Diversity of cultivable bacteria involved in the formation of macroscopic microbial colonies (cave silver) on the walls of a cave in Slovenia

International Journal of Speleology

Volumn 43, Issue 1, 2014, Pages 45-56

  Velikonja, Blagajana Herzog ^a   Tkavc, Rok ^a,b   Pašić, Lejla ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

Author keywords

16S rRNA; Bacteria; Cave; Cultivation; Microbial colonisations

Indexed keywords

BACTERIUM; BIODIVERSITY; CAVE SYSTEM; COLONIZATION; CULTIVATION; GENE; KARST; MICROORGANISM; RNA;

SLOVENIA;

AEROCOCCUS; AGROBACTERIUM; AGROCOCCUS; ARTHROBACTER; BACTERIA (MICROORGANISMS); BOSEA (BACTERIA); KOCURIA; LYSOBACTER; MICROBACTERIUM; MICROCOCCUS; OERSKOVIA; PAENIBACILLUS; PSEUDOMONAS; RHODOCOCCUS; SPHINGOMONAS; STREPTOMYCES;

EID: 84890883725     PISSN: 03926672     EISSN: 1827806X     Source Type: Journal    
DOI: 10.5038/1827-806X.43.1.5     Document Type: Article

References (52)

1. Baba H., Nada T., Okhusu K., Ezaki T., Hasegawa Y. & Paterson D.L., 2009-First case of bloodstram infection caused by Rhodococcus erythropolis. Journal of Clinical Microbiology, 47: 2667-2669. http://dx.doi.org/10.1128/JCM.00294-09
2. Banerjee S. & Joshi S.R., 2013-Insights into cave architecture and the role of bacterial biofilm. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences: 1-14.
3. Banks E.D., Taylor, N.M., Gulley J., Lubbers B.R., Giarrizo J.G., Bullen H.A., Hoehler T.M. & Barton H.A., 2010-Bacterial calcium carbonate precipitation in cave environments: a function of calcium homeostasis. Geomicrobiology Journal, 27: 444-454. http://dx.doi.org/10.1080/01490450903485136
4. Barton H.A. & Jurado V., 2007-What's up down there? Microbial diversity in caves. Microbe, 2: 132-138.
5. Bhullar K., Waglechner N., Pawlowski A., Koteva K., Banks E.D., Johnston M.D., Barton H.A. & Wright G.A., 2012-Antibiotic resistance is prevalent in an isolated cave microbiome. PloS ONE, 7: e34953. http://dx.doi.org/10.1371/journal.pone.0034953
6. Bredholt H. & Fjaervik E., 2008-Actinomycetes from sediments in the Trondheim Fjord, Norway: Diversity and biological activity. Marine Drugs, 6: 12-24. http://dx.doi.org/10.3390/md6010012
7. Bulina T.I., Alferova I.V. & Terekhova L.P., 1997-A novel approach to isolation of actinomycetes involvin irradiation of soil samples with microwaves. Microbiology, 66: 231-234.
8. Burnham K.P. & Overton W.S., 1978-Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika, 65: 625-633. http://dx.doi.org/10.1093/biomet/65.3.625
9. Bussmann I., Philipp B. & Schink B., 2001-Factors influencing the cultivability of lake water bacteria. Journal of Microbiological Methods, 47: 41-50. http://dx.doi.org/10.1016/S0167-7012(01)00289-5
10. Cheeptham N., Sadoway T., Rule D., Watson K., Moote P., Soliman L., Azad N., Donkor K. & Horne D., 2013-Cure from the cave: volcanic cave actinomycetes and their potential in drug discovery. International Journal of Speleology, 42: 35-47. http://dx.doi.org/10.5038/1827-806X.42.1.5
11. Cuezva S., Fernandez-Cortes A., Porca E., Pašić L., Jurado V., Hernandez-Marine M., Serrano-Ortiz P., Hermosin B., Cañaveras J.C., Sanchez-Moral S. & Saiz-Jimenez C. (2012). The biogeochemical role of Actinobacteria in Altamira Cave, Spain. FEMS Microbiology Ecology, 81: 281-290. http://dx.doi.org/10.1111/j.1574-6941.2012.01391.x
