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


Journal

Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612

Informations de publication

Date de publication:
May 2020
Historique:
received: 07 11 2019
accepted: 23 02 2020
revised: 26 01 2020
pubmed: 7 3 2020
medline: 9 1 2021
entrez: 7 3 2020
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 32140841
doi: 10.1007/s00253-020-10498-y
pii: 10.1007/s00253-020-10498-y
doi:

Substances chimiques

Anti-Bacterial Agents 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4109-4126

Subventions

Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : ON173026
Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : ON173032
Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : ON173038
Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : III43001
Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : ON172053
Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : III45016
Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : ON171038
Organisme : Serbian Ministry of Education, Science and Technological Development and the Ministry of Science and Technology of the People's Republic of China
ID : ''Mimetics of Insects for Sensing and Security'', I-2

Références

Barton HA (2006) Introduction to cave microbiology: a review for the non-specialists. J Cave Karst Stud 68(2):43–54
Blum MS (1981) Chemical defenses of arthropods. Academic Press, New York
Borda DR, Năstase-Bucur RM, Spînu M, Uricariu R, Mulec J (2014) Aerosolized microbes from organic rich materials: case study of bat guano from caves in Romania. J Cave Karst Stud 76(2):114–126
Casale A (1988) Revisione degli Sphodrina (Coleoptera, Carabidae, Sphodrini). Monografie V. Regional Museum of Natural Science, Turin
Clark VC (2009) Collecting arthropod and amphibian secretions for chemical analyses. In: Zhang W, Liu H (eds) Behavioral and chemical ecology. Nova Science Publishers, Hauppauge, pp 1–46
Ćurčić SB, Brajković MM, Ćurčić BPM (2007) The carabids of Serbia. Monographs, volume 11. Institute of Zoology, Faculty of Biology, University of Belgrade, Committee for Karst and Speleology, Serbian Academy of Sciences and Arts, Department of Conservation Biology, Vegetation- and Landscape Ecology, Faculty of Life Sciences, University of Vienna & UNESCO MAB Committee of Serbia, Belgrade-Vienna, Serbia-Austria
Daouk KD, Dagher MS, Sattout JE (1995) Antifungal activity of the essential oil of Origanum syriacum L. J Food Prot 58:1147–1149
pubmed: 31137364
De Mandal S, Zothansanga AKP, Bisht SS, Senthil KN (2015) First report of bacterial community from a bat guano using Illumina next-generation sequencing. Genom Data 4:99–101
pubmed: 26484190 pmcid: 4535889
Di Bella C, Piraino C, Caracappa S, Fornasari L, Violani C, Zava B (2003) Enteric microflora in Italian Chiroptera. J Mt Ecol 7:221–224
Di Giulio A, Muzzi M, Romani R (2015) Functional anatomy of the explosive defensive system of bombardier beetles (Coleoptera, Carabidae, Brachininae). Arthropod Struct Dev 44:468–490
pubmed: 26362009
Dimkić I, Živković S, Berić T, Ivanović Ž, Gavrilović V, Stanković S, Fira Đ (2013) Characterization and evaluation of two Bacillus strains, SS-12.6 and SS-13.1, as potential agents for the control of phytopathogenic bacteria and fungi. Biol Control 65(3):312–321
Forsyth DJ (1972) The structure of the pygidial defence glands of Carabidae (Coleoptera). Trans Zool Soc Lond 32:249–309
Giglio A, Brandmayr P, Dalpozzo R, Sindona G, Tagarelli A, Talarico F, Brandmayr TZ, Ferrero EA (2009) The defensive secretion of Carabus lefebvrei Dejean 1826 pupa (Coleoptera, Carabidae): gland ultrastructure and chemical identification. Microsc Res Tech 72(5):351–361
