Diversity and biosynthetic potential of culturable aerobic heterotrophic bacteria isolated from Magura Cave, Bulgaria

International Journal of Speleology

Volumn 42, Issue 1, 2013, Pages 65-76

  Tomova, Iva ^a   Lazarkevich, Irina ^a   Tomova, Anna ^a   Kambourova, Margarita ^a   Vasileva Tonkova, Evgenia ^a  

^a INSTITUTE OF MICROBIOLOGY   (Bulgaria)

Author keywords

16S rDNA; Antimicrobial activity; Caves; Culturable bacteria; Enzyme production; Hemolytic activity; Magura Cave

Indexed keywords

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOACTIVITY; CAVE; DNA; ENZYME ACTIVITY; GENETIC ANALYSIS; KARST; METABOLITE; PHYLOGENETICS; SPECIES DIVERSITY; TAXONOMY;

BULGARIA; MAGURA CAVE;

ACINETOBACTER; ACTINOBACTERIA; ARTHROBACTER; BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); BACTEROIDETES; ENTEROBACTER; FIRMICUTES; MICROCOCCUS; MYROIDES; NEGIBACTERIA; OBESUMBACTERIUM; POSIBACTERIA; PROTEOBACTERIA; PSEUDOMONAS; SERRATIA; SPHINGOBACTERIUM; STENOTROPHOMONAS;

EID: 84880620634     PISSN: 03926672     EISSN: 1827806X     Source Type: Journal    
DOI: 10.5038/1827-806X.42.1.8     Document Type: Article

References (61)

