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
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
26941650
PubMed Central
PMC4764834
DOI
10.3389/fphys.2016.00053
Knihovny.cz E-zdroje
- Klíčová slova
- Bacillus cereus, Tyrophagus putrescentiae, allergen, bacillolysin, exochitinase, nutrition, protease, symbiosis,
- Publikační typ
- časopisecké články MeSH
Tyrophagus putrescentiae (Schrank, 1781) is an emerging source of allergens in stored products and homes. Feces proteases are the major allergens of astigmatid mites (Acari: Acaridida). In addition, the mites are carriers of microorganisms and microbial adjuvant compounds that stimulate innate signaling pathways. We sought to analyze the mite feces proteome, proteolytic activities, and mite-bacterial interaction in dry dog food (DDF). Proteomic methods comprising enzymatic and zymographic analysis of proteases and 2D-E-MS/MS were performed. The highest protease activity was assigned to trypsin-like proteases; lower activity was assigned to chymotrypsin-like proteases, and the cysteine protease cathepsin B-like had very low activity. The 2D-E-MS/MS proteomic analysis identified mite trypsin allergen Tyr p3, fatty acid-binding protein Tyr p13 and putative mite allergens ferritin (Grp 30) and (poly)ubiquitins. Tyr p3 was detected at different positions of the 2D-E. It indicates presence of zymogen at basic pI, and mature-enzyme form and enzyme fragment at acidic pI. Bacillolysins (neutral and alkaline proteases) of Bacillus cereus symbiont can contribute to the protease activity of the mite extract. The bacterial exo-chitinases likely contribute to degradation of mite exuviae, mite bodies or food boluses consisting of chitin, including the peritrophic membrane. Thus, the chitinases disrupt the feces and facilitate release of the allergens. B. cereus was isolated and identified based on amplification and sequencing of 16S rRNA and motB genes. B. cereus was added into high-fat, high-protein (DDF) and low-fat, low-protein (flour) diets to 1 and 5% (w/w), and the diets palatability was evaluated in 21-day population growth test. The supplementation of diet with B. cereus significantly suppressed population growth and the suppressive effect was higher in the high-fat, high-protein diet than in the low-fat, low-protein food. Thus, B. cereus has to coexist with the mite in balance to be beneficial for the mite. The mite-B. cereus symbiosis can be beneficial-suppressive at some level. The results increase the veterinary and medical importance of the allergens detected in feces. The B. cereus enzymes/toxins are important components of mite allergens. The strong symbiotic association of T. putrescentiae with B. cereus in DDF was indicated.
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Adigüzel A. C., Bitlisli B. O., Yasa I., Eriksen N. T. (2009). Sequential secretion of collagenolytic, elastolytic, and keratinolytic proteases in peptide-limited cultures of two Bacillus cereus strains isolated from wool. J. Appl. Microbiol. 107, 226–234. 10.1111/j.1365-2672.2009.04200.x PubMed DOI
Altincicek B., Linder M., Linder D., Preissner K. T., Vilcinskas A. (2007). Microbial metalloproteinases mediate sensing of invading pathogens and activate innate immune responses in the lepidopteran model host Galleria mellonella. Infect. Immun. 75, 175–183. 10.1128/IAI.01385-06 PubMed DOI PMC
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
Arlian L. G., Geis D. P., Vyszenski-Moher D. L., Bernstein I. L., Gallagher J. S. (1984). Antigenic and allergenic properties of the storage mite Tyrophagus putrescentiae. J. Allergy Clin. Immunol. 74, 166–171. 10.1016/0091-6749(84)90281-1 PubMed DOI
Armitage D. M., George C. L. (1986). The effect of three species of mites upon fungal growth on wheat. Exp. Appl. Acarol. 2, 111–124. 10.1007/BF01213755 PubMed DOI
Athanassiou C. G., Palyvos N. E., Eliopoulos P. A., Papadoulis G. T. (2002). Mites associated with stored seed cotton and related products in Greece. Phytoparasitica 30, 387–394. 10.1007/BF02979686 DOI
Barbieri E., Paster B. J., Hughes D., Zurek L., Moser D. P., Teske A., et al. . (2001). Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda: Loliginidae). Environ. Microbiol. 3, 151–167. 10.1046/j.1462-2920.2001.00172.x PubMed DOI
Bottone E. J. (2010). Bacillus cereus, a volatile human pathogen. Clin. Microbiol. Rev. 23, 382–398. 10.1128/CMR.00073-09 PubMed DOI PMC
Bravo C. M., Ortiz I. L., Soto A. O., Vazquez R. G. (1999). Allergy to storage mites. Allergy 54, 769–770. 10.1034/j.1398-9995.1999.00057.x PubMed 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
Cardamone J. M. (2002). Proteolytic activity of Aspergillus flavus on wool. AATCC Rev. 2, 30–35.