pubmed: 19067359
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hänel H, Raether W (1988) A more sophisticated method of determining the fungicidal effect of water-insoluble preparations with a cell harvester, using miconazole as an example. Mycoses 31(3):148–154
pubmed: 3292912
Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180(18):4765–4774
pubmed: 9733676 pmcid: 107498
Ibrahim A, Hage CH, Souissi A, Leray A, Héliot L, Souissi S, Vandenbunder B (2015) Label-free microscopy and stress responses reveal the functional organization of Pseudodiaptomus marinus copepod myofibrils. J Struct Biol 191:224–235
pubmed: 26057347
Ilić B, Dimkić I, Unković N, Ljaljević-Grbić M, Vukojević J, Vujisić L, Tešević V, Stanković S, Makarov S, Lučić L (2018) Millipedes vs. pathogens: defensive secretions of some julids (Diplopoda: Julida) as potential antimicrobial agents. J Appl Entomol 142:775–791
Jiang X, Zhong J, Liu Y, Yu H, Zhuo S, Chen J (2011) Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy. Scanning 33:53–56
pubmed: 21328394
Jovčić B, Begović J, Lozo J, Topisirović L, Kojić M (2009) Dynamics of sodium dodecyl sulfate utilization and antibiotic susceptibility of strain Pseudomonas sp. ATCC19151. Arch Biol Sci 61:159–165
Julg B, Elias J, Zahn A, Koppen S, Becker-Gaab C, Bogner J (2008) Bat-associated histoplasmosis can be transmitted at entrances of bat caves and not only inside the caves. J Travel Med 15:133–136
pubmed: 18346250
Jurado V, Laiz L, Rodriguez-Nava V, Boiron P, Hermosin B, Sanchez-Moral S, Saiz-Jimenez C (2010) Pathogenic and opportunistic microorganisms in caves. Int J Speleol 39:15–24
Kim JJ, Kim SH, Lee S, Breuil C (2003) Distinguishing Ophiostoma ips and Ophiostoma montium, two bark beetle-associated sapstain fungi. FEMS Microbiol Lett 222:187–192
pubmed: 12770706
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
pubmed: 7463489
Kind T (2003) Automated mass spectral deconvolution and identification system (AMDIS). www.amdis.net . Accessed 27 December 2019
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874
pubmed: 27004904 pmcid: 27004904
Lečić S, Ćurčić S, Vujisić L, Ćurčić B, Ćurčić N, Nikolić Z, Anđelković B, Milosavljević S, Tešević V, Makarov S (2014) Defensive secretions in three ground-beetle species (Insecta: Coleoptera: Carabidae). Ann Zool Fenn 51:285–300
Ma Y, Zhang H, Du Y, Tian T, Xiang T, Liu X, Feng H (2015) The community distribution of bacteria and fungi on ancient wall paintings of the Mogao Grottoes. Sci Rep 5:7752
pubmed: 25583346 pmcid: 4291566
Medellin RA, Wiederholt R, Lopez-Hoffman L (2017) Conservation relevance of bat caves for biodiversity and ecosystem services. Biol Conserv 211:45–50
Mulec J (2008) Microorganisms in hypogeon: examples from Slovenian karst caves. Acta Carsol 7(1):153–160
Mulec J, Zalar P, Hajna NZ, Rupnik M (2002) Screening for culturable microorganisms from cave environments (Slovenia). Acta Carsol 31(2):177–187
Nenadić M, Soković M, Glamočlija J, Ćirić A, Perić-Mataruga V, Tešević V, Vujisić L, Todosijević M, Vesović N, Ćurčić S (2016) Antimicrobial activity of the pygidial gland secretion of the troglophilic ground beetle Laemostenus (Pristonychus) punctatus (Dejean, 1828) (Insecta: Coleoptera: Carabidae). Bull Entomol Res 106:474–480
pubmed: 27018928
Nenadić M, Ljaljević-Grbić M, Stupar M, Vukojević J, Ćirić A, Tešević V, Vujisić L, Todosijević M, Vesović N, Živković N, Ćurčić S (2017) Antifungal activity of the pygidial gland secretion of Laemostenus punctatus (Coleoptera: Carabidae) against cave-dwelling micromycetes. Sci Nat 104:52
