Advertisement

Environmental Science and Pollution Research

, Volume 21, Issue 1, pp 473–484 | Cite as

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

  • E. Garcia-Anton
  • S. Cuezva
  • V. Jurado
  • E. Porca
  • A. Z. Miller
  • A. Fernandez-Cortes
  • C. Saiz-JimenezEmail author
  • S. Sanchez-Moral
Research Article

Abstract

Altamira Cave (north of Spain) contains one of the world's most prominent Paleolithic rock art paintings, which are threatened by a massive microbial colonization of ceiling and walls. Previous studies revealed that exchange rates between the cave and the external atmosphere through the entrance door play a decisive role in the entry and transport of microorganisms (bacteria and fungi) and nutrients to the interior of the cave. A spatial-distributed sampling and measurement of carrier (CO2) and trace (CH4) gases and isotopic signal of CO213C) inside the cave supports the existence of a second connection (active gas exchange processes) with the external atmosphere at or near the Well Hall, the innermost and deepest area of the cave. A parallel aerobiological study also showed that, in addition to the entrance door, there is another connection with the external atmosphere, which favors the transport and increases microorganism concentrations in the Well Hall. This double approach provides a more complete knowledge on cave ventilation and revealed the existence of unknown passageways in the cave, a fact that should be taken into account in future cave management.

Keywords

Caves Gases Bacteria Fungi Cave management 

Notes

Acknowledgments

This research was supported by the Spanish Ministry of Sciences and Innovation, project CGL2010-17108/BTE. EG-A is supported by a CSIC JAE-Predoctoral grant. SC benefits of a postdoctoral fellowship from the Spanish Ministry of Science and Innovation, research programme Juan de la Cierva. AF-C was funded by a postdoctoral fellowship the JAE-Doc Program (CSIC). AZM was supported by FCT grant SFRH/BPD/63836/2009. Altamira Cave Research Centre and Museum staffs are acknowledged for their collaboration throughout the research period. This is a TCP-CSD 2007–00058 paper.

References

  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 51:293–304CrossRefGoogle Scholar
  2. Ballero M, Piu G, Ariu A (2000) The impact of the botanical gardens on the aeroplankton of the city of Cagliari, Italy. Aerobiologia 16:143–147CrossRefGoogle Scholar
  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 55:274–280CrossRefGoogle Scholar
  4. Brooke JS (2012) Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 25:2–41CrossRefGoogle Scholar
  5. Che F (2004) The principle and application of airborne microbiology. Science Press, Beijing, pp 1–41Google Scholar
  6. Cooley JD, Wong WC, Jumper CA, Straus DC (1998) Correlation between the prevalence of certain fungi and sick building syndrome. Occup Environ Med 55:579–584CrossRefGoogle Scholar
  7. Crosson ER (2008) A cavity ring-down analyzer for measuring atmospheric levels of methane, carbon dioxide, and water vapor. Appl Physics B 92:403–408CrossRefGoogle Scholar
  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 38:83–92CrossRefGoogle Scholar
  9. Cuezva S, Fernandez-Cortes A, Benavente D, Serrano-Ortiz P, Kowalski AS, Sanchez-Moral S (2011) Short-term CO2(g) exchange between a shallow karstic cavity and the external atmosphere during summer: role of the surface soil layer. Atmos Environ 45:1418–1427CrossRefGoogle Scholar
  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 409:835–843CrossRefGoogle Scholar
  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 63:23–41CrossRefGoogle Scholar
  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 17:7843–7853CrossRefGoogle Scholar
  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 118:122–134CrossRefGoogle Scholar
  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 18:1037–1045CrossRefGoogle Scholar
  15. Flannigan B, Samson RA, Miller JD (2001) Microorganisms in home and indoor work environments: diversity, health impacts, investigation and control. Taylor and Francis, LondonCrossRefGoogle Scholar
  16. Garcia-Anton E, Cuezva S, Fernandez-Cortes A, Sanchez-Moral S, Benavente D (2012) Daily variations of CO2, δ13CO2 and CH4 of cave air controlled by external weather conditions: example of rapid survey in Altamira cave (north of Spain). Geophys Res Abstracts 14:4859–4862Google Scholar
  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 30:217–218CrossRefGoogle Scholar
  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.Google Scholar
  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 39:15–24CrossRefGoogle Scholar
  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 408:3632–3638CrossRefGoogle Scholar
  21. Keeling CD (1958) The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas. Geochim Cosmochim Acta 13:322–334CrossRefGoogle Scholar
  22. King AD, Hocking AD, Pitt JI (1979) Dichloran-rose bengal medium for enumeration and isolation of molds from foods. App Environ Microbiol 37:959–964Google Scholar
  23. Kubicek CP, Komon-Zelazowska M, Druzhinina IS (2008) Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J Zhejiang Univ Sci B 9:753–763CrossRefGoogle Scholar
  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 46:2435–2437CrossRefGoogle Scholar
  25. Mendes RE, Denys GA, Fritsche TR, Jones NR (2009) Case report of Aurantimonas altamirensis bloodstream infection. J Clin Microbiol 47:514–515CrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  27. Porca E (2011) Aerobiología: mecanismos de dispersión de los microorganismos en cuevas turísticas. Ph.D. Thesis, University of Seville.Google Scholar
  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 11:1594–1598CrossRefGoogle Scholar
  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 334:42–43CrossRefGoogle Scholar
  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 16:546–548CrossRefGoogle Scholar
  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 469–474CrossRefGoogle Scholar
  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 211:7–11CrossRefGoogle Scholar
  33. Spieksma FTHM (1995) Outdoor atmospheric mould spores in Europe. XVIth European Congress of Allergology and Clinical Immunology. Monduzzi, Bologna, pp 625–630Google Scholar
  34. Stenfors LP, Mayr R, Scherer S, Granum PE (2002) Pathogenic potential of fifty Bacillus weihenstephanensis strains. FEMS Microbiol Lett 215:47–51CrossRefGoogle Scholar
  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 59:1126–1129CrossRefGoogle Scholar
  36. Usó J, Gil M, Gomila B, Tirado MD (2003) Endocarditis by Micrococcus luteus (in Spanish). Enferm Infec Microbiol Clin 21:116–120CrossRefGoogle Scholar
  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 15:711–713CrossRefGoogle Scholar
  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 315–322CrossRefGoogle Scholar
  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 17:278–282CrossRefGoogle Scholar
  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 22:379–388CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • E. Garcia-Anton
    • 1
  • S. Cuezva
    • 2
  • V. Jurado
    • 3
  • E. Porca
    • 3
  • A. Z. Miller
    • 4
  • A. Fernandez-Cortes
    • 1
  • C. Saiz-Jimenez
    • 3
    Email author
  • S. Sanchez-Moral
    • 1
  1. 1.Museo Nacional de Ciencias Naturales, MNCN-CSICMadridSpain
  2. 2.Laboratorio de Petrología AplicadaUniversidad de AlicanteAlicanteSpain
  3. 3.Instituto de Recursos Naturales y Agrobiologia, IRNAS-CSICSevillaSpain
  4. 4.Instituto Superior TecnicoLisbonPortugal

Personalised recommendations