Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-08T02:30:52.321Z Has data issue: false hasContentIssue false

Brazilian research on extremophiles in the context of astrobiology

Published online by Cambridge University Press:  11 July 2012

Rubens T. D. Duarte
Affiliation:
Laboratório de Ecologia Microbiana, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brazil Laboratório de Astrobiologia, Instituto de Astronomia, Geofísica e Ciências Atmosféricas, Universidade de São Paulo, São Paulo, Brazil
Felipe Nóbrega
Affiliation:
Laboratório de Ecologia Microbiana, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brazil
Cristina R. Nakayama
Affiliation:
Departamento de Ciências Biológicas, Universidade Federal de São Paulo, São Paulo, Brazil
Vivian H. Pellizari*
Affiliation:
Laboratório de Ecologia Microbiana, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brazil

Abstract

Extremophiles are organisms adapted to grow at extreme ranges of environmental variables, such as high or low temperatures, acid or alkaline medium, high salt concentration, high pressures and so forth. Most extremophiles are micro-organisms that belong to the Archaea and Bacteria domains, and are widely spread across the world, which include the polar regions, volcanoes, deserts, deep oceanic sediments, hydrothermal vents, hypersaline lakes, acid and alkaline water bodies, and other extreme environments considered hostile to human life. Despite the tropical climate, Brazil has a wide range of ecosystems which include some permanent or seasonally extreme environments. For example, the Cerrado is a biome with very low soil pH with high Al+3 concentration, the mangroves in the Brazilian coast are anaerobic and saline, Pantanal has thousands of alkaline–saline lakes, the Caatinga arid and hot soils and the deep sea sediments in the Brazilian ocean shelf. These environments harbour extremophilic organisms that, coupled with the high natural biodiversity in Brazil, could be explored for different purposes. However, only a few projects in Brazil intended to study the extremophiles. In the frame of astrobiology, for example, these organisms could provide important models for defining the limits of life and hypothesize about life outside Earth. Brazilian microbiologists have, however, studied the extremophilic micro-organisms inhabiting non-Brazilian environments, such as the Antarctic continent. The experience and previous results obtained from the Brazilian Antarctic Program (PROANTAR) provide important results that are directly related to astrobiology. This article is a brief synopsis of the Brazilian experience in researching extremophiles, indicating the most important results related to astrobiology and some future perspectives in this area.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abraham, W.-R., Estrela, A.B., Nikitin, D.I., Smit, J. & Vancanneyt, M. (2010). Brevundimonas halotolerans sp. nov., Brevundimonas poindexterae sp. nov. and Brevundimonas staleyi sp. nov., prosthecate bacteria from aquatic habitats. Int. J. Syst. Evol. Microbiol. 60, 18371843.Google Scholar
Aguiar, L.M.S., Machado, B.M. & Marinho-Filho, J. (2004). A Diversidade Biológica do Cerrado. In Cerrado: ecologia e caracterização, ed. Aguiar, L.M.S. & Camargo, A.J.A., pp. 740. Embrapa Cerrados, Planaltina.Google Scholar
Almeida, M.A.N. & Franca, F.P. (1999). Thermophilic and mesophilic bacteria in biofilms associated with corrosion in a heat exchanger. World J. Microb. Biot. 15, 439442.Google Scholar
Almeida, W.I. et al. (2009). Archaeal and bacterial communities of heavy metal contaminated acidic waters from zinc mine residues in Sepetiba Bay. Extremophiles 13, 263271.Google Scholar
Almeida, T.I.R., Calijuri, M.C., Falco, P.B., Casali, S.P., Kupriyanova, E., Paranhos-Filho, A.C., Sigolo, J.B. & Bertolo, R.A. (2011). Biogeochemical processes and the diversity of Nhecolândia lakes, Brazil. An. Acad. Bras. Ciênc. 83, 391407.Google Scholar
Appanna, V.D., Kepes, M. & Rochon, P. (1994). Aluminum tolerance in Pseudomonas fluorescens ATCC 13525: Involvement of a gelatinous lipid-rich residue. FEMS Microbiol. Lett. 199, 295302.CrossRefGoogle Scholar
Araújo, L.S., Kagohara, E., Garcia, T.P., Pellizari, V.H. & Andrade, L.H. (2011). Screening of microorganisms producing cold-active oxidoreductases to be applied in enantioselective alcohol oxidation. An Antarctic survey. Mar. Drugs 9, 889905.Google Scholar
