Pathogenic and opportunistic microorganisms in caves

International Journal of Speleology 39 (1) 15-24 Bologna (Italy) January 2010 Available online at www.ijs.speleo.it International Journal of Speleology Official Journal of Union Internationale de Spéléologie Pathogenic and opportunistic microorganisms in caves Valme Jurado, Leonila Laiz, Veronica Rodriguez-Nava1, Patrick Boiron1, Bernardo Hermosin, Sergio Sanchez-Moral2, Cesareo Saiz-Jimenez Abstract: Jurado V., Laiz L., Rodriguez-Nava V., Boiron P., Hermosin H., Sanchez-Moral S. and Saiz-Jimenez C. 2010. Pathogenic and opportunistic microorganisms in caves. International Journal of Speleology, 39 (1), 15-24. Bologna (Italy). ISSN 0392-6672. With today’s leisure tourism, the frequency of visits to many caves makes it necessary to know about possible potentially pathogenic microorganisms in caves, determine their reservoirs, and inform the public about the consequences of such visits. Our data reveal that caves could be a potential danger to visitors because of the presence of opportunistic microorganisms, whose existence and possible development in humans is currently unknown. Keywords: Caves, bacteria, fungi, virus, opportunistic pathogens Received 26 Oktober 2009; Revised 28 November 2009; Accepted 9 December 2009. INTRODUCTION Europe is an exceptional continent for its abundance and variety of subterranean karstic forms comprising the natural geological heritage. Many of them are Protected Sites, and today many countries have programmes for the protection of caves and geodiversity. Some caves can be visited, and are, either ecologically or culturally, a tourist attraction. Today, many caves have been invaded by, and are important centres of, mass tourism. Nevertheless, while certain caves have around 500,000 visits annually (Grotta del Vento, Italy; Postojna caves, Slovenia; Nerja, Spain), others are difficult to get to, and are visited only by speleologists (Calaforra Chordi & Berrocal Pérez, 2008). With today’s leisure tourism, the frequency of visits to many caves makes it necessary to know about possible potentially pathogenic microorganisms in caves, determine their reservoirs, and inform the public about the consequences of such visits for people who are immunosuppressed, undergoing chemotherapy, 1 Research Group on «Bacterial Opportunistic Pathogens and Environment», CNRS, Faculté de Pharmacie, Université de Lyon 1, UMR 5557 Ecologie Microbienne, 8, avenue Rockefeller, 69373, France 2 Museo Nacional de Ciencias Naturales, CSIC, Jose Gutierrez Abascal 2, 28006 Madrid, Spain Instituto de Recursos Naturales y Agrobiologia, CSIC, Avenida Reina Mercedes 10, 41012 Sevilla, Spain or have lowered defences. Unfortunately, information on this topic is not well known, and visitors remain unaware. Determining the extent of the potential danger is of great interest ― not only scientific, but also medical and social. Our data reveal that caves could be a potential danger to visitors, because of the presence of opportunistic microorganisms, whose existence and possible development in humans is currently unknown. CAVE MICROORGANISMS Microorganisms occupy all the niches of the biosphere, including subterranean ones. Underground habitats, represented essentially by caves, have no light, little or no organic nutrient load, a relatively constant temperature, and extensive areas of mineral surfaces. The literature on microbial communities in subterranean environments is scant and chiefly restricted to caves found in Spain, Italy, France, Rumania, and the USA. Most of the existing literature refers to specific aspects, such as the taxonomic or geomicrobiological ones (Hernandez-Marine & Canals, 1994; Northup & Lavoie, 2001; Engel et al., 2003; Barton, & Northup, 2007; Barton et al., 2007; Porter et al. 2009), to the effects on rock-art paintings (Schabereiter-Gurtner et al., 2002 a, b), or colonization by fungi (Dupont et al., 2007; Bastian et al., 2009b). A review on the biodiversity and distribution of V. Jurado et al 16 bacteria in subterranean environments reveals the scant knowledge of these topics. Proteobacteria represent the major portion of bacteria in caves when using molecular tools, but Actinobacteria constitute the majority of isolates (Groth et al., 1999; Barton et al. 2007), although it was formerly believed they were confined mainly to soils, their natural habitat (Porter, 1971; Goodfellow & Williams, 1983). In the last decade, actinobacteria have been shown to be abundant in caves (Groth et al., 1999; Schabereiter-Gurtner et al., 2002 a,b; Jurado et al., 2005 a,c), suggesting that this is a habitat particularly favourable for this group of bacteria (Figure 1). Table 1 shows the new species of actinobacteria isolated from subterranean environments reported since 2000, as gathered in the International Journal of Systematic and Evolutionary Microbiology. The identification of new species of the genera Agromyces, Amycolatopsis, and Kribbella (Figure 2) indicates that these environments constitute an ecological niche with a solid potential for the study of biodiversity. The conditions of high salinity in certain niches, and the stability of the microbial communities over the years, make these habitats of great interest and a target for in-depth study, to obtain an understanding not only of the processes forming natural microbial communities and of their role in the interaction with minerals, but Fig. 1. Pseudonocardia sp. colonies in stalactites (Doña Trinidad Cave, Ardales, Spain). also of the biodiversity of such ecosystems. At the same time, the ecological study of environments other than terrestrial and marine ones is important because of the potential of actinobacteria as producers of new bioactive substances derived from their secondary metabolism. In fact, the actinobacteria are an important source of naturally occurring (non-synthetic) antibiotics, besides substances with antiviral, antitumoural, immunological, and agrobiological (herbicidal) activity. All of these compounds are of high commercial value (Lemriss et al., 2003). A mathematical model estimates the number of undiscovered antimicrobials from the genus Streptomyces to be of the order of a 100,000 – a tiny fraction of which has been unearthed so far (Watve et al., 2001). According to Williams et al. (1993), one possible way to tackle the isolation of new actinobacteria would be to focus on environments not studied or to investigate habitats in which one or various environmental factors (for example, temperature, pH, aeration, osmotic stress, etc.) are extreme. Accordingly, the exploration of caves and their exploitation as reservoirs of bacteria is of great interest to the pharmaceutical industry. Groth & Saiz-Jimenez (1999, 2002) pointed out the importance of caves as a new habitat in which actinobacteria producing bioactive substances could be found. Later, Herold et al. (2005) reported the production of cervimycin A-D by Streptomyces tendae, isolated from the Grotta dei Cervi (...truncated)