Mycophagy should not be considered as a single and homogeneous category of nutritional biology due to the specific symbiotic chitinolytic bacteria associated with mites and fungi. To test interaction among mites, fungi, and chitinolytic bacteria, experiments were conducted on the model species Tyrophagus putrescentiae (Schrank). Mucor sp, Alternaria alternata, Penicillium claviforme, P. griseofulvum, and Verticillium sp. were plated onto malt agar and offered to T. putrescentiae in the laboratory. Mites were evaluated utilizing microanatomical examination based on histology, excrement analysis using fluorescence microscopy, bacterial plating, impact of mite homogenate on fungi in Petri dishes, reproduction of mites feeding upon each fungus, and isolation of associated bacteria inside mites. There were clear differences regarding the digested spores of different fungi passing through the gut and subsequently in the feces. Abundances of bacterial cells in excrement also corresponded to the fungi offered. The extracts from mites had chitinolytic activity, and the plated bacteria are known to produce exochitinases. The various feeding patterns observed were caused by differences in the cell wall structures of the tested fungi. The study illustrates that mycophagy in saprophagous mites does not consist of a single pattern, but rather that it can be classified into several sub-patterns depending upon the digested fungal species and its parts. The results point to a nearly symbiotic relationship between chitinolytic bacteria and digested fungi in mycophagous microarthropods.

Crop Research Institute Drnovská 507 73 Prague 6 Ruzyně 161 06 Czech Republic

Department of Zoology Faculty of Science Charles University Viničná 7 Prague 2 CZ 128 44 Czech Republic

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Aktuganov G. E., Melent'ev A. I., Kuz'mina L. Y., Galimzyanova N. F., Shirokov A. V. 2004. The chitinolytic activity of Bacillus Cohn bacteria antagonistic to phytopathogenic fungi. Microbiology. 72: 313–317. PubMed

Anderson J. M. 1975. The enigma of soil animal species diversity, pp. 517 In Vaněk J. (ed.), Progress in soil zoology. Academia, Prague, Czech Republic.

Brurberg M. B., Synstad B., Klemsdal S. S., van Aalten D. M. F., Sundheim L., Eijsink G. H. 2001. Chitinases from Serratia marcescens. Recent Res. Dev. Microbiol. 5: 187–204.

Chang W. T., Chen C. S., Wang S. L. 2003. An antifungal chitinase produced by Bacillus cereus with shrimp and crab shell powder as a carbon source. Curr. Microbiol. 47: 102–108. PubMed

Citterio B., Malatesta M., Battistelli S., Marcheggiani F., Baffone W., Saltarelli R., Stocchi V., Gazzanelli G. 2001. Possible involvement of Pseudomonas fluorescens and Bacillaceae in structural modifications of Tuber borchii fruit bodies. Can. J. Microbiol. 47: 264–268. PubMed

Czajkowska B. 1970. Rozwój rozkruszków na niektórych gatunkach grzybów. Zesz. Problem. Postep.Nauk Roln. 109: 219–227.

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. PubMed

Haq M. A. 1981. Feeding habits of ten species of Oribatid mites (Acari: Oribatei) from Malabar, South India. Indian J. Acarol. 6: 39–50.

Hubert J., Nesvorná M., Ságová-Marečková M., Kopecký J. 2012. Shift of bacterial community in synanthropic mite Tyrophagus putrescentiae induced by Fusarium fungal diet. PLoS One. 7: e48429.. PubMed PMC

Hudson H. J. 1986. Fungal biology. Edward Arnold, London.

Jaspers E., Overmann J. 2004. Ecological significance of microdiversity: identical 16S rRNA gene sequence can be found in bacteria with highly divergent genomes and ecophysiologies. Appl. Environ. Microbiol. 70: 4831–4839. PubMed PMC

Jollès P., Muzzarelli R.A.A. (eds.). 1999. Chitin and chitinases. Birkhäuser, Basel.

Kaneko N. 1988. Feeding habits and cheliceral size of Oribatid mites in cool temperate forest soils in Japan. Rev.Écol.Biol.Sol. 25: 353–363.

Kishore G. K., Pande S., Podile A. R. 2005. Chitin-supplemented foliar application of Serratia marcescens GPS 5 improves control of late leaf spot disease of groundnut by activating defence-related enzymes. J. Phytopathol. 153: 169–173.

Kobayashi D. Y., Reedy R. M., Bick J. A., Oudemans P. V. 2002. Characterization of chitinase gene from Stenotrophomonas maltophilia Strain 34S1 and its involvement in biological control. Appl. Environ. Microbiol. 68: 1047–1054. PubMed PMC

Koukol O., Mourek J., Janovský Z., Černá K. 2009. Do Oribatid mites (Acari: Oribatida) show a higher preference for ubiquitous vs. specialized saprotrophic fungi from pine litter? Soil Biol. Biochem. 41: 1124–1131.

Luxton M. 1972. Studies on the Oribatid mites of a Danish beech wood soil. I. Nutr. Biol. Pedobiologia. 12: 434–463.

Maraun M., Erdmann G., Fischer B. M., Pollierer M. M., Norton R. A., Schneider K., Scheu S. 2011. Stable isotopes revisited: their use and limits for Oribatid mite trophic ecology. Soil Biol. Biochem. 43: 877–882.

