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Reaction of microorganisms to the digestive fluid of earthworms

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Abstract

The reaction of soil bacteria and fungi to the digestive fluid of the earthworm Aporrectodea caliginosa was studied. The fluid was obtained by centrifugation of the native enzymes of the digestive tract. The inhibition of growth of certain bacteria, spores, and fungal hyphae under the effect of extracts from the anterior and middle sections of the digestive tract of A. caliginosa was discovered for the first time. In bacteria, microcolony formation was inhibited as early as 20–30 s after the application of the gut extracts, which may indicate the nonenzymatic nature of the effect. The digestive fluid exhibited the same microbicidal activity whether the earthworms were feeding on soil or sterile sand. This indicates that the microbicidal agents are formed within the earthworm’s body, rather than by soil microorganisms. The effect of the digestive fluid from the anterior and middle divisions is selective in relation to different microorganisms. Of 42 strains of soil bacteria, seven were susceptible to the microbicidal action of the fluid (Alcaligenes faecalis 345-1, Microbacterium sp. 423-1, Arthrobacter sp. 430-1, Bacillus megaterium 401-1, B. megaterium 413-1, Kluyvera ascorbata 301-1, Pseudomonas reactans 387-2). The remaining bacteria did not die in the digestive fluid. Of 13 micromycetes, the digestive fluid inhibited spore germination in Aspergillus terreus and Paecilomyces lilacinus and the growth of hyphae in Trichoderma harzianum and Penicillium decumbens. The digestive fluid stimulated spore germination in Alternaria alternata and the growth of hyphae in Penicillium chrysogenum. The reaction of the remaining micromycetes was neutral. The gut fluid from the posterior division of the abdominal tract did not possess microbicidal activity. No relation was found between the reaction of microorganisms to the effects of the digestive fluid and the taxonomic position of the microorganisms. The effects revealed are similar to those shown earlier for millipedes and wood lice in the following parameters: quick action of the digestive fluid on microorganisms, and the selectivity of the action on microorganisms revealed at the strain level. The selective effect of the digestive gut fluid of the earthworms on soil microorganisms is important for animal feeding, maintaining the homeostasis of the gut microbial community, and the formation of microbial communities in soils.

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References

  1. Pokarzhevskii, A.D., Sikora, I., and Gordienko, S.A., Amino Acid Resources in Nutrition of Saprophages, Dokl. Akad. Nauk SSSR, 1984, vol. 277, no. 1, pp. 253–256.

    CAS  Google Scholar 

  2. Byzov, B.A., Zoomicrobial Interactions in Soil, Extended Abstract of Doctoral (Biol.) Dissertation, Moscow: Izd-vo “Maks Press”, 2003.

    Google Scholar 

  3. Kozlovskaya, L.S., Methods of Studying Microorganism-Invertebrate Relations, Razlozhenie rastitel’nykh ostatkov v pochve (Decomposition of Plant Residues in Soil), Moscow: Nauka, 1985.

    Google Scholar 

  4. Zvyagintsev, D.G., Panikov, N.S., and Gorbenko, A.Yu., Quantitative Estimation of the Effect of Invertebrates on Microbial Growth in Soil, Pochvennaya fauna i pochvennoe plodorodie. Trudy 9 Mezhdunarodnogo kollokviuma po pochvennoi zoologii (Soil Fauna and Soil Fertility. Proc. 9th Int. Colloquium), B.R. Striganova, Ed., Moscow: Nauka, 1987.

    Google Scholar 

  5. Marfenina, O.E., Effect of Earthworms on the Microscopic Fungi as Soil Destructors of Organic Matter, Destruktsiya organicheskikh veshchestv v pochve (Destruction of Organic Matter in Soil), Vilnus, 1989, pp. 104–108.

  6. Tret’yakova, E.B., Dobrovol’skaya, T.G., Byzov, B.A., and Zvyagintsev, D.G., Bacterial Communities Associated with Soil Invertebrates, Mikrobiologiya, 1996, vol. 65, no. 1, pp. 102–110 [Microbiology (Engl. Transl.), vol. 65, no. 1, pp. 91–97].

