Abstract
The growing pollution mainly caused by the discharge of industrial, sanitary, and agricultural wastes has become one of the main current environmental issues. Thus, the use of bioindicators has become an important tool for investigating environmental imbalance. In this context, microorganisms have shown to be important for the identification of altered environments because of their ubiquity and their ability to grow in inhospitable habitats. Yeasts of the genus Candida are potential bioindicators because of their ability to survive in contaminated freshwater environments. Besides, they are more frequently recovered than fecal coliforms. It is noteworthy that the nonspecific activity of efflux pumps, which help in cellular detoxification processes, may be associated with the presence of chemical compounds in contaminated environments. Thus, the activity of efflux pumps may be the main mechanism involved in the resistance to azole derivatives in Candida spp. and the assessment of their activity may also be a tool for environmental monitoring. As a result, the phenotypical and molecular evaluation of this antifungal resistance in Candida species has been pointed as a promising tool for monitoring the quality of aquatic environments. Hence, the objective of this study was to collect and systematize data pointing to an alternative use of Candida spp. as bioindicators by assessing the occurrence of azole resistance among environmental Candida as a strategy to monitor the quality of freshwater environments.
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Alexander, N. J., McComick, S. P., & Hohn, T. M. (1999). TRI12, a trichothecene afflux pump from Fusarium sporotrichioides: gene isolation and expression in yeast. Molecular Genetics and Genomics, 261, 977–984.
Almeida, J. M. (2005). Yeast community survey in the Tagus estuary. FEMS Microbiology Ecology, 53(2), 295–303.
American Public Health Association (APHA), American Water Works Association (AWWA) and Water Environmental Federation (WEF). Standard methods for the examination of water and wastewater. 20. ed. Washington: APHA/ AWWA/ WEF, 1998.
Andrade, N. P. C., Filho, F. M., Carrera, M. V., Silva, L. J., Franco, I., & Costa, M. M. (2010). Bacterial microbiota of the Macrobrachium amazonicum from São Francisco river, Brazil. Acta Veterinaria Brasilica, 4(3), 176–180.
Arvanitidou, M., Kanellou, K., Katsouyannopoulos, V., & Tsakris, A. (2002). Occurrence and densities of fungi from northern Greek coastal bathing waters and their relation with faecal pollution indicators. Water Research, 36(20), 5127–5131.
Barus, V., Jarkovsky, J., & Prokes, M. (2007). Philometra ovata (Nematoda: Philometroidea): a potential sentinel species of heavy metal accumulation. Parasitology Research, 100, 929–933.
Beeby, A. (2001). What do sentinels stand for? Environmental Pollution, 112(2), 285–298.
Brandão, L. R., Duarte, M. C., Barbosa, A. C., & Rosa, C. A. (2010). Diversity and antifungal susceptibility of yeasts isolated by multiple-tube fermentation from three freshwater lakes in Brazil. Journal of Water and Health, 8(2), 279–289.
Brilhante, R. S. N., Paiva, M. A. N., Sampaio, C. M. S., Teixeira, C. E. C., Castelo-Branco, D. S. C. M., Leite, J. J. G., Moreira, C. A., Silva, L. P., Cordeiro, R. A., Monteiro, A. J., Sidrim, J. J. C., & Rocha, M. F. G. (2011). Yeasts from Macrobrachium amazonicum: a focus on antifungal susceptibility and virulence factors of Candida spp. FEMS Microbiology Ecology, 76(2), 268–277.
Brilhante, R. S. N., Castelo-Branco, D. S. C. M., Duarte, G. P. S., Paiva, M. A. N., Teixeira, C. E. C., Zeferino, J. P. O., Monteiro, A. J., Cordeiro, R. A., Sidrim, J. J. C., & Rocha, M. F. G. (2012). Yeast microbiota of raptors: a possible tool for environmental monitoring. Environmental Microbiology Reports, 4(2), 189–193.
Bruins, M. R., Kapil, S., & Oehme, F. W. (2000). Microbial resistance to metals in the environment. Ecotoxicology and Environmental Safety, 45(3), 198–207.
Buchberger, W. W. (2011). Current approaches to trace analysis of pharmaceuticals and personal care products in the environment. Journal of Chromatography A, 1218, 603–618.
Butinar, L., Santos, S., Spencer-Martins, I., Oren, A., & Gunde-Cimerman, N. (2005). Yeast diversity in hypersaline habitats. FEMS Microbiology Letters, 15(2), 229–234.
Cannon, R. D., Lamping, E., Holmes, A. R., Niimi, K., Baret, P. V., Keniya, M. V., Tanabe, K., Niimi, M., Goffeau, A., & Monk, B. C. (2009). Efflux-mediated antifungal drug resistance. Clinical Microbiology Reviews, 22(2), 291–321.
Castelo-Branco, D. S. C. M., Brilhante, R. S. N., Paiva, M. A. N., Teixeira, C. E. C., Caetano, E. P., Ribeiro, J. F., Cordeiro, R. A., Sidrim, J. J. C., Monteiro, A. J., & Rocha, M. F. G. (2013). Azole-resistant Candida albicans from a wild Brazilian porcupine (Coendou prehensilis): a sign of an environmental imbalance? Medical Mycology, 51(5), 555–560.