Colloff M. J., Spieksma F. T. M. (1992). Pictorial keys for the identification of domestic mites. Clin. Exp. Allergy 22, 823–830. 10.1111/j.1365-2222.1992.tb02826.x PubMed DOI
de Boer R., van der Hoeven W. A., Stapel S. O. (1995). The decay of house dust mite allergens, Der p I and Der p II, under natural conditions. Clin. Exp. Allergy 25, 765–770. 10.1111/j.1365-2222.1995.tb00015.x PubMed DOI
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. 10.1093/jmedent/24.4.408 PubMed DOI
Didelot X., Barker M., Falush D., Priest F. G. (2009). Evolution of pathogenicity in the Bacillus cereus group. Syst. Appl. Microbiol. 32, 81–90. 10.1016/j.syapm.2009.01.001 PubMed DOI
Douwes J., Zuidhof A., Doekes G., van der Zee S. C., Wouters I., Boezen M. H., et al. . (2000). (1 → 3)-beta-D-glucan and endotoxin in house dust and peak flow variability in children. Am. J. Respir. Crit. Care Med. 162, 1348–1354. 10.1164/ajrccm.162.4.9909118 PubMed DOI
Drobniewski F. A. (1993). Bacillus cereus and related species. Clin. Microbiol. Rev. 6, 324–338. 10.1128/CMR.6.4.324 PubMed DOI PMC
Elder B. L., Morgan M. S., Arlian L. G. (2012). Effect of stored product mite extracts on human dermal microvascular endothelial cells. J. Med. Entomol. 49, 1411–1418. 10.1603/ME12142 PubMed DOI PMC
Erban T., Erbanova M., Nesvorna M., Hubert J. (2009a). The importance of starch and sucrose digestion in nutritive biology of synanthropic acaridid mites: alpha-amylases and alpha-glucosidases are suitable targets for inhibitor-based strategies of mite control. Arch. Insect Biochem. Physiol. 71, 139–158. 10.1002/arch.20312 PubMed DOI
Erban T., Harant K., Hubalek M., Vitamvas P., Kamler M., Poltronieri P., et al. . (2015a). In-depth proteomic analysis of Varroa destructor: detection of DWV-complex, ABPV, VdMLV and honeybee proteins in the mite. Sci. Rep. 5:13907. 10.1038/srep13907 PubMed DOI PMC
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. 10.1007/s10493-008-9138-x PubMed DOI
Erban T., Hubert J. (2010a). Comparative analyses of proteolytic activities in seven species of synanthropic acaridid mites. Arch. Insect Biochem. Physiol. 75, 187–206. 10.1002/arch.20388 PubMed DOI
Erban T., Hubert J. (2010b). Determination of pH in regions of the midguts of acaridid mites. J. Insect Sci. 10:42. 10.1673/031.010.4201 PubMed DOI PMC
Erban T., Hubert J. (2011). Visualization of protein digestion in the midgut of the acarid mite Lepidoglyphus destructor. Arch. Insect Biochem. Physiol. 78, 74–86. 10.1002/arch.20441 PubMed DOI
Erban T., Hubert J. (2015). Two-dimensional gel proteomic analysis of Dermatophagoides farinae feces. Exp. Appl. Acarol. 65, 73–87. 10.1007/s10493-014-9848-1 PubMed DOI
Erban T., Nesvorna M., Erbanova M., Hubert J. (2009b). Bacillus thuringiensis var. tenebrionis control of synanthropic mites (Acari: Acaridida) under laboratory conditions. Exp. Appl. Acarol. 49, 339–346. 10.1007/s10493-009-9265-z PubMed DOI
Erban T., Rybanska D., Hubert J. (2015b). Population growth of the generalist mite Tyrophagus putrescentiae (Acari: Acaridida) following adaptation to high- or low-fat and high- or low-protein diets and the effect of dietary switch. Environ. Entomol. 44, 1599–1604. 10.1093/ee/nvv129 PubMed DOI