Nenadić M, Soković M, Calhelha RC, Ferreira ICFR, Ćirić A, Vesović N, Ćurčić S (2018) Inhibition of tumour and non-tumour cell proliferation by pygidial gland secretions of four ground beetle species (Coleoptera: Carabidae). Biologia 73(8):787–792
Nešić D, Pavićević D, Zatezalo A, Mijatović M, Grubač B (2008) Rezultati kompleksnih istraživanja Ogoreličke pećine. Zaštita Prirode 59:51–66
Newman MM, Kloepper LN, Duncan M, McInroy JA, Kloepper JW (2018) Variation in bat guano bacterial community composition with depth. Front Microbiol 9:914
pubmed: 29867825 pmcid: 5958644
Nieves-Rivera ÁM, Santos-Flores CJ, Dugan FM, Miller TE (2009) Guanophilic fungi in three caves of southwestern Puerto Rico. Int J Speleol 38(1):61–70
Nováková A (2009) Microscopic fungi isolated from Domica cave system (Slovak karst National Park, Slovakia). A review. Int J Speleol 38(1):71–82
Nováková A, Elhottová D, Krištůfek V, Lukešová A, Hill P, Kováč L, Mock A, Luptačik P (2005) Feeding sources of invertebrates in the Ardovská Cave and Domica Cave systems – preliminary results. In: Tajovský K, Schlaghamerský J, Pižl V (eds) Contributions to soil zoology in Central Europe. Institute of Soil Biology of the Czech Academy of Sciences, České Budějovice, pp 107–112
O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7:103–116
Ogórek R, Lejman A, Matkowski K (2013) Fungi isolated from Niedźwiedzia cave in Kletno (lower Silesia, Poland). Int J Speleol 42(2):161–166
Ogórek R, Dyląg M, Kozak B, Višnovska Z, Tančinová D, Lejman A (2016) Fungi isolated and quantified from bat guano and air in Harmanecká and Driny Caves (Slovakia). J Cave Karst Stud 78(1):41–49
Pitt JI (1979) The genus Penicillium and its teleomorphic state Eupenicillium and Talaromyces. Academic Press, London
Porca M, Jurado V, Martin-Sanchez MP, Hermonis B, Bastian F, Alabouvette C, Saiz-Jimenez C (2011) Aerobiology: an ecological indicator for early detection and control of fungal outbreaks in caves. Ecol Indic 11:1594–1598
Poulson TL, Lavoie KH (2000) The trophic basis of subsurface ecosystems. In: Wilkens H, Culver DC, Humphreys WF (eds) Ecosystems of the world, Subterranean ecosystems, vol 30. Elsevier, Amsterdam, pp 231–249
Rabasović MD, Pantelić DV, Jelenković BM, Ćurčić SB, Rabasović MS, Vrbica MD, Lazović VM, Ćurčić BPM, Krmpot AJ (2015) Nonlinear microscopy of chitin and chitinous structures: a case study of two cave-dwelling insects. J Biomed Opt 20:016010
pubmed: 25574994
Raper BK, Fennel DI (1965) The genus Aspergillus. The Williams and Wilkins company, Baltimore
Ristivojević P, Dimkić I, Trifković J, Berić T, Vovk I, Milojković-Opsenica D, Stanković S (2016) Antimicrobial activity of Serbian propolis evaluated by means of MIC, HPTLC, bioautography and chemometrics. PLoS One 11:e0157097
pubmed: 27272728 pmcid: 4896501
Rocha-Silva F, Figueiredo SM, Silveira TT, Assunção CB, Campolina SS, Pena-Barbosa JP, Rotondo A, Caligiorne RB (2014) Histoplasmosis outbreak in Tamboril cave—Minas Gerais state, Brazil. Med Mycol Case Rep 4:1–4
pubmed: 24567897
Roe AD, Rice AV, Coltman DW, Cooke JE, Sperling FA (2011) Comparative phylogeography, genetic differentiation and contrasting reproductive modes in three fungal symbionts of a multipartite bark beetle symbiosis. Mol Ecol 20:584–600
pubmed: 21166729
Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010) Food and indoor fungi. CBS-KNAW Fungal Biodiversity Centre, Utrecht
Savković Ž, Unković N, Stupar M, Franković M, Jovanović M, Erić S, Šarić K, Stanković S, Dimkić I, Vukojević J, Grbić ML (2016) Diversity and biodeteriorative potential of fungal dwellers on ancient stone stela. Int Biodeterior Biodegradation 115:212–223
