Combining stable isotope (δ13C) of trace gases and aerobiological data to monitor the entry and dispersion of microorganisms in caves

Environmental Science and Pollution Research

Volumn 21, Issue 1, 2014, Pages 473-484

  Garcia Anton, E ^a   Cuezva, S ^b   Jurado, V ^c   Porca, E ^c   Miller, A Z ^d   Fernandez Cortes, A ^a   Saiz Jimenez, C ^c   Sanchez Moral, S ^a  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b UNIVERSITY OF ALICANTE   (Spain)

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

^d INSTITUTO SUPERIOR TÉCNICO   (Portugal)

Author keywords

Bacteria; Cave management; Caves; Fungi; Gases

Indexed keywords

ATMOSPHERIC TRANSPORT; BACTERIUM; BIOMONITORING; CARBON DIOXIDE; CARBON ISOTOPE; CAVE; CONCENTRATION (COMPOSITION); DATA SET; DISPERSION; FUNGUS; GAS EXCHANGE; METHANE; MICROORGANISM; PALEOLITHIC; STABLE ISOTOPE; TRACE GAS;

BACTERIA (MICROORGANISMS); FUNGI;

CARBON;

ARTICLE; BACTERIUM; CAVE; ENVIRONMENTAL MONITORING; FUNGUS; GAS; GROWTH, DEVELOPMENT AND AGING; METHODOLOGY; MICROBIOLOGY; PHYSIOLOGY; SPAIN;

BACTERIA; CARBON ISOTOPES; CAVES; ENVIRONMENTAL MONITORING; FUNGI; GASES; SPAIN;

EID: 84891627081     PISSN: 09441344     EISSN: 16147499     Source Type: Journal    
DOI: 10.1007/s11356-013-1915-3     Document Type: Article

References (40)

