Eukaryotic Organisms in Extreme Acidic Environments, the Río Tinto Case
Abstract
:1. Introduction
2. Eukaryotic Extremophiles
3. Acidic Environments. The Río Tinto (SW, Spain) Case
Location | pH | Cond | Redox | Fe | Cu | As | Cd | Zn |
---|---|---|---|---|---|---|---|---|
Iz-Iz | 1.8 ± 0.2 | 25.7 ± 2.3 | 569 ± 22 | 17 ± 4 | 12 ± 3 | 16 ± 4 | 43 ± 16 | 14 ± 3 |
ANG | 1.5 ± 0.2 | 30.8 ± 3.4 | 471 ± 16 | 16 ± 3 | 132 ± 43 | 24 ± 3 | 30 ± 12 | 162 ± 5 |
UMA | 1.6 ± 0.3 | 40.2 ± 8.3 | 473 ± 10 | 18 ± 7 | 85 ± 36 | 32 ± 5 | 40 ± 18 | 118 ± 4 |
RI | 0.9 ± 0.3 | 38.9 ± 1.6 | 460 ± 30 | 22 ± 5 | 100 ± 36 | 48 ± 7 | 34 ± 11 | 94 ± 31 |
LPC | 2.6 ± 0.3 | 3.70 ± 1.1 | 548 ± 70 | 0.2 ± 0.1 | 19 ± 7 | 0.2 ± 0.1 | 0.7 ± 0.1 | 50 ± 10 |
4. Acidophilic Eukaryotic Diversity, an Ecological Paradox
5. Photosynthesis in Acidic Environments
Species | Ic | Ik | α | β |
---|---|---|---|---|
Chlo_AG | 10.36 ± 3.26 | 59.65 ± 7.03 | 0.448 ± 0.13 | 0.0123 ± 0.01 |
Chlo_ANG | 23.19 ± 3.24 | 120.34 ± 8.08 | 0.137 ± 0.02 | 0.0431 ± 0.01 |
Eug_3.1 | 18.93 ± 0.72 | 95.41 ± 9.23 | 0.448 ± 0.09 | 0.0450 ± 0.02 |
Eug_AG | 18.44 ± 5.34 | 49.91 ± 5.89 | 0.278 ± 0.12 | 0.0441 ± 0.00 |
Eug_NUR | 16.84 ± 0.76 | 96.23 ± 5.32 | 0.263 ± 0.02 | 0.0247 ± 0.02 |
Eug_SM | 17.43 ± 4.59 | 48.53 ± 5.32 | 0.558 ± 0.05 | 0.0179 ± 0.00 |
Dia_NUR | 5.06 ± 1.72 | 47.82 ± 6.47 | 1.423 ± 0.10 | 0.0426± 0.02 |
Zyg_LPC | 38.89 ± 22.70 | 13.22 ± 3.23 | 0.249 ± 0.03 |
6. Conclusions
Acknowledgments
Conflicts of Interest
References
- 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. [Google Scholar]
- Pikuta, E.V.; Hoover, R.B.; Tang, J. Microbial extremophiles at the limits of life. Crit. Rev. Microbiol. 2007, 33, 183–209. [Google Scholar] [CrossRef]
- Brock, T.D. Thermophilic Microorganisms and Life at High Temperatures; Springer-Verlag: Berlin, Germany, 1978; p. 245. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Alexandrof, V.Y. Conformational Flexibility of Macromolecules and Ecological Adaptations. In Cells, Molecules and Temperature; Springer-Verlag: Berlin, Germany, 1977; p. 342. [Google Scholar]
- Rothschild, L.J.; Mancinelli, R.L. Life in extreme environments. Nature 2001, 409, 1092–1101. [Google Scholar] [CrossRef]
- Brock, T. Lower pH limit for the existence of blue-green algae: Evolutionary and ecological implications. Science 1973, 179, 480–483. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Stibal, M.; Elster, J.; Šabacká, M.; Kaštovská, 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Gross, S.; Robbins, E.I. Acidophilic and acid-tolerant fungi and yeasts. Hydrobiologia 2000, 433, 91–109. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Schleper, C.; Puehler, G.; Kuhlmorgen, B.; Zillig, W. Life at extremely low pH. Nature 1995, 375, 741–742. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar]
- Johnson, D.B. Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol. Ecol. 1998, 27, 307–317. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Visviki, I.; Santikul, D. The pH tolerance of Chlamydomonas applanata (Volvocales, Chlorophyta). Arch. Environ. Cont. Toxicol. 2000, 38, 147–151. [Google Scholar] [CrossRef]
- DeNicola, D.M. A review of diatoms found in highly acidic environments. Hydrobiologia 2000, 433, 111–122. [Google Scholar] [CrossRef]
- Battarbee, R.W.; Smol, J.P.; Meriläinen, J. Diatoms as indicators of pH: An Historical Review. In Diatoms and Lake Acidity; Smol, J.P., Battarbee, R.W., Davis, R.B., Meriläinen, J., Eds.; Dr. W. Junk Publication: Dordrecht, Germany, 1986; pp. 5–14. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar]
- Rodrıguez, 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. [Google Scholar]
- Schmidt, W. Iron solutions: Acquisition strategies and signalling pathways in plants. Trends Plant Sci. 2003, 8, 188–193. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- Koschorrek, M.; Tittel, J. Benthic photosynthesis in acidic mining lake (pH 2.6). Limnol. Oceanogr. 2002, 47, 1197–1201. [Google Scholar]
- Souza-Egipsy, V.; Altamirano, M.; Amils, R.; Aguilera, A. Photosynthetic performance of phototrophic biofilms in extreme acidic environments. Environ. Microbiol. 2011, 13, 2351–2358. [Google Scholar]
- Ritchie, R.J. Fitting light saturation curves measured using modulated fluorometry. Photosynth. Res. 2008, 96, 201–215. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- Hanikenne, M. C. reinhardtii as a eukaryotic photosynthetic model for studies of heavy metal homeostasis and tolerance. New Phytol. 2003, 159, 331–340. [Google Scholar] [CrossRef]
- Pinto, E.; Sigaud-Kutner, T.; Leitão, M.; Okamoto, O. Heavy-metal induced oxidative stress in algae. J. Phycol. 2003, 39, 1008–1018. [Google Scholar]
- Boswell, C.; Sharma, N.C.; Sahi, S.V. Copper tolerance and accumulation potential of Chlamydomonas reinhardtii. Bull. Environ. Cont. Toxicol. 2002, 69, 546–553. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- Furuya, M. Phytochromes: Their molecular species, gene families, and functions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1993, 44, 617–641. [Google Scholar] [CrossRef]
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Aguilera, A. Eukaryotic Organisms in Extreme Acidic Environments, the Río Tinto Case. Life 2013, 3, 363-374. https://doi.org/10.3390/life3030363
Aguilera A. Eukaryotic Organisms in Extreme Acidic Environments, the Río Tinto Case. Life. 2013; 3(3):363-374. https://doi.org/10.3390/life3030363
Chicago/Turabian StyleAguilera, Angeles. 2013. "Eukaryotic Organisms in Extreme Acidic Environments, the Río Tinto Case" Life 3, no. 3: 363-374. https://doi.org/10.3390/life3030363