    CAS  Google Scholar 

  7. Dash, N.K., Behera, N., and Dash, M.C., Gut Load, Transit Time, Gut Microflora and Turnover of Soil, Plant and Fungal Material by Some Tropical Earthworms, Pedobiologia, 1986, vol. 29, pp. 13–20.

    Google Scholar 

  8. Daniel, O. and Anderson, J.M., Microbial Biomass and Activity in Contrasting Soil Materials After Passage Through the Gut of the Earthworms Lumbricus rubellus Hoffmeister, Soil Biol. Biochem., 1992, vol. 24, pp. 465–470.

    Article  Google Scholar 

  9. Kristufek, V., Ravasz, K., and Pizl, V., Changes in Densities of Bacteria and Microfungi During Gut Transit in Lumbricus rubellus and Aporrectodea caliginosa (Oligochaeta: Lumbricidae), Soil Biol. Biochem., 1992, vol. 24, no. 12, pp. 1499–1500.

    Article  Google Scholar 

  10. Doube, B.M., Ryder, M.H., Davoren, C.W., and Meyer, T., Earthworms: a Down-Under Delivery Service for Biocontrol Agents of Root Disease, Acta Zoologica Fennica, 1995, vol. 196, pp. 219–223.

    Google Scholar 

  11. Moody, S.A., Piearce, T.G., and Dighton, J., Fate of Some Fungal Spores Associated with Wheat Straw Decomposition on Passage Through the Guts of Lumbricus terrestris and Aporrectodea longa, Soil Biol. Biochem., 1996, vol. 28, pp. 533–537.

    Article  CAS  Google Scholar 

  12. Bonkowski, M., Griffiths, B.S., and Ritz, K., Food Preference of Earthworms for Soil Fungi, Pedobiologia, 2000, vol. 44, pp. 666–676.

    Article  Google Scholar 

  13. Tiunov, A.V. and Scheu, S., Microfungal Communities in Soil, Litter and Casts of Lumbricus terrestris L. (Lumbricidae): a Laboratory Experiment, Appl. Soil Ecol, 2000, vol. 14, pp. 17–26.

    Article  Google Scholar 

  14. Vu Nguen Thanh, Byzov B.A., Bab’eva I.P., Sensitivity of Yeast to the Digestive Fluid of Pachyiulus flavipes C.L. Koch, Mikrobiologiya, 1994, vol. 63, no. 4, pp. 715–720.

    Google Scholar 

  15. Byzov, B.A., Vu Nguyen Thanh, Bab’Eva, I.P., Tretyakova, E.B., Dyvak, I.A., and Rabinovich, Ya.M., Killing and Hydrolytic Activities of the Gut Fluid of the Millipede Pachyiulus flavipes C.L. Koch on yeast cells, Soil Biol. Biochem, 1998, vol. 30, no. 8/9, pp. 1137–1145.

    Article  CAS  Google Scholar 

  16. Byzov, B.A., Kurakov, A.V., Tretyakova, E.B., Vu Nguyen Thanh, Nguyen Duc To Luu, and Rabinovich, Ya.M., Principles of the Digestion of Microorganisms in the Gut of Soil Millipedes: Specificity and Possible Mechanisms, Appl. Soil. Ecol., 1998, vol. 9, pp. 145–151.

    Article  Google Scholar 

  17. Sambrook, J. and Russel, D.W., Molecular Cloning: a Laboratory Manual, 3rd ed., New York: Cold Spring Harbor Laboratory Press, 2001, pp. 6–22.

    Google Scholar 

  18. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Mille, W., and Lipman, D.J., Gapped BLAST and PSI-BLAST: a New Generation of Protein Database Search Programs, Nucleic Acids Res., 1997, vol. 25, pp. 3389–3402.