12. th Field conference, Carlsbad region, New Mexico and West Texas, p. 129-136.
13. Davis K.E., Joseph S. J & Janssen P.H., 2005-Effects of growth medium, inoculum size, and incubation time on culturability and isolation of soil bacteria. Applied and Environmental Microbiology, 71: 826-834. http://dx.doi.org/10.1128/AEM.71.2.826-834.2005
14. Edgar R.C., 2004-MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32: 1792-1797. http://dx.doi.org/10.1093/nar/gkh340
15. Fernandez-Cortes A., Cuezva S., Sanchez-Moral S., Cañaveras J.C., Porca E., Jurado V., Martin-Sanchez P.M. & Saiz-Jimenez C., 2011-Detection of human-induced environmental disturbances in a show cave. Environmental Science and Pollution Research, 18: 1037-1045. http://dx.doi.org/10.1007/s11356-011-0513-5
16. Ferriss R.S. 1984-Effects of microwave oven treatment of microorganisms in soil. Phytopathology, 74: 121-126. http://dx.doi.org/10.1094/Phyto-74-121
17. Garcia M.G., Moya M., Spilde M.N., Stone F.D. & Northup D.E. 2009-Discovering new diversity in Hawaiian lava tube microbial mats. In: White W.B. (Ed.), Proceedings of the 15th International Congress of Speleology, 1: 364-369.
18. Hall T.A., 1999-BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95-98.
19. Hardin G., 1960-The Competitive Exclusion Principle. Science, 131: 1292-1297. http://dx.doi.org/10.1126/science.131.3409.1292
20. Janssen P.H., Yates P.S., Grinton B.E., Taylor P.M. & Sait M., 2002-Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria and Verrucomicrobia. Applied and Environmental Microbiology, 68: 2391-2396. http://dx.doi.org/10.1128/AEM.68.5.2391-2396.2002
21. Johnston M.D., Millette J., Banks E.D., Jurado V. & Barton H.A., 2011-The culturable diversity of oligotrophic heterotrophs: the Lechuguilla cave culture library. New Orleans: Proceedings of the American Society for Microbiology General Meeting, N149, 1795 p.
22. Johnston M.D., Muench B.A., Banks E.D. & Barton H.A., 2012-Human urine in Lechuguilla Cave: the microbiological impact and potential for bioremediation. Journal of Cave and Karst Studies, 74: 278-291. http://dx.doi.org/10.4311/2011MB0227
23. Jurado V., Boiron P., Kroppenstedt R.M., Laurent F., Couble A., Laiz L., Klenk H.P., González J.M., Saiz-Jimenez C., Mouniée D., Bergeron E. & Rodríguez-Nava V., 2008-Nocardia altamirensis sp. nov., isolated from Altamira cave, Cantabria, Spain. International Journal of Systematics and Evolutionary Microbiology, 58: 2210-2214. http://dx.doi.org/10.1099/ijs.0.65482-0
24. Jurado V., Gonzalez J.M., Laiz L. & Saiz-Jimenez C., 2006-Aurantimonas altamirensis sp. nov., a member of the order Rhizobiales isolated from Altamira Cave. International Journal of Systematic and Evolutionary Microbiology, 56: 2583-2585. http://dx.doi.org/10.1099/ijs.0.64397-0
25. Jurado V., Kroppenstedt R.M., Saiz-Jimenez C., Klenk H.P., Mouniée D., Laiz L., Couble A., Pötter G., Boiron P. & Rodríguez-Nava V., 2009-Hoyosella altamirensis gen. nov., sp. nov., a new member of the order Actinomycetales isolated from a cave biofilm. International Journal of Systematic and Evolutionary Microbiology, 59: 3105-3110. http://dx.doi.org/10.1099/ijs.0.008664-0
