A major issue in microbial ecology is to identify the limits of life for growth and survival, and to understand the molecular mechanisms that define these limits. Thus, interest in the biodiversity and ecology of extreme environments has grown in recent years for several reasons. Some are basic and revolve around the idea that extreme environments are believed to reflect early Earth conditions. Others are related to the biotechnological potential of extremophiles. In this regard, the study of extremely acidic environments has become increasingly important since environmental acidity is often caused by microbial activity. Highly acidic environments are relatively scarce worldwide and are generally associated with volcanic activity or mining operations. For most acidic environments, low pH facilitates metal solubility, and therefore acidic waters tend to have high concentrations of heavy metals. However, highly acidic environments are usually inhabited by acidophilic and acidotolerant eukaryotic microorganisms such as algae, amoebas, ciliates, heliozoan and rotifers, not to mention filamentous fungi and yeasts. Here, we review the general trends concerning the diversity and ecophysiology of eukaryotic acidophilic microorganims, as well as summarize our latest results on this topic in one of the largest extreme acidic rivers, Río Tinto (SW, Spain).
References
[1]
González-Toril, E.; Llobet-Brossa, E.; Casamayor, E.O.; Amann, R.; Amils, R. Microbial ecology of an extreme acidic environment, the Tinto River. Appl. Environ. Microbiol.?2003, 69, 4853–4865.
[2]
Pikuta, E.V.; Hoover, R.B.; Tang, J. Microbial extremophiles at the limits of life. Crit. Rev. Microbiol.?2007, 33, 183–209, doi:10.1080/10408410701451948.
[3]
Brock, T.D. Thermophilic Microorganisms and Life at High Temperatures; Springer-Verlag: Berlin, Germany, 1978; p. 245.
[4]
Roberts, D.M.L. Eukaryotic Cells under Extreme Conditions. In Enigmatic Microorganisms and Life in Extreme Environments; Seckbach, J., Ed.; Kluwer Academic Publication: London, UK, 1999; pp. 165–173.
[5]
Caron, D.A.; Countway, P.D.; Brown, M.V. The growing contributions of molecular biology and immunology to protistan ecology: Molecular signatures as ecological tools. J. Euk. Microbiol.?2004, 51, 38–48, doi:10.1111/j.1550-7408.2004.tb00159.x.
[6]
Alexandrof, V.Y. Conformational Flexibility of Macromolecules and Ecological Adaptations. In Cells, Molecules and Temperature; Springer-Verlag: Berlin, Germany, 1977; p. 342.
[7]
Rothschild, L.J.; Mancinelli, R.L. Life in extreme environments. Nature?2001, 409, 1092–1101, doi:10.1038/35059215.
[8]
Brock, T. Lower pH limit for the existence of blue-green algae: Evolutionary and ecological implications. Science?1973, 179, 480–483.
[9]
Seckbach, J. Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells. In Developments in Hydrobiology; Kluwer Academic Publication: Dordrecht, Germany, 1994; p. 349.
[10]
Ciniglia, C.; Yoon, H.S.; Pollio, A.; Pinto, G.; Bhattacharya, D. Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol. Ecol.?2004, 13, 1827–1838, doi:10.1111/j.1365-294X.2004.02180.x.
[11]
Stibal, M.; Elster, J.; ?abacká, M.; Ka?tovská, K. Seasonal and diel changes in photosynthetic activity of the snow alga Chlamydomonas nivalis (Chlorophyceae) from Svalbard determined by pulse amplitude modulation fluorometry. FEMS Microbiol. Ecol.?2006, 59, 265–273.
[12]
Garrison, D.L.; Close, A.R. Winter ecology of the sea ice biota in Weddel Sea pack ice. Mar. Ecol. Prog. Ser.?1993, 96, 17–31, doi:10.3354/meps096017.
[13]
Gross, S.; Robbins, E.I. Acidophilic and acid-tolerant fungi and yeasts. Hydrobiologia?2000, 433, 91–109, doi:10.1023/A:1004014603333.
[14]
Russo, G.; Libkind, D.; Sampaio, J.P.; VanBrock, M.R. Yeast diversity in the acidic Río Agrio-Lake Caviahue volcanic environment (Patagonia, Argentina). FEMS Microbiol. Ecol.?2008, 65, 415–424, doi:10.1111/j.1574-6941.2008.00514.x.
[15]
Oggerin, M.; Tornos, F.; Rodríguez, N.; del Moral, C.; Sánchez-Román, M.; Amils, R. Specific jarosite biomineralization by Purpureocillium lilacinum, an acidophilic fungi isolated from Río Tinto. Environ. Microbiol.?2013, doi:10.1111/1462–2920.12094.
