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First Reports on the Bacterial Community of the Digestive System of Endemic Baikal Gastropods Benedictia baicalensis

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Abstract—Diversity and comparative analysis of the microbiota composition of the digestive system of Lake Baikal endemic gastropods Benedictia baicalensis (Caenogastropoda) and of the bottom sediments from their habitat were studied. Strains belonging to 11 genera of heterotrophic bacteria (Pseudomonas, Acinetobacter, Alcaligenes, Flavobacterium, Enterobacter, Escherichia, Citrobacter, Klebsiella, Bacillus, Staphylococcus, Streptococcus, and Micrococcus) were isolated from the stomach and gut content. Molecular genetic analysis of total DNA from the digestive tract revealed the 16S rRNA gene sequences of the genera Pseudomonas, Flavobacterium, Mesorhizobium, Deefgea, and of the phylum Tenericutes. Most isolates were found to utilize various organic substances, including those of animal origin, which was probably due to the pantophagy of these mollusks. The cultured bacterial community of B.baicalensis digestive system was shown to be formed by gram-negative bacteria (95–97% strains), although in the bottom sediments 51% of the isolates were gram-positive coccoid and spore-forming rod-shaped bacteria. Low frequency of occurrence or complete absence of gram-positive bacteria in the mollusk intestine compared to the bottom sediments (fivefold or more) may indicate their use as a nutrient substrate.

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REFERENCES

  1. Belykh, M.P., Sukhanova, E.V., and Bel’kova, N.L., Properties of cultured heterotrophic microorganisms from the Lake Baikal rift Zone, Izv. Irkutsk. Gos. Univ., 2013, vol. 6, no. 3(1), pp. 20‒26.

  2. Bergey’s Manual of Systematic Bacteriology, 9th ed., vols. 1–2, Holt, J.G., Ed., Baltimore: Williams and Wilkins, 1994.

  3. Bergey’s Manual of Systematic Bacteriology, 2nd ed., The Firmicutes, De Vos, P., Garrity, G.M., Jones, D., Krieg, N.R, Ludwig, W., Rainey, F.A., Schleifer, K.-H., and Whitman, W.B., Eds., New York: Springer, 2009, vol. 3.

  4. Bergey’s Manual of Systematic Bacteriology, 2nd ed., The Gammaproteobacteria, Brenner, D.J., Krieg, N.R., Staley, J.T., and Garrity, G.M., Eds., New York: Springer, 2005, vol. 2, part B.

  5. Bergey’s Manual of Systematic Bacteriology, 2nd ed., vol. 2 (The Proteobacteria), part B (The Gammaproteobacteria), Brenner, D.J., Krieg, N.R., Staley, J.T., and Garrity, G.M., Eds., New York: Springer, 2005.

  6. Bogatyrenko, E.A. and Buzoleva, L.S., Characterization of the gut bacterial community of the Japanese sea cucumber Apostichopus japonicus, Microbiology (Moscow), 2016, vol. 85, pp. 116‒123.

    Article  CAS  Google Scholar 

  7. Brendelberger, H., Bacteria and digestive enzymes in the alimentary tract of Radix peregra (Gastropoda, Lymnaeidae), Limnol. Oceanogr., 1997, vol. 42, pp. 1635‒1638.

    Article  CAS  Google Scholar 

  8. Chaston, J. and Goodrich-Blair, H., Common trends in mutualism revealed by model associations between invertebrates and bacteria, FEMS Microbiol. Rev., 2010, vol. 34, pp. 41‒58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chechetkina, U.E., Evteeva, N.I., Rechkin, A.I., and Radaev, A.A., Enterobacteria in the microflora of honeybee digestive system in different seasons, Vestn. NNGU, 2011, no. 2 (2), pp. 149‒153.

  10. Dzyuba, E.V., Sukhanova, E.V., Denikina, N.N., and Bel’kova, N.L., Compaterive analysis of gut microbiocenoses of salmonid fishes with different feeding strategies, Fundament. Issled., 2014, no. 11, pp. 2429‒2433.

  11. Gayathri, V., Ganga Baheerathi, C., Revathi, K., and Sethi, S., Identification of gut microflora from green mussel (Perna viridis), Suppl. Adv. Biotech., 2011, vol. 10, no. 10, pp. 119‒122.

    Google Scholar 

  12. Harris, J.M., The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis, Microb. Ecol., 1993, vol. 25, pp. 195‒231.

    Article  CAS  PubMed  Google Scholar 

  13. King, G.M., Judd, G., Kuske, C.R., and Smith, C., Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA, PLoS One, 2012, vol. 7. E. 51475.

  14. Liesack, W., Weyland, H., and Stackebrandt, E., Potential risks of gene amplification by PCR as determined by 16S rDNA analysis of a mixed-culture of strict barophilic bacteria, Microb. Ecol., 1991, vol. 21, pp. 191‒198. doi 10.1007/BF02539153

    Article  CAS  PubMed  Google Scholar 

  15. Maksimiva, E.A. and Maksimov, V.N., Mikrobiologiya vod Baikala (Baikal Water Microbiology), Irkutsk: Irkutsk Gos. Univ., 1989.