Maraun M., Martens H., Migge M., Theenhaus A., Scheu S. 2003. Adding to the ‘enigma of soil animal diversity’: fungal feeders and saprophagous soil invertebrates prefer similar food substrates. Eur. J. Soil Biol. 39: 85–95.

Merzendorfer H., Zimoch L. 2003. Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J. Exp. Biol. 206: 4393–4412. PubMed

Pankiewicz-Nowicka D., Boczek J., Davis R. 1984. Food selection in Tyrophagus putrescentiae (Schrank) (Acarina, Acaridae). J. Georgia Entomol. Soc. 19: 317–321.

Ruess L., Häggblomd M. M., Zapata E. J. G., Dighton J. 2002. Fatty acids of fungi and nematodes—possible biomarkers in the soil food chain? Soil Biol. Biochem. 34: 745–756.

Schneider K., Maraun M. 2005. Feeding preferences among dark pigmented fungi (“Dematiacea”) indicate trophic niche differentiation of Oribatid mites. Pedobiologia. 49: 61–67.

Schneider K., Migge S., Norton R. A., Scheu S., Langel R., Reineking A., Maraun M. 2004a. Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N). Soil Biol. Biochem. 36: 1769–1774.

Schneider K., Renker C., Maraun M. 2005. Oribatid mite (Acari, Oribatida) feeding on ectomycorrhizal fungi. Mycorrhiza. 16: 67–72. PubMed

Schneider K., Renker C., Scheu S., Maraun M. 2004b. Feeding biology of Oribatid mites: a minireview. Phytophaga. 14: 247–256.

Schuster R. 1956. Der Anteil der Oribatiden an den Zersetzungsvorgängen im Boden. Z. Morphol. Ökol. Tiere. 45: 1–33.

Siepel H., de Ruiter-Dijkman E. M. 1993. Feeding guilds of Oribatid mites based on their carbohydrase activities. Soil Biol. Biochem. 25: 1491–1497.

Smrž J. 1989. Internal anatomy of Hypochthonius rufulus (Acari: Oribatida). J. Morphol. 200: 215–230. PubMed

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

Smrž J. 2000. A modified test for chitinase and cellulase activity in soil mites. Pedobiologia. 44: 186–189.

Smrž J. 2002a. Nutritional biology: the basic step in the autecological studies (multi-methodical approach). Eur. J. Soil Biol. 38: 35–38.

Smrž J. 2002b. The excrement analysis—the useful tool for the biological and autecological studies in soil zoology, pp. 185–189. In Tajovský K., Balík V., Pižl V. (eds.), Studies on Soil Fauna in Central Europe. Proceedings of the 6th Central European Workshop on Soil Zoology Studies on Soil Fauna in Central Europe. 23–25 April 2001, České Budějovice, Czech Republic: Institute of Soil Biology, Czech Academy of Sciences, České Budějovice, Czech Republic.

Smrž J. 2003. Microanatomical and biological aspects of bacterial associations in Tyrophagus putrescentiae (Acari: Acaridida). Exp. Appl. Acarol. 31: 105–113. PubMed

Smrž J. 2009. Mycophagy—dream and reality in soil saprophagous mites (Acari: Oribatida and Acaridida), pp 147–150. In Tajovský K., Schlaghamerský J., Pižl V. (eds.), Contributions to Soil Zoology in Central Europe III, Proceedings of the 9th Central European Workshop on Soil Zoology, 17–20 April 2007, České Budějovice, Czech Republic: Institute of Soil Biology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.

Smrž J., Čatská V. 1987. Food selection of the field population of Tyrophagus putrescentiae (Schrank) (Acari, Acaridida). J. Appl. Entomol. 104: 329–335.

Smrž J., Čatská 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. Carolinae-Biol. 33: 81–93.

Smrž J., Čatská V. 2010. Mycophagous mites and their internal associated bacteria cooperate to digest chitin in soil. Symbiosis. 52: 33–40.

Smrž J., Jungová E. 1989. The ecology of a field population of Tyrophagus putrescentiae (Acari, Acaridida). Pedobiologia. 33: 183–192.

Smrž J., Norton R. A. 2004. Food selection and internal processing in Archegozetes longisetosus (Acari: Oribatida). Pedobiologia. 48: 111–120.

Smrž J., Soukalová H. 2008. Mycophagous mites (Acari: Oribatida and Acaridida) and their cooperation with chitinolytic bacteria, pp. 374–377. In Bertrand M., Kreiter S., McCoy K. D., Migeon A., Navajas M., Tixier M.-S., Vial L. (eds.), Integrative acarology, Proceedings of the Sixth Congress of the European Association of Acarologists, 21–25 July 2008, Montpellier, France: European Association of Acarologists, Montpellier, France.

Smrž J., Svobodová J., Čatská V. 1991. Synergetic participation Tyrophagus putrescentiae (Schrank) (Acari, Acaridida) and its associated bacteria on the destruction of some soil micromycetes. J. Appl. Entomol. 111: 206–210.

Wallwork J. A. 1976. The distribution and diversity of soil fauna. Academic Press, London.

Zhang Z., Yuen G., Sarath Y. G., Penheiter A. R. 2001. Chitinases from the plant disease biocontrol agent. Stenotrophomonas Maltophilia C3. Phytopathol. 91: 204–211. PubMed

Zinkler D. 1972. Vergleichende Untersuchungen zum Wirkungsspektrum der Carbohydrases laubstreubewohnender Oribatiden. Verh. Deutsch. Zool. Gesell. 65: 149–153.

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