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Bat guano-dwelling microbes and antimicrobial properties of the pygidial gland secretion of a troglophilic ground beetle against them

  • Applied microbial and cell physiology
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Abstract

Bat guano is an important source of microbial diversity in caves and can be a source of potential pathogens. Laemostenus (Pristonychus) punctatus is a guanophilic ground beetle species, which pygidial gland secretion exhibits action against pathogenic and other microbes. The distribution and diversity of microbes in bat guano from a karstic cave were determined in this study. Additionally, antimicrobial activity of the pygidial gland secretion of L. (P.) punctatus against guano-dwelling microbes was tested; minimal inhibitory concentration (MIC) and chemical composition of the secretion were analyzed. In total, 63 different bacterial species and 16 fungal morphotypes were isolated from guano samples by the cultivation method and confirmed using and phenotypic characterization and molecular identification. There was a difference in the composition of certain microorganisms between the sampling points (cave locations) and between the guano layers. The largest number of bacterial isolates belongs to the genera Lysinibacillus and Paenibacillus, while Pseudomonas species were highly abundant at the innermost sampling point. For the guanophilic fungi, the majority are ascomycetes, with Penicillium and Aspergillus as the most dominant genera. Meyerozyma guilliermondii was the only yeast species found in the guano samples. The most sensitive isolates were Enterococcus eurekensis (MIC 0.007 mg/mL) and Escherichia fergusonii (MIC 0.028 mg/mL). The most sensitive fungal isolates were M. guilliermondii, Penicillium expansum, and Trichoderma harzianum (MIC 0.15 mg/mL). This study opens a new possibility for better understanding of ecological relations between microorganisms and troglophilic ground beetles and for detailed investigations of morpho-anatomical aspects of pygidial glands.

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Acknowledgments

We are grateful to Dr. Saša Stanković (University of Niš - Faculty of Science and Mathematics, Niš, Serbia), who helped us in field research. The assistance of Marina Todosijević, B.Sc., in secretion measuring is acknowledged.

Funding

The work was financially supported by the Serbian Ministry of Education, Science and Technological Development (Grants Nos. ON173026, ON173032, ON173038, III43001, ON172053, III45016, and ON171038). This study was additionally funded jointly by the Serbian Ministry of Education, Science and Technological Development and the Ministry of Science and Technology of the People’s Republic of China (Grant “Mimetics of Insects for Sensing and Security,” I-2).

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Authors and Affiliations

  1. University of Belgrade - Faculty of Biology, Studentski Trg 16, Belgrade, 11000, Serbia

    Ivica Dimkić, Slaviša Stanković, Jovana Kabić, Miloš Stupar, Marija Nenadić, Milica Ljaljević-Grbić, Nikola Vesović, Jelena Vukojević & Srećko Ćurčić

  2. Department of Biology and Ecology, University of Niš - Faculty of Science and Mathematics, Višegradska 33, Niš, 18000, Serbia

    Vladimir Žikić

  3. University of Belgrade - Faculty of Chemistry, Studentski Trg 12-16, Belgrade, 11000, Serbia

    Ljubodrag Vujisić & Vele Tešević

  4. University of Belgrade - Institute of Physics, Pregrevica 118, Belgrade, 11080, Serbia

    Dejan Pantelić & Svetlana Savić-Šević

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  1. Ivica Dimkić
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Ivica Dimkić, Jovana Kabić, Marija Nenadić, Miloš Stupar, Ljubodrag Vujisić, Svetlana Savić-Šević, Vladimir Žikić, and Nikola Vesović. The first draft of the manuscript was written by Ivica Dimkić, Jovana Kabić, Miloš Stupar, Marija Nenadić, Milica Ljaljević Grbić, and Srećko Ćurčić, and all authors commented on previous versions of the manuscript. Funding acquisition: Slaviša Stanković, Jelena Vukojević, Dejan Pantelić, Vele Tešević, Srećko Ćurčić. Supervision: Ivica Dimkić, Slaviša Stanković, Milica Ljaljević Grbić, and Srećko Ćurčić. All authors read and approved the final manuscript.

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Dimkić, I., Stanković, S., Kabić, J. et al. Bat guano-dwelling microbes and antimicrobial properties of the pygidial gland secretion of a troglophilic ground beetle against them. Appl Microbiol Biotechnol 104, 4109–4126 (2020). https://doi.org/10.1007/s00253-020-10498-y

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