Feder J., Keay L., Garrett L. R., Cirulis N., Moseley M. H., Wildi B. S. (1971). Bacillus cereus neutral protease. Biochim. Biophys. Acta Protein Struct. 251, 74–78. 10.1016/0005-2795(71)90061-4 PubMed DOI
Fekete T. (2010). Bacillus species and related genera other than Bacillus anthracis, in Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases, 7th Edn., eds Mandell G. L., Bennett J. E., Dolin E. (Philadelphia, PA: Churchill Livingstone/Elsevier; ), 2727–2731. 10.1016/B978-0-443-06839-3.00209-5 DOI
Flach J., Pilet P. E., Jolles P. (1992). What's new in chitinase research? Experientia 48, 701–716. 10.1007/BF02124285 PubMed DOI
Gámez C., Zafra M., Boquete M., Sanz V., Mazzeo C., Ibáñez M. D., et al. . (2014). New shrimp IgE-binding proteins involved in mite-seafood cross-reactivity. Mol. Nutr. Food Res. 58, 1915–1925. 10.1002/mnfr.201400122 PubMed DOI
Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R. D., Bairoch A. (2003). ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31, 3784–3788. 10.1093/nar/gkg563 PubMed DOI PMC
Gill C., McEwan N., McGarry J., Nuttall T. (2011). House dust and storage mite contamination of dry dog food stored in open bags and sealed boxes in 10 domestic households. Vet. Dermatol. 22, 162–172. 10.1111/j.1365-3164.2010.00931.x PubMed DOI
Gunderson A. R. (2008). Feather-degrading bacteria: a new frontier in avian and host–parasite research. Auk 125, 972–979. 10.1525/auk.2008.91008 DOI
Gupta R., Beg Q. K., Khan S., Chauhan B. (2002). An overview on fermentation, downstream processing and properties of microbial alkaline proteases. Appl. Microbiol. Biotechnol. 60, 381–395. 10.1007/s00253-002-1142-1 PubMed DOI
Häggblom M. M., Apetroaie C., Andersson M. A., Salkinoja-Salonen M. S. (2002). Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced under various conditions. Appl. Environ. Microbiol. 68, 2479–2483. 10.1128/AEM.68.5.2479-2483.2002 PubMed DOI PMC
Hamid R., Khan M. A., Ahmad M., Ahmad M. M., Abdin M. Z., Musarrat J., et al. . (2013). Chitinases: an update. J. Pharm. Bioallied Sci. 5, 21–29. 10.4103/0975-7406.106559 PubMed DOI PMC
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
Holmquist B., Vallee B. L. (1976). Esterase activity of zinc neutral proteases. Biochemistry 15, 101–107. 10.1021/bi00646a016 PubMed DOI
Huang Y. J., Nariya S., Harris J. M., Lynch S. V., Choy D. F., Arron J. R., et al. . (2015). The airway microbiome in patients with severe asthma: associations with disease features and severity. J. Allergy Clin. Immunol. 136, 874–884. 10.1016/j.jaci.2015.05.044 PubMed DOI PMC
Hubert J., Kopecky J., Perotti M. A., Nesvorna M., Braig H. R., Sagova-Mareckova M., et al. . (2012a). Detection and identification of species-specific bacteria associated with synanthropic mites. Microb. Ecol. 63, 919–928. 10.1007/s00248-011-9969-6 PubMed DOI
Hubert J., Nesvorna M., Erban T. (2014). Growth-suppressive effect of the alpha-amylase inhibitor of Triticum aestivum on stored-product mites varies by the species and type of diet. Exp. Appl. Acarol. 62, 57–65. 10.1007/s10493-013-9718-2 PubMed DOI