    Article  PubMed  CAS  Google Scholar 

  19. Kurakov, A.V., Kharin, S.A., Nechitailo, T.Yu., Golyshin, P.N., and Zvyagintsev, D.G., Modification of Fungal Numbers, Biomass, and Composition in the Digestive Tract of Aporrectodea caliginosa Earthworm, Ekologiya i biologiya pochv. Materialy Mezhdunarodnoi nauchnoi konferentsii (Soil Ecology and Biology. Proc. Int. Sci. Conf.), Rostov-on-Don, 2005, pp. 255–259.

  20. Makeschin, F., Earthworms (Lumbricidae: Oligochaeta): Important Promoters of Soil Development and Soil Fertility, Fauna in soil ecosystems. Recycling processes, nutrient fluxes and agricultural production, Benckiser, G., Ed. 1997, pp. 173–223.

  21. Parle, J.N., A Microbial Study of Earthworms Casts, J. Gen. Microbiol., 1963, vol. 31, pp. 13–22.

    CAS  Google Scholar 

  22. Dkhar, M.S. and Mishra, R.R., Microflora in the Gut Contents of the Earthworm (Amynthas diffringens Baird.), J. Phytol. Res., 1991, vol. 4, pp. 155–159.

    Google Scholar 

  23. Schönholzer, F., Hanh, D., and Zeyer, J., Origins and Fate of Fungi and Bacteria in the Gut of Lumbricus terrestris L. Studied by Image Analysis, FEMS Microbiol. Ecol, 1999, vol. 28, pp. 235–248.

    Google Scholar 

  24. Anderson, J.M. and Bignell, D.E., Bacteria in the Food, Gut Contents and Faeces of the Litter Feeding Millipede Glomeris marginata, Soil Biol. Biochem., 1980, vol. 12, pp. 251–254.

    Article  Google Scholar 

  25. Bignell, D.E., Relative Assimilation of 14C-Labeled Microbial Tissue and 14C-Plant Fibers Ingested with Leaf Litter by the Millipede Glomeris marginata Under Experimental Conditions, Soil Biol. Biochem., 1989, vol. 21, pp. 819–827.

    Article  Google Scholar 

  26. Piearce, T.G. and Phillips, M.J., The Fate of Ciliates in the Earthworm Gut: An in Vitro Studies, Microbial Ecol., 1980, no. 5, pp. 313–320.

  27. Khomyakov, N.V., Dobrovol’skaya, T.S., Nechitailo, T.Yu., Golyshin, P.N., and Byzov, B.A., Fate of Bacteria in Earthworm Gut Ekologiya i biologiya pochv. Materialy Mezhdunarodnoi nauchnoi konferentsii (Soil Ecology and Biology. Proc. Int. Sci. Conf.), Rostov-on-Don, 2005, pp. 523–528.

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Authors and Affiliations

  1. Department of Soil Biology, Moscow State University, Moscow, Russia

    N. V. Khomyakov, S. A. Kharin, B. A. Byzov & D. G. Zvyagintsev

  2. National Biotechnology Center, Braunschweig, Germany

    T. Yu. Nechitailo & P. N. Golyshin

  3. International Biotechnology Center, Moscow State University, Moscow, Russia

    A. V. Kurakov

Authors
  1. N. V. Khomyakov
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  2. S. A. Kharin
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  3. T. Yu. Nechitailo
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  4. P. N. Golyshin
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  5. A. V. Kurakov
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  6. B. A. Byzov
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  7. D. G. Zvyagintsev
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Correspondence to B. A. Byzov.

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Original Russian Text © N.V. Khomyakov, S.A. Kharin, T.Yu. Nechitailo, P.N. Golyshin, A.V. Kurakov, B.A. Byzov, D.G. Zvyagintsev, 2007, published in Mikrobiologiya, 2007, Vol. 76, No. 1, pp. 55–65.

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Khomyakov, N.V., Kharin, S.A., Nechitailo, T.Y. et al. Reaction of microorganisms to the digestive fluid of earthworms. Microbiology 76, 45–54 (2007). https://doi.org/10.1134/S0026261707010079

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