    Google Scholar 

  16. Margulis, L. and Hinkle, G., Large symbiotic spirochetes: Clevelandina, Cristispira, Diplocalyx, Hollandina and Pillotina, Prokaryotes, 2006, vol. 7, pp. 971‒982.

    Article  Google Scholar 

  17. Marsollier, L., Severin, T., Aubry, J., and Merritt, R.W., Aquatic snails, passive hosts of Mycobacterium ulcerans, Appl. Environ. Microbiol., 2004, vol. 70, pp. 6296‒6298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. MR 3923-85, Metodicheskie rekomedatsii po identifikatsii gramotritsatel’nukh nefermentiruyushchikh mikroorganizmov (Methodical Recommendations for Identification of Gram-Negative Nonfermenting Microorganisms).

  19. MU 04-723/3, Metodicheskie ukazaniya po mikrobiologicheskoi diagnostike zabolevanii, vyzyvaemykh enterobakteriyami (Methodical Recommendations for Microbiological Diagnostics of Enterobacteria-Caused Diseases).

  20. Namsaraev, B.B. and Zemskaya, T.I., Mikrobiologicheskie protsessy krugovorota ugleroda v donnykh osadkakh ozera Baikal (Microbiological Processes of the Carbon Cycle in Lake Baikal Bottom Sediments), Novosibirsk: SO RAN, 2000.

    Google Scholar 

  21. Panasyuk, E.Yu., Dryukker, V.V., Parfenova, V.V., and Kostornova, T.Ya., Biodiversity and distribution of bacteria of the family Enterobacteriaceae and the nonfermenting group in Lake Baikal, Sib. Ekol. Zh., 2002, vol. 4, pp. 485‒490.

    Google Scholar 

  22. Parvathi, A., Kumar, H.S., Karunasagar, I., and Karunasagar, I., Detection and enumeration of Vibrio vulnificus in oysters from two estuaries along the southwest coast of India, using molecular methods, Appl. Environ. Microbiol., 2004, vol. 70, pp. 6909‒6913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Pavlova, O.N., Dryukker, V.V., Kostornova, T.Ya., and Nikulina, I.G., Patterns of Pseudomonas in Lake Baikal, Sib. Ekol. Zh., 2003, vol. 3, pp. 267‒272.

    Google Scholar 

  24. Praktikum po mikrobiologii (Practical Course in Microbiology), Netrusov, A.I., Ed., Moscow: Akademiya, 2005.

    Google Scholar 

  25. Pujalte, M.J., Ortigosa, M., Macian, M.C., and Garay, E., Aerobic and facultative anaerobic heterotrophic bacteria associated to Mediterranean oysters and seawater, Int. Microbiol., 1999, vol. 2, pp. 259‒266.

    CAS  PubMed  Google Scholar 

  26. Rodina, A.G., Bacteria in production of the Lake Baikal stony littoral, Proc. Conf. Zool. Inst. Akad. Nauk SSSU, 1954, no. 2, pp. 172‒201.

  27. Ropstorf, P., Sitnikova, T.Ya., Timoshkin, O.A., and Pomazkina, G.V., Observation on stomach contents, food uptake and feeding strategies of endemic baikalian gastropods, Berliner Palaobiologische Abhandlungen, 2003, vol. 4, pp. 151‒156.

    Google Scholar 

  28. Sayler, G.S., Nelson, J.D., Justice, A., and Colwell, R.R., Incidence of Salmonella spp., Clostridium botulinum, and Vibrio parahaemolyticus in an estuary, Appl. Environ. Microbiol., 1976, vol. 31, pp. 723‒730.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Simon, C.A. and McQuaid, C., Extracellular digestion in two co-occurring intertidal mussels (Perna perna (L.) and Choromytilus meridionalis (Kr)) and the role of enteric bacteria in their digestive ecology, J. Exp. Marine. Biol. Ecol., 1999, vol. 234, pp. 59‒81.

    Article  Google Scholar 

  30. Sitnikova, T., Michel, E., Tulupova, Yu., Khanaev, I., Parfenova, V., and Prozorova, L., Spirochetes in gastropods from Lake Baikal and North American freshwaters: new multi-family, multi-habitat host records, Symbiosis, 2012, vol. 56, pp. 103‒110.

    Article  Google Scholar 

  31. Sitnikova, T.Ya., Lake Baikal Prosobranchia (Gastropoda: Prosobranchia): morphology, taxonomy, biology, and fauna formation, Doctoral (Biol.) Dissertation, 03.00.08, Irkutsk, 2004.