Hubert J., Nesvorna M., Sagova-Mareckova M., Kopecky J. (2012b). Shift of bacterial community in synanthropic mite Tyrophagus putrescentiae induced by Fusarium fungal diet. PLoS ONE 7:e48429. 10.1371/journal.pone.0048429 PubMed DOI PMC
Hubert J., Stejskal V., Kubatova A., Munzbergova Z., Vanova M., Zdarkova E. (2003). Mites as selective fungal carriers in stored grain habitats. Exp. Appl. Acarol. 29, 69–87. 10.1023/A:1024271107703 PubMed DOI
Hubert J., Stejskal V., Munzbergova Z., Kubatova A., Vanova M., Zdarkova E. (2004). Mites and fungi in heavily infested stores in the Czech Republic. J. Econ. Entomol. 97, 2144–2153. 10.1093/jee/97.6.2144 PubMed DOI
Hughes A. M. (1976). The Mites of Stored Food and Houses: Technical Bulletin of the Ministry of Agriculture, Fisheries and Food, 2nd Edn. London: Her Majesty's Stationery Office.
Jacquet A. (2013). Innate immune responses in house dust mite allergy. ISRN Allergy 2013:735031. 10.1155/2013/735031 PubMed DOI PMC
Jeong S. K., Kim H. J., Youm J.-K., Ahn S. K., Choi E. H., Sohn M. H., et al. . (2008). Mite and cockroach allergens activate protease-activated receptor 2 and delay epidermal permeability barrier recovery. J. Invest. Dermatol. 128, 1930–1939. 10.1038/jid.2008.13 PubMed DOI
Jiang H., Dong H., Zhang G., Yu B., Chapman L. R., Fields M. W. (2006). Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl. Environ. Microbiol. 72, 3832–3845. 10.1128/AEM.02869-05 PubMed DOI PMC
Klimov P. B., OConnor B. M. (2015). Comment on Acarus putrescentiae Schrank, 1781 (currently Tyrophagus putrescentiae; Acariformes, Acaridae): proposed conservation of usage by designation of a replacement neotype. Bull. Zool. Nomencl. 72, 50–56.
Kondo S., Helin H., Shichijo M., Bacon K. B. (2004). Cockroach allergen extract stimulates protease-activated receptor-2 (PAR-2) expressed in mouse lung fibroblast. Inflamm. Res. 53, 489–496. 10.1007/s00011-004-1287-8 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
Lambrecht B. N., Hammad H. (2012). The airway epithelium in asthma. Nat. Med. 18, 684–692. 10.1038/nm.2737 PubMed DOI
Lee C. G., Da Silva C. A., Lee J.-Y., Hartl D., Elias J. A. (2008). Chitin regulation of immune responses: an old molecule with new roles. Curr. Opin. Immunol. 20, 684–689. 10.1016/j.coi.2008.10.002 PubMed DOI PMC
Mack I., Hector A., Ballbach M., Kohlhaufl J., Fuchs K. J., Weber A., et al. . (2015). The role of chitin, chitinases, and chitinase-like proteins in pediatric lung diseases. Mol. Cell. Pediatr. 2:3. 10.1186/s40348-015-0014-6 PubMed DOI PMC
Manjula K., Podile A. R. (2005). Production of fungal cell wall degrading enzymes by a biocontrol strain of Bacillus subtilis AF 1. Indian J. Exp. Biol. 43, 892–896. PubMed
Margulis L., Jorgensen J. Z., Dolan S., Kolchinsky R., Rainey F. A., Lo S.-C. (1998). The Arthromitus stage of Bacillus cereus: intestinal symbionts of animals. Proc. Natl. Acad. Sci. U.S.A. 95, 1236–1241. 10.1073/pnas.95.3.1236 PubMed DOI PMC
Marsella R., Saridomichelakis M. N. (2010). Environmental and oral challenge with storage mites in beagles experimentally sensitized to Dermatophagoides farinae. Vet. Dermatol. 21, 106–112. 10.1111/j.1365-3164.2009.00859.x PubMed DOI
Martinez J. P., Falomir M. P., Gozalbo D. (2014). Chitin: a structural biopolysaccharide with multiple applications, in eLS (John Wiley & Sons, Ltd.). 10.1002/9780470015902.a0000694.pub3 DOI