1. Allemand L. & Bahn P.G., 2005, Best way to protect rock art is to leave it alone. Nature, 433: 800. http://dx.doi.org/10.1038/433800c
2. Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J., 1990, Basic local alignment search tool. Journal of Molecular Biology, 215: 403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2
3. Bae H.D., Yanke L.J., Cheng K.-J. & Selinger L.B., 1999, A novel staining method for detecting phytase activity. Journal of Microbiological Methods, 39: 17-22. http://dx.doi.org/10.1016/S0167-7012(99)00096-2.
4. Banat, I.M., Franzetti A., Gandolfi I., Bestetti G., Martinotti, M.G., Fracchia L., Smyth T.J. & Marchant R., 2010, Microbial biosurfactants production, applications and future potential. Applied Microbiology and Biotechnology, 87: 427-444. http://dx.doi.org/10.1007/s00253-010-2589-0
5. Barton H.A. & Northup D.E., 2007, Geomicrobiology in cave environments: past, current and future perspectives. Journal of Caves & Karst Studies, 69: 163-178.
6. Bastian F., Alabouvette C. & Saiz-Jimenez C., 2009, Bacteria and free-living amoeba in the Lascaux Cave. Research in Microbiology, 160: 38-40. http://dx.doi.org/10.1016/j.resmic.2008.10.001
7. Boschker H.T.S. & Cappenberg T.E., 1998, Patterns of extracellular enzyme activities in littoral sediments of Lake Gooimeer, The Netherlands. FEMS Microbiology and Ecology, 25: 79-86. http://dx.doi.org/10.1111/j.1574-6941.1998.tb00461.x
8. Bottos E., 2004, Screening for Biosurfactant Production in Actinomycetes Isolated from Cave and Forest Soils. (Student Poster Presentation).
9. Burgess J.G., Jordan E.M., Bregu M., Mearns-Spragg A. & Boyd K.G., 1999, Microbial antagonism: A neglected avenue of natural products research. Journal of Biotechnology, 70: 27-32. http://dx.doi.org/10.1016/S0168-1656(99)00054-1
10. Burgos-Diaz C., Pons R., Espuny M.J., Aranda F.J., Tereul J.A., Manresa A., Ortiz A. & Marqués A.M., 2011, Isolation and partial characterization of a biosurfactant mixture produced by Sphingobacterium sp. isolated from soil. Journal of Colloid and Interface Science, 361: 195-204. http://dx.doi.org/10.1016/j.jcis.2011.05.054
11. Cabeza M.S., Baca F.L., Puntes E.M., Loto F., Baigorí M.D. & Morata V.I., 2011, Selection of psychrotolerant microorganisms producing cold-active pectinases for biotechnological processes at low temperature. Food Technology & Biotechnology, 49: 187-195.
12. Campbell J.W., Watson A., Watson C., Ball H. & Pirkle R., 2011, Escherichia coli, other coliform, and environmental chemoheterotrophic bacteria in isolated water pools from six caves in northern Alabama and northwestern Georgia. Journal of Cave and Karst Studies, 73: 75-82. http://dx.doi.org/10.4311/jcks2009mb0131
13. Cañaveras J.C., Sanchez-Moral S., Sloer V. & Saiz-Jimenez C., 2001, Microorganisms and microbially induced fabrics in cave walls. Geomicrobiological Journal, 18: 223-240. http://dx.doi.org/10.1080/01490450152467769
14. Castanier S., Le Méteyer-Levrel G. & and Martire L., 2000, Bacterial roles in the precipitation of carbonate minerals. In: Riding R.E. & Awramik S.M. (Eds.), Microbial sediments. Heidelberg: Springer: 32-39.
15. Cavicchioli R., Charlton T., Ertan H., Mohd Omar S., Siddiqui K.S. & Williams T.J., 2011, Biotechnological uses of enzymes from psychrophiles. Microbial Biotechnology, 4: 449-460. http://dx.doi.org/10.1111/j.1751-7915.2011.00258.x
16. Chelius M.K. & Moore J.C., 2004, Molecular phylogenetic analysis of archaea and bacteria in Wind Cave, South Dakota. Geomicrobiology Journal, 21: 123-134. http://dx.doi.org/10.1080/01490450490266389
17. Cotty P.J., Cleveland T.E., Brown R.L. & Mellon J.E., 1990, Variation in polygalacturonase production among Aspergillus flavus isolates. Applied & Environmental Microbiology, 56: 3885-3887.
18. Davis J. & Webb V., 1998, Antibiotic resistance in bacteria. In: Krause R.M. (Ed.), Emerging infections: biomedical research reports. New York: Academic Press: 239-273. http://dx.doi.org/10.1016/S1874-5326(07)80032-9
19. Dhawale M.R., Wilson J.J., Khachatourians G.G. & Ingledew W.M., 1982, Improved method for detection of starch hydrolysis. Applied & Environmental Microbiology, 44: 747-750.
