathol. 113 64–72. 10.1016/j.vetimm.2006.04.005 PubMed DOI

Onchuru T. O., Martinez A. J., Ingham C. S., Kaltenpoth M. (2018). Transmission of mutualistic bacteria in social and gregarious insects. Curr. Opin. Insect Sci. 28 50–58. 10.1016/j.cois.2018.05.002 PubMed DOI

Pekar S., Hubert J. (2008). Assessing biological control of Acarus siro by Cheyletus malaccensis under laboratory conditions: effect of temperatures and prey density. J. Stored Prod. Res. 44 335–340. 10.1016/j.jspr.2008.02.011 DOI

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41 D590–D596. 10.1093/nar/gks1219 PubMed DOI PMC

R Development Core Team (2017). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available online at: http://www.R-project.org (accessed March 15, 2018).

Rognes T., Flouri T., Nichols B., Quince C., Mahe F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. 10.7717/peerj.2584 PubMed DOI PMC

Rybanska D., Hubert J., Markovic M., Erban T. (2016). Dry dog food integrity and mite strain influence the density-dependent growth of the stored-product mite Tyrophagus putrescentiae (Acari: Acaridida). J. Econ. Entomol. 109 454–460. 10.1093/jee/tov298 PubMed DOI

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

Salem H., Onchuru T. O., Bauer E., Kaltenpoth M. (2015b). Symbiont transmission entails the risk of parasite infection. Biol. Lett. 11:20150840. 10.1098/rsbl.2015.0840 PubMed DOI PMC

Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75 7537–7541. 10.1128/Aem.01541-09 PubMed DOI PMC

Smrz J., Catska V. (1989). The effect of the consumption of some soil fungi on the internal microanatomy of the mite Tyrophagus putrescentiae (Schrank) (Acari, Acaridida). Acta Univ. Carol. Biol. 33 81–93.

Sobotnik J., Alberti G., Weyda F., Hubert J. (2008). Ultrastructure of the digestive tract in Acarus siro (Acari: Acaridida). J. Morphol. 269 54–71. 10.1002/jmor.10573 PubMed DOI

Suh S.-O., Nguyen N. H., Blackwell M. (2008). Yeasts isolated from plant-associated beetles and other insects: seven novel Candida species near Candida albicans. FEMS Yeast Res. 8 88–102. 10.1111/j.1567-1364.2007.00320.x PubMed DOI

Valerio C. R., Murray P., Arlian L. G., Slater J. E. (2005). Bacterial 16S ribosomal DNA in house dust mite cultures. J. Allergy Clin. Immunol. 116 1296–1300. 10.1016/j.jaci.2005.09.046 PubMed DOI

Wada-Katsumata A., Zurek L., Nalyanya G., Roelofs W. L., Zhang A., Schal C. (2015). Gut bacteria mediate aggregation in the German cockroach. Proc. Natl. Acad. Sci. U.S.A. 112 15678–15683. 10.1073/pnas.1504031112 PubMed DOI PMC

Walters W., Hyde E. R., Berg-Lyons D., Ackermann G., Humphrey G., Parada A., et al. (2016). Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1:e00009-15. 10.1128/mSystems.00009-15 PubMed DOI PMC

Werren J. H. (1997). Biology of Wolbachia. Annu. Rev. Entomol. 42 587–609. 10.1146/annurev.ento.42.1.587 PubMed DOI

A novel Bartonella-like bacterium forms an interdependent mutualistic symbiosis with its host, the stored-product mite Tyrophagus putrescentiae