McCall C., Hunter S., Stedman K., Weber E., Hillier A., Bozic C., et al. . (2001). Characterization and cloning of a major high molecular weight house dust mite allergen (Der f 15) for dogs. Vet. Immunol. Immunopathol. 78, 231–247. 10.1016/S0165-2427(00)00258-0 PubMed DOI
Mercado D., Boluda L., Caraballo L., Fernandez-Caldas E. (2003). Identification of ubiquitin as a low molecular weight allergen of Blomia tropicalis (Bt). J. Allergy Clin. Immunol. 111, S326 10.1016/s0091-6749(03)81188-0 DOI
Morihara K., Tsuzuki H., Oka T. (1968). Comparison of the specificities of various neutral proteinases from microorganisms. Arch. Biochem. Biophys. 123, 572–588. 10.1016/0003-9861(68)90179-3 PubMed DOI
Muhsin T. M., Hadi R. B. (2002). Degradation of keratin substrates by fungi isolated from sewage sludge. Mycopathologia 154, 185–189. 10.1023/A:1016335623534 PubMed DOI
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. 10.1080/09603123.2012.699029 PubMed DOI
Nicholson J. K., Holmes E., Kinross J., Burcelin R., Gibson G., Jia W., et al. . (2012). Host-gut microbiota metabolic interactions. Science 336, 1262–1267. 10.1126/science.1223813 PubMed DOI
OConnor B. M. (1979). Evolutionary origins of astigmatid mites inhabiting stored products, in Recent Advances in Acarology, Vol. 1, Proceedings of the V International Congress of Acarology, held August 6-12, 1978 at Michigan State University, East Lansing, Michigan, ed Rodriguez G. J. (New York, NY; San Francisco, CA; London: Academic Press; ), 273–278.
OConnor B. M. (1982). Evolutionary ecology of astigmatid mites. Annu. Rev. Entomol. 27, 385–409. 10.1146/annurev.en.27.010182.002125 DOI
OConnor B. M. (1984). Acarine-fungal relationships: the evolution of symbiotic associations, in Fungus-Insect Relationships: Perspectives in Ecology and Evolution, ed. Wheeler Q., Blackwell M. (New York, NY; Guildford: Columbia University Press; ), 354–381.
Oliwa-Stasiak K., Molnar C. I., Arshak K., Bartoszcze M., Adley C. C. (2010). Development of a PCR assay for identification of the Bacillus cereus group species. J. Appl. Microbiol. 108, 266–273. 10.1111/j.1365-2672.2009.04419.x PubMed DOI
Ortego F., Sanchez-Ramos I., Ruiz M., Castanera P. (2000). Characterization of proteases from a stored product mite, Tyrophagus putrescentiae. Arch. Insect Biochem. Physiol. 43, 116–124. 10.1002/(SICI)1520-6327(200003) PubMed DOI
Park J. W., Ko S. H., Yong T.-S., Ree H.-I., Jeoung B.-J., Hong C.-S. (1999). Cross-reactivity of Tyrophagus putrescentiae with Dermatophagoides farinae and Dermatophagoides pteronyssinus in urban areas. Ann. Allergy Asthma Immunol. 83, 533–539. 10.1016/S1081-1206(10)62865-7 PubMed DOI
Platts-Mills T. A. E., Woodfolk J. A. (2011). Allergens and their role in the allergic immune response. Immunol. Rev. 242, 51–68. 10.1111/j.1600-065X.2011.01021.x PubMed DOI
Podile A. R., Prakash A. P. (1996). Lysis and biological control of Aspergillus niger by Bacillus subtilis AF 1. Can. J. Microbiol. 42, 533–538. 10.1139/m96-072 PubMed DOI
Podile A. R., Prasad G. S., Dube H. C. (1985). Bacillus subtilis as antagonist to vascular wilt pathogens. Curr. Sci. 54, 864–865.