26. Jurado V., Laiz L., Rodriguez-Nava V., Boiron P., Hermosin H., Sanchez-Moral S. & Saiz-Jimenez C., 2010-Pathogenic and opportunistic microorganisms in caves. International Journal of Speleology, 39: 15-24. http://dx.doi.org/10.5038/1827-806X.39.1.2
27. Keswick B.H., Wang D.S. & Gerba C.P., 1982-The use of microorganisms as ground-water tracers: a review. Groundwater, 20: 142-149. http://dx.doi.org/10.1111/j.1745-6584.1982.tb02741.x
28. Kim O.S., Cho Y.J., Lee K., Yoon S.H., Kim M., Na H., Park S.C., Jeon Y.S., Lee J.H., Yi H., Won S. & Chun J., 2012-Introducing EzTaxon-e: a prokaryotic 16S rRNA Gene sequence database with phylotypes that represent uncultured species. International Journal of Systematic and Evolutionary Microbiology, 62: 716-721. http://dx.doi.org/10.1099/ijs.0.038075-0
29. Ko K.S., Oh W.S., Lee M.Y., Lee J.H., Lee H., Peck K.R., Lee N.Y. & Song J.H., 2006-Bacillus infantis sp. nov. and Bacillus idriensis sp. nov., isolated from a patient with neonatal sepsis. International Journal of Systematics and Evolutionary Microbiology, 56: 2541-2544. http://dx.doi.org/10.1099/ijs.0.64213-0
30. Laiz L., Gonzalez-Delvalle M., Hermosin B., Ortiz-Martinez A. & Saiz-Jimenez, C., 2003-Isolation of cave bacteria and substrate utilization at different temperatures. Geomicrobiology Journal, 20: 479-489. http://dx.doi.org/10.1080/713851125
31. Laffineur K., Avesani V., Cornu G., Charlier J., Janssens M., Wauters G. & Delmée M., 2003-Bacteremia due to a novel Microbacterium species in a patient with leukemia and description of Microbacterium paraoxydans sp. nov. Journal of Clinical Microbiology, 41: 2242-2246. http://dx.doi.org/10.1128/JCM.41.5.2242-2246.2003
32. Ma E.S., Wong C.L., Lai K.T., Chan E.C., Yam W.C. & Chan A.C., 2005-Kocuria kristinae infection associated with acute cholecystitis. BMC Infectious Diseases, 5: 60. http://dx.doi.org/10.1186/1471-2334-5-60
33. th International Congress of Speleology, 2: 709-713.
34. Mulec J., 2008-Microorganisms in hypogeon: examples from Slovenian karst caves. Acta Carsologica, 37: 153-160.
35. Niyomvong N., Pathom-Aree W., Thamchaipenet A. & Duangmal K., 2012-Actinomycetes from tropical limestone caves. Chiang Mai Journal of Science, 39: 373-388.
36. Northup D.E., Carr D.L., Crocker M.T., Cunningham K.I., Hawkins L.K., Leonard P. & Welbourn W.C., 1994-Biological investigations in Lechuguilla Cave, Carlsbad Caverns National Park, New Mexico. Bulletin of the National Speleological Society, 56: 54-63.
37. Northup, D.E., Connolly, C.A., Trent, A., Peck, V.M., Spilde, M.N., Welbourn, W.C. & Natvig, D.O. 2008-The nature of bacterial communities in Four Windows Cave, El Malpais National Monument, New Mexico, USA. AMCS Bulletin 19: 119-125.
38. Northup D.E., Melim L.A., Spilde M.N., Hathaway J.J.M., Garcia M.G., Moya M., Stone F.D., Boston P.J., Dapkevicius M.L.N.E. & Riquelme C., 2011-Lava cave microbial communities within mats and secondary mineral deposits: implications for life detection on other planets. Astrobiology, 11: 601-618. http://dx.doi.org/10.1089/ast.2010.0562
39. Palmer A.N., Palmer M.V. & Davis D.G., 1991-Geology and origin of Lechuguilla cave. In: Taylor M.R. (Ed.), Lechuguilla-Jewel of the underground, Speleoprojects, Basel, Switzerland: 22-31.
40. Pašić L., Kovče B., Sket B. & Herzog-Velikonja B., 2010-Diversity of microbial communities colonizing the walls of a Karstic cave in Slovenia. FEMS Microbiology Ecology, 71: 50-60. http://dx.doi.org/10.1111/j.1574-6941.2009.00789.x