Chen, Y. S., Yanagida, F., & Chen, L. Y. (2009). Isolation of marine yeasts from coastal waters of northeastern Taiwan. Aquatic Biology, 8(55–60), 55–60.
Chiba, W. A. C., Passerini, M. D., & Tundisi, J. G. (2011). Metal contamination in benthic macroinvertebrates in a sub-basin in the southeast of Brazil. Brazilian Journal of Biology, 71(2), 391–399.
Chun, S. B. (1984). Ecological studies on Yeasts in the waters of the Yeong San River Estuary. Korean Journal of Microbiology, 22(1), 1–18.
Coelho, M. A., Almeida, J. M. F., Martins, I. M., Silva, A. J., & Sampaio, J. P. (2010). The dynamics of the yeast community of the Tagus river estuary: testing the hypothesis of the multiple origins of estuarine yeasts. Antonie van Leeuwenhoek, 98, 331–342.
Farag, S., & Soliman, N. A. (2011). Biodegradation of crude petroleum oil and environmental pollutants by Candida tropicalis strain. Brazilian Archives of Biology and Technology, 54(4), 821–830.
Feng, L., Wan, Z., Wang, X., Li, R., & Li, W. (2010). Relationship between antifungal resistance of fluconazole resistant. Strain, 123(5), 544–548.
Gadanho, M., & Sampaio, J. P. (2005). Occurrence and diversity of yeasts in the Mid-Atlantic ridge hydrothermal fields near the Azores archipelago. Microbial Ecology, 50(3), 408–417.
Gerba, C. P. (2009). Indicator microorganisms. In R. M. Maier, I. L. Pepper, & C. P. Gerba (Eds.), Environmental microbiology (pp. 485–499). San Diego, California: Elsevier.
Hacon, S. (2003). Avaliação e gestão do risco ecotoxicológico à saúde humana. In F. A. Azevedo & A. A. M. Chasin (Eds.), As bases toxicológicas da ecotoxicologia (pp. 245–322). São Carlos: RiMa.
Hagler, A. N. (2006). Yeast as indicators of environmental quality. In C. Rosa & P. Gábor (Eds.), Biodiversity and ecophysiology of yeasts (pp. 514–532). Berlin Heidelberg: Springer.
Hagler, A. N., Mendonça-Hagler, L. C., Rosa, C. A., & Morais, P. P. (1995). Yeast as an example of microbial diversity in Brazilian ecosystems. Oecologia Brasiliensis, 1, 225–244.
Hopkins, W. A. (2007). Amphibians as models for studying environmental change. ILAR Journal, 48(3), 270–277.
Jungwirth, H., & Kuchler, K. (2006). Yeast ABC transporters—a tale of sex, stress, drugs and aging. FEBS Letters, 580(4), 1131–1138.
Kanafani, Z. A., & Perfect, J. R. (2008). Resistance to antifungal agents: mechanisms and clinical impact. Clinical Infectious Diseases, 46(1), 120–128.
Keenan, P. O., Knight, A. W., Billinton, N., Cahill, P. A., Dalrymple, I. M., & Hawkyard, C. J. (2007). Clear and present danger? The use of a yeast biosensor to monitor changes in the toxicity of industrial effluents subjected to oxidative colour removal treatments. Journal of Environmental Monitoring, 9, 1394–1401.
Kieboom, J., Dennis, J. J., De Bont, J. A., & Zylstra, G. J. (1998). Identification and molecular characterization of an efflux pump involved in Pseudomonas putida S12 solvent tolerance. Journal of Biological Chemistry, 273, 85–91.
Kutty, S. N., & Philip, R. (2008). Marine yeasts—a review. Yeast, 25, 465–483.
Lambert, O., Piroux, M., Puyo, S., Thorin, C., Larhantec, M., Delbac, F., & Pouliquen, H. (2012). Bees, honey and pollen as sentinels for lead environmental contamination. Environment Pollution, 170, 254–259.
Lategan, M. J., Torpy, F. R., Newby, S., & Sterphenson, S. (2012). Fungal diversity of shallow aquifers in southeastern Australia. Geomicrobiology Journal, 29(4), 352–361.
Libkind, D., Brizzio, S., Ruffini, A., Gadanho, M., Broock, M. V., & Sampaio, P. J. (2003). Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. Antonie van Leeuwenhoek, 84(4), 313–322.
Loureiro, S. T. A., Cavalcanti, M. A. Q., Neves, R. P., & Passavante, J. Z. O. (2005). Yeasts isolated from sand and sea water in beaches of Olinda, Pernambuco state, Brazil. Brazilian Journal Microbiology, 36(4), 333–337.
Mahmoud, K. M. A., & Taleb, H. M. A. A. (2013). Fresh water snails as bioindicator for some heavy metals in the aquatic environment. African Journal of Ecology, 51(2), 193–198.