Priest F. G. (1977). Extracellular enzyme synthesis in genus Bacillus. Bacteriol. Rev. 41, 711–753. PubMed PMC
Ribeiro N. F. F., Heath C. H., Kierath J., Rea S., Duncan-Smith M., Wood F. M. (2010). Burn wounds infected by contaminated water: case reports, review of the literature and recommendations for treatment. Burns 36, 9–22. 10.1016/j.burns.2009.03.002 PubMed DOI
Roelandt T., Heughebaert C., Hachem J.-P. (2008). Proteolytically active allergens cause barrier breakdown. J. Invest. Dermatol. 128, 1878–1880. 10.1038/jid.2008.168 PubMed DOI
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
Saleh S. M., Kelada N. L., Shaker N. (1991). Control of European house dust mite Dermatophagoides pteronyssinus (Trouessart) with Bacillus spp. Acarologia 32, 257–260.
Saridomichelakis M. N., Marsella R., Lee K. W., Esch R. E., Farmaki R., Koutinas A. F. (2008). Assessment of cross-reactivity among five species of house dust and storage mites. Vet. Dermatol. 19, 67–76. 10.1111/j.1365-3164.2008.00654.x PubMed DOI
Sidenius K. E., Hallas T. E., Stenderup J., Poulsen L. K., Mosbech H. (2002). Decay of house-dust mite allergen Der f 1 at indoor climatic conditions. Ann. Allergy Asthma Immunol. 89, 34–37. 10.1016/S1081-1206(10)61908-4 PubMed DOI
Sidler W., Niederer E., Suter F., Zuber H. (1986). The primary structure of Bacillus cereus neutral proteinase and comparison with thermolysin and Bacillus subtilis neutral proteinase. Biol. Chem. Hoppe-Seyler 367, 643–657. 10.1515/bchm3.1986.367.2.643 PubMed DOI
Sinha R. N. (1966). Feeding and reproduction of some stored-product mites on seed-borne fungi. J. Econ. Entomol. 59, 1227–1232.
Smrz J. (2003). Microanatomical and biological aspects of bacterial associations in Tyrophagus putrescentiae (Acari: Acaridida). Exp. Appl. Acarol. 31, 105–113. 10.1023/B:APPA.0000005111.05959.d6 PubMed DOI
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.
Smrz J., Catska V. (2010). Mycophagous mites and their internal associated bacteria cooperate to digest chitin in soil. Symbiosis 52, 33–40. 10.1007/s13199-010-0099-6 DOI
Smrz J., Jungova E. (1989). The ecology of a field population of Tyrophagus putrescentiae (Acari, Acaridida). Pedobiologia 33, 183–192.