1. Aira MJ, Rodríguez-Rajo F-J, Fernández-González M, Seijo C, Elvira-Rendueles B, Gutiérrez-Bustillo M, Abreu I, Pérez-Sánchez E, Oliveira M, Recio M, Morales J, Muñoz-Rodríguez A-F (2012) Cladosporium airborne spore incidence in the environmental quality of the Iberian Peninsula. Grana 51: 293-304.
2. Ballero M, Piu G, Ariu A (2000) The impact of the botanical gardens on the aeroplankton of the city of Cagliari, Italy. Aerobiologia 16: 143-147.
3. Bisht V, Singh BP, Arora N, Sridhara S, Gaur SN (2008) Allergens of Epicoccum nigrum grown in different media for quality source material. Allergy 55: 274-280.
4. Brooke JS (2012) Stenotrophomonas maltophilia: An emerging global opportunistic pathogen. Clin Microbiol Rev 25: 2-41.
5. Che F (2004) The principle and application of airborne microbiology. Science Press, Beijing, pp 1-41.
6. Cooley JD, Wong WC, Jumper CA, Straus DC (1998) Correlation between the prevalence of certain fungi and sick building syndrome. Occup Environ Med 55: 579-584.
7. Crosson ER (2008) A cavity ring-down analyzer for measuring atmospheric levels of methane, carbon dioxide, and water vapor. Appl Physics B 92: 403-408.
8. Cuezva S, Sanchez-Moral S, Saiz-Jimenez C, Cañaveras JC (2009) Microbial communities and associated mineral fabrics in Altamira Cave, Spain. Community structure in oligotrophic cave environments. Int J Speleol 38: 83-92.
9. 2(g) exchange between a shallow karstic cavity and the external atmosphere during summer: role of the surface soil layer. Atmos Environ 45: 1418-1427.
10. Docampo S, Trigo MM, Recio M, Melgar M, García-Sánchez J, Cabezudo B (2011) Fungal spore content of the atmosphere of the Cave of Nerja (southern Spain): diversity and origin. Sci Total Environ 409: 835-843.
11. Dredge J, Fairchild IJ, Harrison RM, Fernandez-Cortes A, Sanchez-Moral S, Jurado V, Gunn J, Smith A, Spotl C, Mattey D, Wynn PM, Grassineau N (2013) Cave aerosols: distribution and contribution to speleothem geochemistry. Quat Sci Rev 63: 23-41.
12. Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17: 7843-7853.
13. Elez J, Cuezva S, Fernandez-Cortes A, Garcia-Anton E, Benavante D, Cañaveras JC, Sanchez-Moral S (2013) A GIS based methodology to quantitatively define an adjacent protected area in a shallow karst cavity: the case of Altamira cave. J Environ Manage 118: 122-134.
14. Fernandez-Cortes A, Cuezva S, Sanchez-Moral S, Porca E, Jurado V, Martin-Sanchez PM, Saiz-Jimenez C (2011) Detection of human-induced environmental disturbances in a show cave. Environ Sci Poll Res 18: 1037-1045.
15. Flannigan B, Samson RA, Miller JD (2001) Microorganisms in home and indoor work environments: diversity, health impacts, investigation and control. Taylor and Francis, London.
16. 4 of cave air controlled by external weather conditions: example of rapid survey in Altamira cave (north of Spain). Geophys Res Abstracts 14: 4859-4862.
17. García-Lozano T, Aznar Oroval E, Juan Bañón JL (2012) First isolation in Spain of Aurantimonas altamirensis in a blood culture from a port-a-cath in a patient with Bence-Jones type multiple myeloma (in Spanish). Enferm Infec Microbiol Clin 30: 217-218.
18. Hoog GS de, Guarro J, Gené J, Figueras MJ (2000) Atlas of Clinical Fungi, 2nd edn. CBS, Utrecht and Universitat Rovira i Virgili, Reus.
19. Jurado V, Laiz L, Rodriguez-Nava V, Boiron P, Hermosin B, Sanchez-Moral S, Saiz-Jimenez C (2010a) Pathogenic and opportunistic microorganisms in caves. Int J Speleol 39: 15-24.
20. Jurado V, Porca E, Cuezva S, Fernandez-Cortes A, Sanchez-Moral S, Saiz-Jimenez C (2010b) Fungal outbreak in a show cave. Sci Total Environ 408: 3632-3638.
21. Keeling CD (1958) The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas. Geochim Cosmochim Acta 13: 322-334.
22. King AD, Hocking AD, Pitt JI (1979) Dichloran-rose bengal medium for enumeration and isolation of molds from foods. App Environ Microbiol 37: 959-964.
23. Kubicek CP, Komon-Zelazowska M, Druzhinina IS (2008) Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J Zhejiang Univ Sci B 9: 753-763.
24. Luong M-L, Békal S, Vinh DC, Lauzon D, Leung V, Al-Rawahi GN, Ng B, Burdz T, Bernard K (2008) First report of isolation and characterization of Aurantimonas altamirensis from clinical samples. J Clin Microbiol 46: 2435-2437.
25. Mendes RE, Denys GA, Fritsche TR, Jones NR (2009) Case report of Aurantimonas altamirensis bloodstream infection. J Clin Microbiol 47: 514-515.
26. Pataki DE, Ehleringer JR, Flanagan LB, Yakir D, Bowling DR, Still CJ, Buchmann N, Kaplan JO, Berry JA (2003) The application and interpretation of Keeling plots in terrestrial carbon cycle research. Glob Biogeochem Cycle 17: 1022. doi: 10. 1029/2001GB001850.
27. Porca E (2011) Aerobiología: Mecanismos de dispersión de los microorganismos en cuevas turísticas. Ph. D. Thesis, University of Seville.
28. Porca E, Jurado V, Martin-Sanchez PM, Hermosin 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.
29. Saiz-Jimenez C, Cuezva S, Jurado V, Fernandez-Cortes A, Porca E, Benavente D, Cañaveras JC, Sanchez-Moral S (2011) Paleolithic art in peril: policy and science collide at Altamira Cave. Science 334: 42-43.
30. Salar A, Carratalà J, Fernández-Sevilla A, Marín D, Grañena A (1997) Pneumonia caused by Micrococcus species in a neutropenic patient with acute leukemia. Eur J Clin Microbiol Infect Dis 16: 546-548.
31. Sanchez-Moral S, Cuezva S, Fernández-Cortés A, Benavente D, Cañaveras JC (2010) Effect of ventilation on karst system equilibrium (Altamira Cave, N Spain): An appraisal of karst contribution to the global carbon cycle balance. In: Andreo B, Carrasco F, Duran JJ, LaMoreaux JW (eds) Advances in research in karst media. Springer, Berlin, pp 469-474.
32. Schabereiter-Gurtner C, Saiz-Jimenez C, Piñar G, Lubitz W, Rolleke S (2002) Altamira Cave paleolithic paintings harbour partly unknown bacterial communities. FEMS Microbiol Lett 211: 7-11.
33. Spieksma FTHM (1995) Outdoor atmospheric mould spores in Europe. XVIth European Congress of Allergology and Clinical Immunology. Monduzzi, Bologna, pp 625-630.
34. Stenfors LP, Mayr R, Scherer S, Granum PE (2002) Pathogenic potential of fifty Bacillus weihenstephanensis strains. FEMS Microbiol Lett 215: 47-51.
35. Téllez-Castillo CJ, González Granda D, Bosch Alepuz M, Jurado Lobo V, Saiz-Jimenez C, Juan JL, Millán Oria J (2010) Isolation of Aurantimonas altamirensis from pleural effusions. J Med Microbiol 59: 1126-1129.
36. Usó J, Gil M, Gomila B, Tirado MD (2003) Endocarditis by Micrococcus luteus (in Spanish). Enferm Infec Microbiol Clin 21: 116-120.
37. von Eiff C, Kuhn N, Herrmann M, Weber S, Peters G (1996) Micrococcus luteus as a cause of recurrent bacteremia. Pediatr Infect Dis J 15: 711-713.
38. 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.
39. Yoshino Y, Kitazawa T, Kamimura M, Tatsuno K, Ota Y, Yotsuyanagi H (2011) Pseudomonas putida bacteremia in adult patients: five case reports and a review of the literature. J Infect Chemother 17: 278-282.
40. Zimmermann J, Gonzalez JM, Ludwig W, Saiz-Jimenez C (2005) Detection and phylogenetic relationships of a highly diverse uncultured acidobacterial community on paleolithic paintings in Altamira Cave using 23S rRNA sequence analyses. Geomicrobiol J 22: 379-388.