[16]
Schleper, C.; Puehler, G.; Kuhlmorgen, B.; Zillig, W. Life at extremely low pH. Nature?1995, 375, 741–742.
[17]
Baffico, G.D.; Díaz, M.M.; Wenzel, M.T.; Koschorreck, M.; Schimmele, M.; Neu, T.R.; Pedrozo, F. Community structure and photosynthetic activity of epilithon from a highly acidic (pH < 2) mountain stream in Patagania, Argentina. Extremophiles?2004, 8, 465–475.
[18]
Nordstrom, D.K.; Southam, G. Geomicrobiology of Sulphide Mineral Oxidation. In Geomicrobiology: Interactions Between Microbes and Minerals; Banfield, J.F., Nealson, K.H., Eds.; Mineralogical Society of America: Washington, DC, USA, 1997; Volume 35, pp. 361–390.
[19]
Johnson, D.B. Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol. Ecol.?1998, 27, 307–317, doi:10.1111/j.1574-6941.1998.tb00547.x.
[20]
Amaral, L.A.; Gómez, F.; Zettler, E.; Keenan, B.G.; Amils, R.; Sogin, M.L. Eukaryotic diversity in Spain’s river of fire. Nature?2002, 417, 137, doi:10.1038/417137a.
[21]
Aguilera, A.; Manrubia, S.C.; Gómez, F.; Rodríguez, N.; Amils, R. Eukaryotic community distribution and their relationship to water physicochemical parameters in an extreme acidic environment, Río Tinto (SW, Spain). Appl. Environ. Microbiol.?2006, 72, 5325–5330, doi:10.1128/AEM.00513-06.
[22]
Boulter, C.A. Did both extensional tectonics and magmas act as major drivers of convection cells during the formation of the Iberian Pyritic Belt massive sulfide deposits? J. Geol. Soc. Lond.?1996, 153, 181–184, doi:10.1144/gsjgs.153.2.0181.
[23]
Leistel, J.M.; Marcoux, E.; Thieblemont, D.; Quesada, C.; Sanchez, A.; Almodovar, G.R.; Pascual, E.; Saez, R. The volcanic-hosted massive sulphidic deposits of the Iberian Pyritic Belt. Miner. Deposita?1998, 33, 2–30.
[24]
Aguilera, A.; Souza-Egipsy, V.; Gómez, F.; Amils, R. Development and structure of eukaryotic biofilms in an extreme acidic environment, Río Tinto (SW, Spain). Microb. Ecol.?2006, 53, 294–305.
[25]
Aguilera, A.; Gómez, F.; Lospitao, E.; Amils, R. A molecular approach to the characterization of the eukaryotic communities of an extreme acidic environment: Methods for DNA extraction and denaturing gradient electrophoresis analysis. Syst. Appl. Microbiol.?2006, 29, 593–605, doi:10.1016/j.syapm.2006.01.006.
[26]
Visviki, I.; Santikul, D. The pH tolerance of Chlamydomonas applanata (Volvocales, Chlorophyta). Arch. Environ. Cont. Toxicol.?2000, 38, 147–151, doi:10.1007/s002449910018.
[27]
DeNicola, D.M. A review of diatoms found in highly acidic environments. Hydrobiologia?2000, 433, 111–122, doi:10.1023/A:1004066620172.
[28]
Battarbee, R.W.; Smol, J.P.; Meril?inen, J. Diatoms as indicators of pH: An Historical Review. In Diatoms and Lake Acidity; Smol, J.P., Battarbee, R.W., Davis, R.B., Meril?inen, J., Eds.; Dr. W. Junk Publication: Dordrecht, Germany, 1986; pp. 5–14.
[29]
Aguilera, A.; Amils, R. Tolerance to cadmium in Chlamydomonas sp. (Chlorophyta) strains isolated from an extreme acidic environment, the Tinto River (SW, Spain). Aquat. Toxicol.?2005, 75, 316–329.
[30]
López-Archilla, A.I.; Marín, I.; Amils, R. Microbial community composition and ecology of an acidic aquatic environment: The Tinto river, Spain. Microb. Ecol.?2001, 41, 20–35.
[31]
López-Archilla, A.I.; González, A.E.; Terrón, M.C.; Amils, R. Diversity and ecological relationships of the fungal populations of an acidic river of Southwestern Spain: The Tinto River. Can. J. Microbiol.?2005, 50, 923–934.