41. Porca E., Jurado V., Žgur-Bertok D., Saiz-Jimenez C. & Pašić L., 2012-Comparative analysis of yellow microbial communities growing on the walls of geographically distinct caves indicates a common core of microorganisms involved in their formation. FEMS Microbiology Ecology, 81: 255-266. http://dx.doi.org/10.1111/j.1574-6941.2012.01383.x
42. Portillo M.C., Gonzalez J.M. & Saiz-Jimenez C., 2008-Metabolically active microbial communities of yellow and grey colonizations on the walls of Altamira Cave, Spain. Journal of Applied Microbiology, 104: 681-691. http://dx.doi.org/10.1111/j.1365-2672.2007.03594.x
43. Portillo M.C., Saiz-Jimenez C. & Gonzalez J.M., 2009-Molecular characterization of total and metabolically active bacterial communities of 'white colonization' in the Altamira Cave, Spain. Research in Microbiology, 160: 41-47. http://dx.doi.org/10.1016/j.resmic.2008.10.002
44. Rusterholtz K.J. & Mallory L.M., 1994-Density, activity, and diversity of bacteria indigenous to a karstic aquifier. Microbial Ecology, 28: 79-99. http://dx.doi.org/10.1007/BF00170249
45. Schabereiter-Gurtner C., Saiz-Jimenez C., Piñar G., Lubitz W. & Rölleke S., 2004-Phylogenetic diversity of bacteria associated with palaeolithic paintings and surrounding rock walls in two Spanish caves (Llonin and La Garma). FEMS Microbiology Ecology, 47: 235-247. http://dx.doi.org/10.1016/S0168-6496(03)00280-0
46. Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.A., Oakley B.B., Parks D.H., Robinson C.J., Sahl J.W., Stres B., Thallinger G.G., Van Horn D.J., Weber C.F., 2009-Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75: 7537-7541. http://dx.doi.org/10.1128/AEM.01541-09
47. Seong C.N., Choi J.H. & Baik K-S., 2001-An improved selective isolateion of rare actinomycetes from forest soil. The Journal of Microbiology, 39: 17-23.
48. Tamura K., Peterson D., Peterson N., Stecher G., Nei M. & Kumar S., 2011-MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28: 2731-2739. http://dx.doi.org/10.1093/molbev/msr121
49. Vela A.I., Gutiérrez M.C., Falsen E., Rollán E., Simarro I., García P., Domínguez L., Ventosa A. & Fernández-Garayzáabal J.F., 2006-Pseudomonas simiae sp. nov., isolated from clinical specimens from monkeys (Callithrix geoffroyi). International Journal of Systematics and Evolutionary Microbiology, 56: 2671-2676. http://dx.doi.org/10.1099/ijs.0.64378-0
50. Wang D.S., Xue Q.H., Zhu W.J., Zhao J., Duan J.L. & Shen G.H., 2013-Microwave irradiation is a useful tool for improving isolation of actinomycetes from soil. Microbiology 82: 102-110. http://dx.doi.org/10.1134/S0026261712060161
51. Wellington E.M.H. & Cross T., 1983-Taxonomy of antibiotic producing Actinomycetes and new approaches to their selective isolation. In: Bushell M.E. (Eds.), Progress in industrial microbiology? Elsevier, Amsterdam. pp. 36.
52. Yokota A., Takeuchi M., Sakane T. & Weiss N., 1993-Proposal of six new species of the genus Aureobacterium and transfer of Flavobacterium esteraromaticum Omelianski to the genus Aureobacterium as Aureobacterium esteraromaticum comb. nov. International Journal of Systematics and Bacteriology, 43: 555-564. http://dx.doi.org/10.1099/00207713-43-3-555