20. Engel A.S., 2010, Microbial diversity of cave ecosystems. In: Loy, A., Mandl, M. & Barton, L.L. (Eds.), Geomicrobiology: Molecular and Environmental Perspective. New York: Springer: 219-238.
21. Fox J. L., 2008, Some say Lascaux Cave paintings are in microbial "crisis" mode. Microbe, 3: 110-112.
22. Gerday C., Aittaleb M., Bentahir M., Chessa J.P., Claverie P., Collins T., D'Amico S., Dumont J., Garsoux G., Georlette D., Hoyoux A., Lonhienne T., Meuwis M.A. & Feller G., 2000, Cold-adapted enzymes: From fundamentals to biotechnology. Trends in Biotechnology, 18: 103-107. http://dx.doi.org/10.1016/S0167-7799(99)01413-4
23. Gerič B., Pipan T. & Mulec J., 2004, Diversity of culturable bacteria and meiofauna in the epikarst of Škocjanske jame Caves (Slovenia). Acta carsologica, 33: 301-309.
24. Gounot A.M., 1994, Microbial ecology of groundwaters. In: Gibert J., Danielopol D.L., & Stanford J.A. (Eds). Groundwater ecology. San Diego, CA: Academic Press: 189-215.
25. Groth I. & Saiz-Jimenez C., 1999, Actinomycetes in hypogean environments. Geomicrobiology Journal, 16: 1-8. http://dx.doi.org/10.1080/014904599270703
26. Groth I., Schumann P., Laiz L., Sanchez-Moral S., Cañaveras J.C. & Saiz-Jimenez C., 2001, Geomicrobiological study of the Grotta dei Cervi, Porto Badisco, Italy. Geomicrobiology Journal, 18: 241-258. http://dx.doi.org/10.1080/01490450152467778
27. Groth I., Vettermann R., Schuetze B. et al., 1999, Actinomycetes in karstic caves of northern Spain (Altamira and Tito Bustillo). Journal of Microbiological Methods, 36: 115-1220. http://dx.doi.org/10.1016/S0167-7012(99)00016-0
28. Ikner L.A., Toomey R.S., Nolan G., Neilson J.W., Pryor B.M. & Maier R.M., 2007, Culturable microbial diversity and the impact of tourism in Kartchner Caverns, Arizona. Microbial Ecology, 53: 30-42. http://dx.doi.org/10.1007/s00248-006-9135-8
29. Jurado V., Laiz L., Rodriguez-Nava V., Boiron P., Hermosin B., Sanchez-Moral S. & Saiz-Jimenez C., 2010, Pathogenic microorganisms in caves. International Journal of Speleology, 39: 15-21. http://dx.doi.org/10.5038/1827-806X.39.1.2
30. Khizhnyak S.V., Tausheva I.V., Berezikova A.A., Nesterenko E.V. & Rogozin D.Y., 2003, Psychrophilic and psychrotolerant heterotrophic microorganisms of middle Siberian karst cavities. Russian Journal of Ecology, 34: 231-235. http://dx.doi.org/10.1023/A:1024537513439
31. Kim B.S., Lee J.Y. & Hwang B.K., 1998, Diversity of actinomycetes antagonistic to plant pathogenic fungi in cave and sea-mud soils of Korea. Journal of Microbiology, 36: 86-92.
32. Lavoie K.H. & Northup D.E., 2006, Bacteria as indicators of human impact in caves. In: Rea G.T. (Ed.), 17th National Cave and Karst Management Symposium, Proceedings. Albany, NY: NICKMS Steering Committee: 40-47.
33. MacFaddin J. F., 2000, Biochemical tests for the identification of medical bacteria, 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins.
34. Maidak B.L., Larsen N., McCaughey M.J., Overbeek R., Olsen G.J., Fogel K., Blandy J. & Woese C.R., 1994, The Ribosomal Database Project. Nucleic Acids Research, 22: 3485-3487. http://dx.doi.org/10.1093/nar/22.17.3485
35. Margesin R. & Miteva V., 2011, Diversity and ecology of psychrophilic microorganisms. Research in Microbiology, 162: 346-361. http://dx.doi.org/10.1016/j.resmic.2010.12.004
36. Martinez N.G., Sinsabaugh R.L. & Northup D.E., 2011, Human Impact on Extracellular Enzyme Activity within Carlsbad Cavern and Lechuguilla and Spider Caves in Carlsbad Caverns National Park, New Mexico. http://sacnas.confex.com/sacnas/2011/webprogram/Paper1801.html
37. Mendes Ferreira A., Clímaco M.C. & Mendes Faia A., 2001, The role of non-Saccharomyces species in releasing glycosidic bound fraction of grape aroma components--a preliminary study. Journal of Applied Microbiology, 91: 67-71. http://dx.doi.org/10.1046/j.1365-2672.2001.01348.x
38. Moran A.C., Martinez M.A. & Siñeriz F., 2002, Quantification of surfactin in culture supernatants by hemolytic activity. Biotechnology Letters, 24: 177-180. http://dx.doi.org/10.1023/A:1014140820207
39. Morita R.Y., 1975, Psychrophilic bacteria. Bacteriological Reviews, 39: 144-167.
40. Mulec J., Krištůfek V. & Chroňáková A., 2012, Comparative microbial sampling from eutrophic caves in Slovenia and Slovakia using RIDA®COUNT test kits. International Journal of Speleology, 41: 1-8. http://dx.doi.org/10.5038/1827-806X.41.1.1