  32. Stackebrandt, E., Lang, E., Cousin, S., Pauker, O., Brambilla, E., Kroppenstedt, R., and Lunsdorf, H., Deefgea rivuli gen. nov., sp. nov., a member of the class Betaproteobacteria, Int. J. Syst. Evol. Microbiol., 2007, vol. 57, pp. 639‒645.

    Article  CAS  PubMed  Google Scholar 

  33. Syvokiene, J. and Mickeniene, L., Change in the intestinal microflora of molluscs from the Neris river depending on pollution, Acta. Zool. Lituanica, 2002, vol. 12, pp. 76‒81.

    Article  Google Scholar 

  34. Syvokiene, J., Mickeniene, L., and Barsiene, J., Bacteria in the digestive system of molluscs from Lithuanian lakes, Ecologija, 2008, vol. 54, pp. 271‒277.

    CAS  Google Scholar 

  35. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S., MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725‒2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tatsukami, Y., Nambu, M., Morisaka, H., Kuroda, K., and Ueda, M., Disclosure of the differences of Mesorhizobium loti under the free-living and symbiotic conditions by comparative proteome analysis without bacteroid isolation, BMC Microbiol., 2013, vol. 13, p. 180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Timoshkin, O.A., Ivanov, V.G., Obolkin, V.A., and Sherstyankin, P.P., Water temperature dynamics in the shallow zone of the Southern Baikal western side at the area of a Cape Berezovyi interdisciplinary polygon according to the data of continuous measurement using ONSET StowAway Tid Bit Loggers, in Annotirovannyi spisok fauny ozera Baikia i ego vodosbornogo basseina (Annotated List of the Fauna of Lake Baikal and Its Catchment Basin), vol. 2, Water Bodies and Water Courses of Southern Eastern Siberia and Northern Mongolia, book 1, Timoshkin, O.A., Ed., Novosibirsk: Nauka, 2009, pp. 727‒731.

  38. Timoshkin, O.A., Samsonov, D.P., Yamamuro, M., Moore, M.V., Belykh, O.I., Malnik, V.V., Sakirko, M.V., Shirokaya, A.A., Bondarenko, N.A., Domysheva, V.M., Fedorova, G.A., Kochetkov, A.I., Kuzmin, A.V., Lukhnev, A.G., Medvezhonkova, O.V., et al., Rapid ecological change in the coastal zone of Lake Baikal (East Siberia): is the site of the world’s greatest freshwater biodiversity in danger?, J. Great Lakes Res., 2016, vol. 42, pp. 487‒497.

    Article  CAS  Google Scholar 

  39. Tulupova, Y.R., Parfenova, V.V., Sitnikova, T.Y., Sorokovnikova, E.G., and Khanaev, I.B., First report on bacteria of the family Spirochaetaceae from digestive tract of endemic gastropods from Lake Baikal, Microbiology (Moscow), 2012, vol. 81, pp. 460‒467.

    Article  CAS  Google Scholar 

  40. Van Horn, D.J., Garcia, J.R, Loker, E.S., Mitchell, K.R., Mkoji, G.M., Adema, C.M., and Takacs-Vesbach, C.D., Complex intestinal bacterial communities in three species of planorbid snails, J. Mollus. Stud., 2012, vol. 78, pp. 74‒80.

    Article  Google Scholar 

  41. Watkinson, A.J., Micalizzi, G.B., Graham, G.M., Bates, J.B., and Costanzo, S.D., Antibiotic-resistant Escherichia coli in wastewaters, surface waters, and oysters from an urban riverine system, Appl. Environ. Microbiol., 2007b, vol. 73, pp. 5667‒5670.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Young, C.M., Feeding and digestion in Pterocera and Vermetus, with a discussion of the occurrence of the crystalline style in the Gastropoda, Science Reprints Great Barrier Reef Expedition, British Museum (Natural History), 1932, no. 1, pp. 259–281.

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ACKNOWLEDGMENTS

The authors are grateful to A.B. Kupchinskii for his help in collection of the mollusks and to O.I. Belykh and M.Yu. Suslova for their help in interpretation and presentation of experimental results. The work was carried out within the framework of the State Assignment for the Limnological Institute, Siberian Branch, Russian Academy of Sciences no. 0345-2016-0003 (AAAA-A16-116122110061-6) and was supported by the Russian Foundation for Basic Research, project no. 15-29-02515-ofi_m.

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  1. Limnological Institute, Siberian Branch, Russian Academy of Sciences, Irkutsk, Russia

    Yu. R. Shtykova, T. Ya. Sitnikova, N. V. Kulakova, E. V. Sukhanova, I. V. Khanayev & V. V. Parfenova

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  1. Yu. R. Shtykova
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  2. T. Ya. Sitnikova
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Correspondence to Yu. R. Shtykova.

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Shtykova, Y.R., Sitnikova, T.Y., Kulakova, N.V. et al. First Reports on the Bacterial Community of the Digestive System of Endemic Baikal Gastropods Benedictia baicalensis. Microbiology 87, 825–832 (2018). https://doi.org/10.1134/S0026261718060140

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