Sobotnik J., Alberti G., Weyda F., Hubert J. (2008a). Ultrastructure of the digestive tract in Acarus siro (Acari: Acaridida). J. Morphol. 269, 54–71. 10.1002/jmor.10573 PubMed DOI
Sobotnik J., Kudlikova-Krizkova I., Vancova M., Munzbergova Z., Hubert J. (2008b). Chitin in the peritrophic membrane of Acarus siro (Acari: Acaridae) as a target for novel acaricides. J. Econ. Entomol. 101, 1028–1033. 10.1603/0022-0493(2008)101[1028:CITPMO]2.0.CO;2 PubMed DOI
Stara J., Erban T., Hubert J. (2010). The effect of chitin metabolic effectors on the population increase of stored product mites. Exp. Appl. Acarol. 52, 155–167. 10.1007/s10493-010-9352-1 PubMed DOI
Staubach F., Baines J. F., Kunzel S., Bik E. M., Petrov D. A. (2013). Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS ONE 8:e70749. 10.1371/journal.pone.0070749 PubMed DOI PMC
Stenfors Arnesen L. P., Fagerlund A., Granum P. E. (2008). From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 32, 579–606. 10.1111/j.1574-6976.2008.00112.x PubMed DOI
Stewart G. A., Lake F. R., Thompson P. J. (1991). Faecally derived hydrolytic enzymes from Dermatophagoides pteronyssinus: physicochemical characterisation of potential allergens. Int. Arch. Allergy Appl. Immunol. 95, 248–256. 10.1159/000235437 PubMed DOI
Swiecicka I., Mahillon J. (2006). Diversity of commensal Bacillus cereus sensu lato isolated from the common sow bug (Porcellio scaber, Isopoda). FEMS Microbiol. Ecol. 56, 132–140. 10.1111/j.1574-6941.2006.00063.x PubMed DOI
Tang V. H., Chang B. J., Srinivasan A., Mathaba L. T., Harnett G. B., Stewart G. A. (2013). Skin-associated Bacillus, staphylococcal and micrococcal species from the house dust mite, Dermatophagoides pteronyssinus and bacteriolytic enzymes. Exp. Appl. Acarol. 61, 431–447. 10.1007/s10493-013-9712-8 PubMed DOI
Terra W. R. (1990). Evolution of digestive systems of insects. Annu. Rev. Entomol. 35, 181–200. 10.1146/annurev.en.35.010190.001145 DOI
Terra W. R. (2001). The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch. Insect Biochem. Physiol. 47, 47–61. 10.1002/arch.1036 PubMed DOI
Thomas W. R., Hales B. J., Smith W.-A. (2010). House dust mite allergens in asthma and allergy. Trends Mol. Med. 16, 321–328. 10.1016/j.molmed.2010.04.008 PubMed DOI
Thompson A. (2008). Ingredients: where pet food starts. Top. Companion Anim. Med. 23, 127–132. 10.1053/j.tcam.2008.04.004 PubMed DOI
Tovey E. R., Chapman M. D., Platts-Mills T. A. E. (1981). Mite faeces are a major source of house dust allergens. Nature 289, 592–593. 10.1038/289592a0 PubMed DOI
van Hage-Hamsten M., Johansson E. (1998). Clinical and immunologic aspects of storage mite allergy. Allergy 53(Suppl. 48), 49–53. 10.1111/j.1398-9995.1998.tb04997.x PubMed DOI
Vasantha N., Thompson L. D., Rhodes C., Banner C., Nagle J., Filpula D. (1984). Genes for alkaline protease and neutral protease from Bacillus amyloliquefaciens contain a large open reading frame between the regions coding for signal sequence and mature protein. J. Bacteriol. 159, 811–819. PubMed PMC
Vilain S., Luo Y., Hildreth M. B., Brozel V. S. (2006). Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Appl. Environ. Microbiol. 72, 4970–4977. 10.1128/AEM.03076-05 PubMed DOI PMC
Wang S.-Y., Moyne A.-L., Thottappilly G., Wu S.-J., Locy R. D., Singh N. K. (2001). Purification and characterization of a Bacillus cereus exochitinase. Enzyme Microb. Technol. 28, 492–498. 10.1016/S0141-0229(00)00362-8 PubMed DOI
Weber E., Hunter S., Stedman K., Dreitz S., Olivry T., Hillier A., et al. . (2003). Identification, characterization, and cloning of a complementary DNA encoding a 60-kd house dust mite allergen (Der f 18) for human beings and dogs. J. Allergy Clin. Immunol. 112, 79–86. 10.1067/mai.2003.1602 PubMed DOI
Zhan Z.-K., Ji K.-M., Liu X.-Y., Liu Z.-G., Li M., Chen J.-J, et al. . (2010). Monoclonal antibodies against recombinant Der f 3 reveal localization of Der f 3 in the gut and faecal pellets of Dermatophagoides farinae. Exp. Appl. Acarol. 52, 63–71. 10.1007/s10493-010-9349-9 PubMed DOI
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