41. Munster U. & De Haan, H., 1998, The role of microbial extracellular enzymes in the transformation of dissolved organic matter in humic waters. Ecology Studies, 133: 199-257.
42. Northup D.E. & Lavoie K.H., 2001, Geomicrobiology of caves: A review. Geomicrobiology Journal, 18: 199, 222. http://dx.doi.org/10.1080/01490450152467750
43. Rashid N., Yuji S., Satoshi E., Haruyuki A. & Tadayuki I., 2001, Low-temperature lipase from psychrotrophic Pseudomonas sp. strain KB700A. Applied & Environmental Microbiology, 67: 4064-4069. http://dx.doi.org/10.1128/AEM.67.9.4064-4069.2001
44. Russell N.J., 1998, Molecular adaptations in psychrophilic bacteria: potential for biotechnological applications. In: Scheper T. (Ed.), Advances in Biochemical Engineering/ Biotechnology. Berlin: Springer, 61: 1-21.
45. Sanchez L.A., Gomez F.F. & Delgado O.D., 2009, Cold-adapted microorganisms as a source of new antimicrobials. Extremophiles, 13: 111-120. http://dx.doi.org/10.1007/s00792-008-0203-5
46. Schabereiter-Gurtner C., Saiz-Jimenez C., Piñar G., Lubitz W. & Rölleke S., 2002a, Altamira cave Paleolithic paintings harbor partly unknown bacterial communities. FEMS Microbiology Letters, 211: 7-11. http://dx.doi.org/10.1111/j.1574-6968.2002.tb11195.x
47. Schabereiter-Gurtner C., Saiz-Jimenez C., Piñar G., Lubitz W. & Rölleke S., 2002b, Culture-independent analyses of bacterial communities on paleolithic paintings and surrounding rock walls in karstic caves (Altamira, Tito Bustillo, La Garma and Llonin). Coalition Newsletter, 5: 7-10.
48. Slattery M., Rajbhandari I. & Wesson K., 2001, Competition mediated antibiotic induction in the marine bacterium Streptomyces tenjimariensis. Microbial Ecology, 41: 90-96.
49. Smalås A.O., Leiros H.K., Os V. & Willassen N.P., 2000, Cold adapted enzymes. Biotechnology Annual Review, 6: 1-57. http://dx.doi.org/10.1016/S1387-2656(00)06018-X
50. Smilbert R.M., 1994, Phenotypic characterization. In: Gerhardt P., Murray R.E.G., Wood W.A. & Krieg N.R. (Eds.), Methods for general and molecular microbiology. Washington: American Society for Microbiology: 611-654.
51. Stoychev T., 1994, Eneolithic paintings from Magoura cave, Bulgaria. (in Bulgarian; English summary). Annuary of Department of Architecture NBU, 1: 307-320.
52. Stoytchev T., 1995, Newfound prehistorical imiges and signs in Magoura cave and Tzarevetz cave complex (in Bulgarian). Architecture Discoveries and Excavations during 1994. Smolian: 13-15.
53. Swofford D.L., 2002, PAUP: Phylogenetic Analysis Using Parsimony (and other methods), version 4. Sunderland, MA: Sinauer Associates.
54. Teather R.M. & Wood P.J., 1982, Use of Congo red, polysaccharide interaction in enumeration and characterization of cellulohydrolytic bacteria from the bovine rumen. Applied and Environmental Microbiology, 53: 41-46.
55. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F. & Higgins D.G., 1997, The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25: 4876-4882. http://dx.doi.org/10.1093/nar/25.24.4876
56. Urzì C., De Leo F., Bruno L. & Albertano P., 2010, Microbial diversity in Paleolithic caves: A study case on the phototrophic biofilms of the Cave of Bats (Zuheros, Spain). Microbial Ecology, 60: 116-129. http://dx.doi.org/10.1007/s00248-010-9710-x
57. Van den Burg B., 2003, Extremophiles as a source for novel enzymes. Current Opinion in Microbiology, 6: 213-218. http://dx.doi.org/10.1016/S1369-5274(03)00060-2
58. Vinardell M.P. & Infante M.R., 1999, The relationship between the chain length of non-ionic surfactants and their hemolytic action on human erythrocytes. Comparative Biochemistry & Physiology Part C, 124: 117-120.
59. Weisburg W.G., Barns S.M., Pelletier D.A. & Lane D.J., 1991, 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 173: 697-703.
60. Yucel S. & Yamac M., 2010, Selection of Streptomycetes isolates from Turkish karstic caves against antibiotic resistant microorganisms. Pakistan Journal of Pharmaceutical Sciences, 23: 1-6.
61. Zhou J.P., Gu Y.Q., Zou C.S., Mo M.H., 2007, Phylogenetic diversity of bacteria in an earth-vave in Guizhou Province, Southwest of China. Journal of Microbiology, 45: 105-112.