Stanković S, Dimkić I, Vujisić L, Pavković-Lučić S, Jovanović Z, Stević T, Sofrenić I, Mitić B, Tomić V (2016) Chemical defence in a millipede: evaluation and characterization of antimicrobial activity of the defensive secretion from Pachyiulus hungaricus (Karsch, 1881) (Diplopoda, Julida, Julidae). PLoS One 11:e0167249
pubmed: 27907048 pmcid: 5132186
Suzina NE, Mulyukin AL, Kozlova AN, Shorokhova AP, Dmitriev VV, Barinova ES, Mokhova ON, Duda VI (2004) Ultrastructure of resting cells of some non-spore-forming bacteria. Microbiology 73(4):435–447
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. J Mol Evol 30:2725–2729
Ulloa M, Lappe P, Aguilar S, Park H, Pérez-Mejía A, Toriello C, Taylor LM (2006) Contribution to the study of the mycobiota present in the natural habitats of Histoplasma capsulatum: an integrative study in Guerrero, Mexico. Rev Mex Biodivers 77:153–168
Vanderwolf KJ, Malloch D, Ivanova VN, McAlpine FD (2016) Lack of cave-associated mammals influences the fungal assemblages of insular solution caves in eastern Canada. J Cave Karst Stud 78(3):198–207
Vandžurová A, Bačkor P, Javorský P, Pristaš P (2013) Staphylococcus nepalensis in the guano of bats (Mammalia). Vet Microbiol 164:116–121
pubmed: 23462520
Vesović N, Ćurčić S, Vujisić L, Nenadić M, Krstić G, Perić-Mataruga V, Milosavljević S, Antić D, Mandić B, Petković M, Vučković I, Marković Đ, Vrbica M, Ćurčić B, Makarov S (2015) Molecular diversity of compounds from pygidial gland secretions of cave-dwelling ground beetles (Insecta: Coleoptera: Carabidae): the first evidence. J Chem Ecol 41:533–539
pubmed: 26044390
Vrbica M, Petrović A, Pantelić D, Krmpot A, Rabasović M, Pavlović D, Jovanić S, Guéorguiev B, Goranov S, Vesović N, Antić D, Marković Đ, Petković M, Stanisavljević L, Ćurčić S (2018) The genus Pheggomisetes Knirsch, 1923 (Coleoptera: Carabidae: Trechinae) in Serbia: taxonomy, morphology and molecular phylogeny. Zool J Linnean Soc 183:347–371
Wallace SJ, Morrison JL, Botting KJ, Kee TW (2008) Second-harmonic generation and two-photon-excited autofluorescence microscopy of cardiomyocytes: quantification of cell volume and myosin filaments. J Biomed Opt 13:064018
pubmed: 19123664
Watanabe T (2002) Soil and seed fungi. Morphologies of cultured fungi and key to species. CRC Press, London
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

Auteurs

Ivica Dimkić (I)

University of Belgrade - Faculty of Biology, Studentski Trg 16, Belgrade, 11000, Serbia. ivicad@bio.bg.ac.rs.

Slaviša Stanković (S)

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

Jovana Kabić (J)

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

Miloš Stupar (M)

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

Marija Nenadić (M)

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

Milica Ljaljević-Grbić (M)

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

Vladimir Žikić (V)

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

Ljubodrag Vujisić (L)

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

Vele Tešević (V)

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

Nikola Vesović (N)

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

Dejan Pantelić (D)

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

Svetlana Savić-Šević (S)

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

Jelena Vukojević (J)

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

Srećko Ćurčić (S)

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

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH