Pathogenic and opportunistic microorganisms in caves

International Journal of Speleology

Volumn 39, Issue 1, 2010, Pages 15-24

  Jurado, Valme ^c   Laiz, Leonila ^c   Rodriguez Nava, Veronica ^a   Boiron, Patrick ^a   Hermosin, Bernardo ^c   Sanchez Moral, Sergio ^b   Saiz Jimenez, Cesareo ^c  

^a CNRS   (France)

^b MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^c INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SEVILLA   (Spain)

Author keywords

Bacteria; Caves; Fungi; Opportunistic pathogens; Virus

Indexed keywords

BACTERIUM; CAVE; FUNGUS; MICROORGANISM; PATHOGEN; VIRUS;

BACTERIA (MICROORGANISMS); FUNGI;

EID: 77949560492     PISSN: 03926672     EISSN: 1827806X     Source Type: Journal    
DOI: 10.5038/1827-806X.39.1.2     Document Type: Article

References (91)

1. Ajello L., Brown J., Macdonald E. & Head E., 1987. Actinomycetoma caused by Nocardiopsis dassonvillei. Archives of Dermatology, 123: 426.
2. Ara I., Bakir M. A. & Kudo T., 2008 Transfer of Catellatospora koreensis Lee et al. 2000 as Catelliglobosispora koreensis gen. nov., comb. nov. and Catellatospora tsunoense Asano et al. 1989 as Hamadaea tsunoensis gen. nov., comb. nov., and emended description of the genus Catellatospora Asano and Kawamoto 1986 emend. Lee and Hah 2002. International Journal of Systematic and Evolutionary Microbiology, 58: 1950-1960.
3. Assous M.V. & Wilamowski A., 2009 - Relapsing fever borreliosis in Eurasia-forgotten, but certainly not gone! Clinical Microbiology & Infection, 15: 407-414.
4. Barton H.A. & Northup D.E., 2007 Geomicrobiology in cave environments: past, current and future perspectives. Journal of Cave and Karst Studies, 69: 163-178.
5. Barton H.A., Taylor N.T., Kreate M.P., Springer A.C., Oehrle S.A. & Bertog J.L., 2007 - The impact of host rock geochemistry on bacterial community structure in oligotrophic cave environments. International Journal of Speleology 36: 93-104.
6. Bastian F., Alabouvette C. & Saiz-Jimenez C., 2009a Bacteria and free-living amoeba in the Lascaux Cave. Research in Microbiology, 160: 38-40.
7. Bastian F., Alabouvette C. & Saiz-Jimenez C., 2009b The impact of arthropods on fungal community structure in Lascaux Cave. Journal of Applied Microbiology, 106: 1456-1462.
8. Bausch D.G., Nichol S.T., Muyembe-Tamfum J.J. et al., 2006 Marburg hemorrhagic fever associated with multiple genetic lineages of virus. The New England Journal of Medicine, 355: 909-919.
9. Beau F., Bollet C., Coton T., Garnotel E. & Drancourt M., 1999 Molecular identification of a Nocardiopsis dassonvillei blood isolate. Journal of Clinical Microbiology, 37: 3366-3368.
10. Betrán A., Rezusta A., Lezcano M.A., Villuendas M.C., Revillo M.J., Boiron P. & Rodríguez-Nava V., 2009 First Spanish case of nocardiosis caused by Nocardia takedensis. Journal of Clinical Microbiology, 47: 1918-1919.
11. Blanc V., Dalle M., Markarian A., Debunne M. V., Duplay E., Rodriguez-Nava V. & Boiron P., 2007 Gordonia terrae: a difficult-to-diagnose emerging pathogen?. Journal of Clinical Microbiology, 45: 1076-1077.
12. Calaforra Chordi J.M. & Berrocal Pérez J.A., 2008 El Karst de Andalucía. Consejería de Medio Ambiente, Sevilla, 247 p.
13. Carlsohn M. R., Groth I., Tan G. Y. A., Schütze B., Saluz H.-P., Munder T., Yang J., Wink J. & Goodfellow M., 2007a Amycolatopsis saalfeldensis sp. nov., a novel actinomycete isolated from a medieval alum slate mine. International Journal of Systematic and Evolutionary Microbiology, 57: 1640-1646.
14. Carlsohn M. R., Groth I., Spröer C., Schütze B., Saluz H.-P., Munder T. & Stackebrandt E., 2007b Kribbella aluminosa sp. nov., isolated rom a medieval alum slate mine. International Journal of Systematic and Evolutionary Microbiology, 57: 1943-1947.
15. Carlsohn M. R., Groth I., Saluz H.-P., Schumann P. & Stackebrandt E., 2008 Fodinicola feengrottensis gen. nov., sp. nov., an actinomycete isolated from a medieval mine. International Journal of Systematic and Evolutionary Microbiology, 58: 1529-1536.
16. Christen-Zaech S., Patel S. & Mancini A. J., 2008 Recurrent cutaneous Geomyces pannorum infection in three brothers with ichthyosis. Journal of the American Academy of Dermatology, 58: S112-S113.
17. Domsch K.H., Gams W. & Anderson T.H., 2007 Compendium of Soil Fungi. 2nd edition, IHW-Verlag, Eching, 672 p.
18. Dupont J., Jacquet C., Dennetière B., Lacoste S., Bousta F., Orial G., Cruaud C., Couloux A. & Roquebert M. F., 2007 Invasion of the French Paleolithic painted cave of Lascaux by members of the Fusarium solani species complex. Mycologia, 99: 526-533.
19. El Karoui K., Guillet C., Sekkal N., Lanternier F., Méchai F., Hue K., Hiesse C., Mamzer Bruneel M.F., Catherinot E., Viard J.P., Mainardi J.L., Lecuit M., Ferroni A., Lortholary O., 2009 Synergistic effect of carbapenemteicoplanin combination during severe Rhodococcus equi pneumonia in a kidney transplant recipient. Transplant Infectious Disease, 11: 359-362.
20. Engel A.S., Lee N., Porter M.L., Stern L.A., Bennett P.C., Wagner M., 2003 Filamentous "Epsilonproteobacteria" dominate microbial mats from sulfidic cave springs. Applied and Environmental Microbiology, 69: 5503-5511.
21. Gargas A., Trest M.T., Christensen M., Volk T.J. & Blehert D.S., 2009 Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon, 108: 147-154.
22. Ghosheh F.R., Ehlers J.P., Ayres B.D., Hammersmith K.M., Rapuano C.J. & Cohen E.J., 2007 Corneal ulcers associated with aerosolized crack cocaine use. Cornea, 26: 966-9.
23. Goodfellow M. & Williams S. T., 1983 Ecology of actinomycetes. Annual Review of Microbiology, 37: 189-216.
24. Groth I. & Saiz-Jimenez C., 1999 Actinomycetes in hypogean environments. Geomicrobiology Journal, 16: 1-8.
25. Groth I. & Saiz-Jimenez C., 2002 Actinomycetes in caves. Coalition, 4: 12-14.
26. Groth I., Vetermann R., Schuetze B., Schumann P. & Saiz-Jimenez C., 1999 Actinomycetes in kartic caves of Northern Spain (Altamira and Tito Bustillo). Journal of Microbiological Methods, 36: 115-122.
27. Groth I., Schumann P., Schutze B., Augsten K. & Stackebrandt E., 2002 Knoellia sinensis gen. nov., sp. nov. and Knoellia subterranean sp. nov., two novel actinobacteria isolated from a cave. International Journal of Systematic and Evolutionary Microbiology, 52: 77-84.
28. Groth I., Schumann P., Schüetze B., Gonzalez J. M., Laiz L., Saiz-Jimenez C. & Stackebrandt E., 2005 Isoptericola hypogeus sp. nov., isolated from the Roman catacomb of Domitilla. International Journal of Systematic and Evolutionary Microbiology, 55: 1715-1719.
29. Groth I., Schumann P., Schüetze B., Gonzalez J. M., Laiz L., Suihko M.-L. & Stackebrandt E., 2006 Myceligenerans crystallogenes sp. nov., isolated from Roman catacombs. International Journal of Systematic and Evolutionary Microbiology, 56: 283-287.
30. Groth I., Tan G. Y. G., Gonzalez J. M., Laiz L., Carlsohn M. R., Schütze B., Wink J. & Goodfellow M., 2007 Amycolatopsis nigrescens sp. nov., an actinomycete isolated from a Roman catacomb. International Journal of Systematic and Evolutionary Microbiology, 57: 513-519.
31. Hernandez-Marine M, & Canals T., 1994 Herpyzonema pulverulentum (Mastigocladaceae) a new cavernicolous atmophytic and lime-incrusted cyanophyte. Algological Studies, 75: 123-136.
32. Herold K., Gollmick F. A., Groth I., Roth M., Menzel K-D., Möllmann U., Gräfe U. & Hertweck C., 2005 Cervimycin A-D: A polyketide glycoside complex from a cave bacterium can defeat vancomycin resistance. Chemistry, A European Journal, 11: 5523-5530.
33. Hoog G. S. de, Guarro J., Gene J. & Figueras M. J., 2000 Atlas of Clinical Fungi. Centraalbureau voor Schimmelcultures, Baarn, 1126 p.
34. Iida S., Taniguchi H., Kageyama A., Yazawa K., Chibana H., Murata S., Nomura F., Kroppenstedt R.M. & Mikami Y., 2005 Gordonia otitidis sp. nov., isolated from a patient with external otitis. International Journal of Systematic and Evolutionary Microbiology, 55: 1871-1876.
35. Johnson B., Bacelar-Nicolau P., Okibe N., Thomas A. & Hallberg K.B., 2009 Ferrimicrobium acidiphilum gen. nov., sp. nov. and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic, iron-oxidizing, extremely acidophilic actinobacteria. International Journal of Systematic and Evolutionary Microbiology, 59: 1082-1089.
36. Jülg B., Elias J., Zahn A., Köppen S., Becker-Gaab C., Bogner J.R., 2008. Bat-associated histoplasmosis can be transmitted at entrances of bat caves and not only inside the caves. Journal of Travel Medicine, 15: 133-136.
37. Jurado V., Groth I., Gonzalez J. M., Laiz L. & Saiz- Jimenez C., 2005a Agromyces salentinus sp. nov. and A. neoliticus sp. nov. International Journal of Systematic and Evolutionary Microbiology, 55: 153-157.
38. Jurado V., Groth I., Gonzalez J. M., Laiz L., Schuetze B. & Saiz-Jimenez C., 2005b Agromyces italicus sp. nov., Agromyces humatus sp. nov. and Agromyces lapidis sp. nov., isolated from Roman catacombs. International Journal of Systematic and Evolutionary Microbiology, 55: 871-875.
39. Jurado V., Groth I., Gonzalez J. M., Laiz L. & Saiz-Jimenez C., 2005c Agromyces subbeticus sp. nov., isolated from a cave in southern Spain. International Journal of Systematic and Evolutionary Microbiology, 55: 1897-1901.
40. 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.
41. Jurado V., Boiron P., Kroppenstedt R. M., Laurent F., Couble A., Laiz L., Klenk H.P., Gonzalez 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 Systematic and Evolutionary Microbiology, 58: 2210-2214.
42. 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.
43. Kajihiro E.S., 1965 Occurrence of dermatophytes in fresh bat guano. Applied Microbiology, 13: 720-725.
44. La Scola B., Mallet M-N., Patrick A. D. Grimont P.A.D. & Raoult D, 2002 Description of Afipia birgiae sp. nov. and Afipia massiliensis sp. nov. and recognition of Afipia felis genospecies A. International Journal of Systematic and Evolutionary Microbiology, 52: 1773-1782.
45. Lavoie K.H. & Northup D.E., 2006 Bacteria as indicators of human impact in caves. In: Proceedings of the 17th National Cave and Karst Management Symposium, October 31 to November 4, 2005, Albany, New York. The NCKMS Steering Committee, pp. 40-47.
46. Lee S. D., 2006a Amycolatopsis jejuensis sp. nov., and Amycolatopsis halotolerans sp. nov., novel actinomycetes isolated from a natural cave. International Journal of Systematic and Evolutionary Microbiology, 56: 549-553.
47. Lee S. D., 2006b Nocardia jejuensis sp. nov., a novel actinomycete isolated from a natural cave on Jeju Island, Republic of Korea. International Journal of Systematic and Evolutionary Microbiology, 56: 559-562.
48. Lee S. D., 2006c Actinocorallia cavernae sp. nov., isolated from a natural cave on Jeju, Korea. International Journal of Systematic and Evolutionary Microbiology, 56: 1085-1088.
49. Lee S. D., 2008 Jiangella alkaliphila sp. nov., an actinobacterium isolated from a cave. International Journal of Systematic and Evolutionary Microbiology, 58: 1176-1179.
50. Lee S. D., Kang S. O. & Hah Y. C., 2000a Hongia gen. nov., a new genus of the order Actinomycetales. International Journal of Systematic and Evolutionary Microbiology, 50: 191-199.
51. Lee S. D., Kang S. O. & Hah Y. C., 2000b Catellatospora koreensis sp. nov., a novel actinomycete isolated from a gold-mine cave. International Journal of Systematic and Evolutionary Microbiology, 50: 1103-1111.
52. Lee S. D., Kim E. S., Roe J. H., Jim J., Kang S.O. & Hah Y. C., 2000c Saccharothrix violacea sp. nov., isolated from a gold mine cave, and Saccharothrix albidocapillata comb. nov. International Journal of Systematic and Evolutionary Microbiology, 50: 1315-1323.
53. Lee S. D., Kim E. S., Min K. L., Lee W. Y., Kang S. O. & Hah Y. C., 2001. Pseudonocardia kongjuensis sp. nov., isolated from a gold mine cave. International Journal of Systematic and Evolutionary Microbiology, 51: 1505-1510.
54. Lee S. D., Kim E. S., Kang S. O. & Hah Y. C., 2002 Pseudonocardia spinosispora sp. nov., isolated from Korean soil. International Journal of Systematic and Evolutionary Microbiology, 52: 1603-1608.
55. Lee M., Kim M. K., Kwon M. J., Park B. D., Kim M. H., Goodfellow M. & Lee S. T., 2005 Effect of the synthesized mycolic acid on the biodegradation of diesel oil by Gordonia nitida strain LE31. Journal of Bioscience and Bioengineering, 100: 429-436.
56. Lemriss S., Laurent F., Couble A., Casoli E., Lancelin J.M., Saintpierre-Bonaccio D., Rifai S., Fassouane A. & Boiron P., 2003 Screening of nonpolyenic antifungal metabolites produced by clinical isolates of actinomycetes. Canadian Journal of Microbiology, 49: 669-674.
57. Luong M-L., Békal S., Vinh D.C., Lauzon D., Leung V., Al-Rawahi G.N., N. B. Burdz & Bernard K., 2008. First report of isolation and characterization of Aurantimonas altamirensis from clinical samples. Journal of Clinical Microbiology, 46: 2435-2437.
58. Margesin R., Schumann P., Spröer C. & Gounot A.-M., 2004 Arthrobacter psychrophenolicus sp. nov., isolated from an alpine ice cave. International Journal of Systematic and Evolutionary Microbiology, 54: 2067-2072.
59. Mendes R.E., Denys G.A., Fritsche T.R. & Jones N.R., 2009 Case report of Aurantimonas altamirensis bloodstream infection. Journal of Clinical Microbiolology, 47: 514-515.
60. Mignard S. & Flandrois J. P., 2008 A seven-gene, multilocus, genus-wide approach to the phylogeny of mycobacteria using supertrees. International Journal of Systematic and Evolutionary Microbiology, 58: 1432-1441.
61. Mortimer R.B., 2005 Leptospirosis in a caver returned from Sarawak, Malaysia. Wilderness and Environmental Medicine. 16: 129-131.
62. Nasher M. A., Hay R. J., Mahgoub E. S. & Gumaa S. A., 1989 In vitro studies of antibiotic sensitivities of Streptomyces somaliensis--a cause of human actinomycetoma. Transactions of the Royal Society of Tropical Medicine and Hygiene, 83: 265-268.
63. Nieves-Rivera A. M., Santos-Flores C. J., Dugan F. M. & Miller T. E., 2009 Guanophilic fungi in three caves of southwestern Puerto Rico. International Journal of Speleology, 38: 61-70.
64. Northup D.E. & Lavoie K.H., 2001 Geomicrobiology of caves: A review. Geomicrobiology Journal, 18: 199-222.
65. Nováková A., 2009 Microscopic fungi isolated from the Domica Cave system (Slovak Karst National Park, Slovakia). A review. International Journal of Speleology, 38: 71-82.
66. Osborne J.C., Rupprecht C.E., Olson J.G., Ksiazek T.G., Rollin P.E., Niezgoda M., Goldsmith C.S., An U.S. & Nichol S.T., 2003 Isolation of Kaeng Khoi virus from dead Chaerephon plicata bats in Cambodia. Journal of General Virology, 84: 2685-2689.
67. Paasche S.R., 2009 Rhodococcus equi infection in a surgical wound. Clinical Laboratory Science, 22:141-145.
68. Porter J. N., 1971 Prevalence and distribution of antibiotic-producing actinomycetes. Advances in Applied Microbiology, 14: 73-92.
69. Porter M. L., Engel A. S., Kane T. C. & Kinkle B. K., 2009 Productivity-diversity relationships from chemolithoautotrophically based sulfidic karst systems. International Journal of Speleology, 38: 27-40.
70. Regnier S., Ouagari Z., Perez Z.L., Veziris N., Bricaire F. & Caumes E., 2009 Cutaneous miliary resistant tuberculosis in a patient infected with human immunodeficiency virus: case report and literature review. Clinical and Experimental Dermatology, 34: e690-e692.
71. Reinert R.R., Schnitzler N., Haase G., Lütticken R., Fabry U., Schaal K.P., & Funke G., 1995 Recurrent bacteremia due to Brevibacterium casei in an immunocompromised patient. European Journal of Clinical Microbiology & Infectious Diseases, 14: 1082-1085.
72. Rodríguez-Nava V., Laurent F., Couble A. & Boiron P., 2007 Identification phénotypique et moléculaire des bactéries appartenant au genre Nocardia. Revue Francophone des Laboratoires, 391: 49-56.
73. Rodríguez-Nava V., Zoropoguy A., Laurent F., Blaha D., Couble A., Mouniée D., & Boiron P., 2008 La nocardiose, une maladie en expansion. Antibiotiques, 10: 115-127.
74. Salar A., Carratalà J., Fernández-Sevilla A., Marín D., & Grañena A., 1997 Pneumonia caused by Micrococcus species in a neutropenic patient with acute leukemia. European Journal of Clinical Microbiology & Infectious Diseases, 16: 546-548.
75. Schabereiter-Gurtner C., Saiz-Jimenez C., Piñar G., Lubitz W. & Rölleke C., 2002a Altamira cave Paleolithic paintings harbor partly unknown bacterial communities. FEMS Microbiology Letter, 211: 7-11.
76. Schabereiter-Gurtner C., Saiz-Jimenez C., Piñar G., Lubitz, W. & Rölleke C., 2002b Phylogenetic 16S rRNA analysis reveals the presence of complex and partly unknown bacterial communities in Tito Bustillo cave, Spain, and on its Palaeolithic paintings. Environmental Microbiology, 4: 392-400.
77. Schmoldt S., Latzin P., Heesemann J., Griese M., Imhof A. & Hogardt M., 2006 Clonal analysis of Inquilinus limosus isolates from six cystic fibrosis patients and specific serum antibody response. Journal of Medical Microbiology, 55: 1425-1433.
78. Seo J. P., Yun Y.-W. & Lee S. D., 2007 Nocardia speluncae sp. nov., isolated from a cave. International Journal of Systematic and Evolutionary Microbiology, 57: 2932-2935.
79. Skoulidis F., Morgan M. S. & MacLeod K. M., 2004 Penicillium marneffei: a pathogen on our doorstep? Journal of the Royal Society of Medicine, 97: 394-395.
80. Sohn K., Hong S. G., Bae S. K. & Chun J., 2003 Transfer of Hongia koreensis Lee et al. 2000 to the genus Kribbella Park et al. 1999 as Kribbella koreensis comb. nov. International Journal of Systematic and Evolutionary Microbiology, 53: 1005-1007.
81. Sugita T., Kikuchi K., Makimura K., Urata K., Someya T., Kamei K., Niimi M. & Uehara Y., 2005 Trichosporon species isolated from guano samples obtained from bat-inhabited caves in Japan. Applied Environmental Microbiology, 71: 7626-7629.
82. Stomeo F., 2008. Análisis de comunidades microbianas presentes en la cueva de Doña Trinidad (Ardales, Málaga) utilizando cultivos y métodos moleculares basados en ADN y ARN. Ph D Thesis. University of Seville, Spain.
83. Timen A., Koopmans M.P.G., Vossen A.C.T.M., van Doornum G.J.J., Günther S., van der Berkmortel F., Verduin K.M., Dittrich S., Emmerich P., Osterhaus A.D.M.E., van Dissel J.T. & Coutinho R.A., 2009. Response to imported case of Marburg hemorrhagic fever, the Netherlands. Emerging Infectious Diseases, 15: 1171-1175.
84. Towner, J.S., Amman, B.R., Sealy, T.K. et al., 2009 Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PloS Pathogens, 5: e1000536. doi:10.1371/journal.ppat.1000536.
85. Urzì C., De Leo F. & Schumann P., 2008 Kribbella catacumbae sp. nov., and Kribbella sancticallisti sp. nov., isolated from whitish-grey patinas in the catacombs of St Callistus in Rome, Italy. International Journal of Systematic and Evolutionary Microbiology, 58: 2090-2097.
86. Vaughan-Martini A., Angelini P. & Zacchi L., 2000 The influence of human and animal visitation on the yeast ecology of three Italian caverns. Annals of Microbiology, 50: 133-140.
87. Vernazza P.L., Bodmer T. & Galeazzi R.L., 1991- Rhodococcus erythropolis infection in HIV-associated immunodeficiency. Schweizerische Medizinische Wochenschrift, 121: 1095-1098.
88. Wang Z.-G., Wang Y.-Z., Liu J.-H., Chen Y.-G., Zhang X.-X., Wen M.-L., Xu L.-H., Peng Q. & Cui X.-L., 2009 Fodinibacter luteus gen. nov., sp. nov., an actinobacterium isolated from a salt mine. International Journal of Systematic and Evolutionary Microbiology, 59: 2185-2190.
89. Watve M.G., Tickoo R., Jog M.M. & Bhole B.D., 2001 How many antibiotics are produced by the genus Streptomyces? Archives of Microbiology, 176: 386-309.
90. Williams S. T., Locci R., Beswick A. et al., 1993 Detection and identification of novel actinomycetes. Research in Microbiology, 144:653-656.
91. Yang L.-L., Tang S.-K., Zhang Y.-Q., Zhi X.-Y., Wang D., Xu L.-H. & Li W.-J., 2008 Thermobifida halotolerans sp. nov., isolated from a salt mine sample, and emended description of the genus Thermobifida. International Journal of Systematic and Evolutionary Microbiology, 58: 1821-1825.