[32]
Rodr?guez, N.; Menendez, N.; Tornero, J.; Amils, R.; de la Fuente, V. Internal iron biomineralization in Imperata cilindrica, aperennial grass: Chemical composition, speciation and plant localization. New Phytol.?2005, 165, 781–789.
[33]
Schmidt, W. Iron solutions: Acquisition strategies and signalling pathways in plants. Trends Plant Sci.?2003, 8, 188–193, doi:10.1016/S1360-1385(03)00048-7.
[34]
Fernandez-Remolar, D.C.; Morris, R.V.; Gruener, J.E.; Amils, R.; Knoll, A.H. The Río Tinto Basin, Spain: Mineralogy, sedimentary geobiology and implications for interpretation of outcrop rocks at Meridiani Planum, Mars. Earth Plannet Sci. Lett.?2005, 240, 149–167, doi:10.1016/j.epsl.2005.09.043.
[35]
Niyogi, D.K.; Lewis, W.M.; McKnight, D.M. Effects of stress from mine drainage on diversity, biomass, and function of primary producers in mountain streams. Ecosystems?2002, 5, 554–567.
[36]
Spijkerman, E.; Barua, D.; Gerloff-Elias, A.; Kern, J.; Gaedke, U.; Heckathorn, S.A. Stress responses and metal tolerance of Chlamydomonas acidophila in metal-enriched lake water and artificial medium. Extremophiles?2007, 11, 551–562, doi:10.1007/s00792-007-0067-0.
[37]
Guyre, R.A.; Konopka, A.; Brooks, A.; Doemel, W. Algal and bacterial activities in acidic (ph3) strip mine lakes. Appl. Environ. Microbiol.?1987, 53, 2069–2076.
[38]
Koschorrek, M.; Tittel, J. Benthic photosynthesis in acidic mining lake (pH 2.6). Limnol. Oceanogr.?2002, 47, 1197–1201.
[39]
Souza-Egipsy, V.; Altamirano, M.; Amils, R.; Aguilera, A. Photosynthetic performance of phototrophic biofilms in extreme acidic environments. Environ. Microbiol.?2011, 13, 2351–2358.
Nixdorf, B.; Krumbeeck, H.; Jander, J.; Beulker, C. Comparison of bacterial an phytoplankton productivity in extremely acidic mining lakes and eutrophic hard water lakes. Acta Oecol.?2003, 24, S281–S288, doi:10.1016/S1146-609X(03)00031-6.
[42]
Cid, C.; Garcia-Descalzo, L.; Casado-Lafuente, V.; Amils, R.; Aguilera, A. Proteomic analysis of the response of an acidophilic strain of Chlamydomonas sp. (Chlorophyta) to natural metal-rich water. Proteomics?2010, 10, 2026–2036.
[43]
Hanikenne, M. C. reinhardtii as a eukaryotic photosynthetic model for studies of heavy metal homeostasis and tolerance. New Phytol.?2003, 159, 331–340, doi:10.1046/j.1469-8137.2003.00788.x.
[44]
Pinto, E.; Sigaud-Kutner, T.; Leit?o, M.; Okamoto, O. Heavy-metal induced oxidative stress in algae. J. Phycol.?2003, 39, 1008–1018.
Gillet, S.; Decottignies, P.; Chardonnet, S.; Maréchal, P. Cadmium response and redoxin targets in Chlamydomonas reinhardtii: A proteomic approach. Photosynth. Res.?2006, 89, 201–211, doi:10.1007/s11120-006-9108-2.
[47]
Takamura, N.; Kasai, F.; Watanabe, M.M. Effects of Cu, Cd and Zn on photosynthesis of fresh water benthic algae. J. Appl. Phycol.?1989, 1, 39–52, doi:10.1007/BF00003534.
[48]
Wang, S.; Chen, F.; Sommerfeld, M.; Hu, Q. Proteomic analysis of molecular response to oxidative stress by the green alga Haematococcus pluvialis (Chlorophyceae). Planta?2004, 220, 17–29, doi:10.1007/s00425-004-1323-5.
[49]
Langner, U.; Jakob, T.; Stehfest, K.; Wilhelm, C. An energy balance from absorbed protons to new biomass for C. reinhardtii and C. acidophila under neutral and extremely acidic growth conditions. Plant Cell Environ.?2009, 32, 250–258.
[50]
Furuya, M. Phytochromes: Their molecular species, gene families, and functions. Annu. Rev. Plant Physiol. Plant Mol. Biol.?1993, 44, 617–641, doi:10.1146/annurev.pp.44.060193.003153.