Manastir, L., Ergon, M. C., & Yücesoy, M. (2009). Investigation of mutations in ERG11 gene of fluconazole resistant Candida albicans isolates from Turkish hospitals. Mycoses, 54(2), 99–104.
Mariano, V., McCrindle, C. M. E., Cenci-Goga, B., & Picard, J. A. (2009). Case-control study to determine whether river water can spread tetracycline resistance to unexposed Impala (Aepyceros melampus) in Kruger National Park (South Africa). Applied and Environmental Microbiology, 75(1), 113–118.
Mazzia, C., Capowiez, Y., Sanchez-Hernandez, J. C., Köhler, H. R., Triebskorn, R., & Rault, M. (2011). Acetylcholinesterase activity in the terrestrial snail Xeropicta derbentina transplanted in apple orchards with different pesticide management strategies. Environmental Pollution, 159(1), 319–323.
Medeiros, A. O., Kohler, L. M., Hamdan, J. S., Missagia, B. S., Barbosa, F. A. R., & Rosa, C. A. (2008). Diversity and antifungal susceptibility of yeasts from tropical freshwater environments in Southeastern Brazil. Water Research, 42(14), 3921–3929.
Müller, F. M. C., Staudigel, A., Salvenmoser, S., Tredup, A., Miltenberger, R., & Hermann, J. V. (2007). Cross-resistance to medical and agricultural azole drugs in yeasts from the oropharynx of human immunodeficiency virus patients and from environmental Bavarian vine grapes. Antimicrobial Agents and Chemotherapy, 51(8), 3014–3016.
Papon, N., Savini, V., Lanoue, A., Simkin, A. J., Crèche, J., Giglioli-Guivarc’h, N., Clastre, M., Courdavault, V., & Sibirny, A. A. (2013). Candida guilliermondii: biotechnological applications, perspectives for biological control, emerging clinical importance and recent advances in genetics. Current Genetics, 59(3), 73–90.
Raspor, P., & Zupan, J. (2006). Yeasts in extreme environments. In C. Rosa & P. Gábor (Eds.), Biodiversity and ecophysiology of yeasts (pp. 371–417). Berlin Heidelberg: Springer.
Rosa, C. A., Resende, M. A., Franzot, S. P., Morais, P. B., & Barbosa, F. A. R. (1990). Yeasts and coliforms distribution in a palaeo-karstic lake of Lagoa Santa Plateau—MG, Brazil. Revista de Microbiologia, 21(1), 19–24.
Sage, L., Bennasser, L., Steiman, R., & Seigle-Murandi, F. (1997). Fungal microflora biodiversity as a function of pollution in Oued Sebou (Morocco). Chemosphere, 35(4), 751–759.
Simard, R. E. (1971). Yeasts as an indicator of pollution. Marine Pollution Bulletin, 2(8), 123–125.
Sláviková, E., & Vadkertiová, R. (1997). Seasonal occurrence of yeasts and yeast-like organisms in the river Danube. Antonie van Leeuwenhoek, 72(2), 77–80.
Sláviková, E., Vadkertiová, R., & Kocková-Kratochvílová, A. (1992). Yeast isolated from artificial lake water. Canadian Journal of Microbiology, 38(11), 1206–1209.
Soares, C. A. G., Maury, M., Pagnocca, F. C., Araújo, F. V., Mendonça-Hagler, L. C., & Hagler, A. N. (1997). Ascomycetous yeast from tropical intertidal dark mud of southeast Brazilian estuaries. Journal of General and Applied Microbiology, 43(5), 265–272.
Valdes-Collazo, L., Schultz, A. J., & Hazenv, T. C. (1987). Survival of Candida albicans in tropical marine and fresh waters. Applied and Environmental Microbiology, 53(8), 1762–1767.
Van Dyk, J. S., & Pletschke, B. (2011). Review on the use of enzymes for the detection of organochlorine, organophosphate and carbamate pesticides in the environment. Chemosphere, 82(3), 291–307.
Washington, H. G. (1984). Diversity, biotic and similarity indices: a review with special relevance to aquatic ecosystems. Water Research, 18(6), 653–694.
Zorita, I., Ortiz-Zarragoitia, M., Apraiz, I., Cancio, I., Orbea, A., Soto, M., Marigómez, I., & Cajaraville, M. P. (2008). Assessment of biological effects of environmental pollution along the NW Mediterranean Sea using red mullets as sentinel organisms. Environmental Pollution, 153(1), 157–168.
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This research was supported by CNPq process (307606/2013-9) and CAPES (AE1-0052-000650100/11).
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Brilhante, R.S.N., Paiva, M.A.N., Sampaio, C.M.S. et al. Surveillance of Azole Resistance Among Candida spp. as a Strategy for the Indirect Monitoring of Freshwater Environments. Water Air Soil Pollut 226, 52 (2015). https://doi.org/10.1007/s11270-015-2340-7
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DOI: https://doi.org/10.1007/s11270-015-2340-7