Borneman, J. & Triplett, E.W. (1997). Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl. Environ. Microbiol. 63, 26472653.Google Scholar
Cardoso, A.M., Vieira, R.P., Paranhos, R., Clementino, M.M., Albano, R.M. & Martins, O.B. (2011). Hunting for extremophiles in Rio de Janeiro. Front. Microbiol. 2, 13.Google Scholar
Castelletti, C.H.M., Santos, A.M.M., Tabarelli, M. & Silva, J.M.C. (2003). Quanto ainda resta da caatinga? Uma estimativa preliminar. In Ecologia e Conservação da Caatinga, ed. Leal, I., Tabarelli, M. & Silva, J.M.C.Editora Universitária da Universidade Federal de Pernambuco, Recife, Brazil, pp. 804.Google Scholar
Chanal, A., Chapon, V., Benzerara, K., Barakat, M., Christen, R., Achouak, W., Barras, F. & Heulin, T. (2006). The desert of Tataouine: na extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria. Environ. Microbiol. 8, 514525.Google Scholar
Clementino, M.M. et al. (2008). Prokaryotic diversity in one of the largest hypersaline coastal lagoons in the world. Extremophiles 12, 595604.Google Scholar
Conrad, R. (2009). The global methane cycle: recent advances in understanding the microbial processes involved. Environ. Microbiol. Reports 1, 285292.CrossRefGoogle ScholarPubMed
Cox, M.M. & Battista, J.R. (2005). Deinococcus radiodurans – the consummate survivor. Nat. Rev. Microbiol. 3, 882892.CrossRefGoogle ScholarPubMed
Cruz, A.K., Terenzi, H.F., Jorge, J.A. & Terenzi, H.F. (1988). Cyclic AMP dependent, constitutive thermotolerance in the adenylate cyclase-deficient cr-1 (crisp) mutant of Neurospora crassa. Curr. Genet. 13, 451454.Google Scholar
Da Silva, G.A., Trufem, S.F., Saggin Júnior, O.J. & Maia, L.C. (2005). Arbuscular mycorrhizal fungi in a semiarid copper mining area in Brazil. Mycorrhiza 15, 4753.CrossRefGoogle Scholar
Dias, A.C.F., Andreote, F.D., Dini-Andreote, F., Lacava, P.T., , A.L.B., Melo, I.S., Azevedo, J.L. & Araújo, W.L. (2009). Diversity and biotechnological potential of culturable bacteria from Brazilian mangrove sediment. World J. Microbiol. Biotechnol. 25, 13051311.Google Scholar
Dias, A.C.F., Andreote, F.D., Rigonato, J., Fiore, M.F., Melo, I.S. & Araújo, W.L. (2010). The bacterial diversity in a Brazilian non-disturbed mangrove sediment. Anton. van Leeuwen. 98, 541551.Google Scholar
Dias, A.C.F., Dini-Andreote, F., Taketani, R.G., Tsai, S.M., Azevedo, J.L., Melo, I.S. & Andreote, F.D. (2011). Archaeal communities in the sediments of three contrasting mangroves. J. Soils Sediments 11, 14661476.CrossRefGoogle Scholar
Gilichinsky, D.A. et al. (2007). Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology 7, 275311.Google Scholar
Gomes, R.C., Semedo, L.T.A.S., Linhares, A.A., Guimarães, A.C.C., Alviano, C.S., Linhares, L.F. & Coelho, R.R.R. (1999). Efficiency of the dispersion and differential centrifugation technique in the isolation of chitinolytic actinomycetes from soil. World J. Microbiol. Biotechnol. 15, 4750.CrossRefGoogle Scholar
Gomes, R.C., Semedo, L.T.A.S., Soares, R.M.A., Linhares, L.F., Ulhoa, C.J., Alviano, C.S. & Coelho, R.R.R. (2001). Purification of a thermostable endochitinase from Streptomyces RC1071 isolated from a cerrado soil and its antagonism against phytopathogenic fungi. J. Appl. Microbiol. 90, 653661.Google Scholar
Gonzáles-Toril, E., Amils, R., Delmas, R.J., Petit, J.-R., Komarek, J. & Elster, J. (2009). Bacterial diversity of autotrophic enriched cultures from remote, glacial Antarctic, Alpine and Andean aerosol, snow and soil samples. Biogeosciences 6, 3344.CrossRefGoogle Scholar
Gorlach-Lira, K. & Coutinho, H.D.M. (2007). Population dynamics and extracellular enzymes activity of mesophilic and thermophilic bacteria isolated from semi-arid soil of northeastern Brazil. Braz. J. Microbiol. 38, 135141.Google Scholar
Holguin, G., Vazquez, P. & Bashan, Y. (2001). The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol. Fertil. Soils 33, 265278.Google Scholar
Hollister, E.B., Engledow, A.S., Hammett, A.J., Provin, T.L., Wilkinson, H.H. & Gentry, T.J. (2010). Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J. 4, 829838.CrossRefGoogle ScholarPubMed
Horneck, G. & Rettberg, P. (2007). Complete Course in Astrobiology. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, p. 413.Google Scholar
Johnson, S.S. et al. (2007). Ancient bacteria show evidence of DNA repair. Proc. Natl. Acad. Sci. U.S.A. 104, 1440114405.Google Scholar
Jones, B.E., Grant, W.D., Duckworth, A.W. & Owenson, G.G. (1998). Microbial diversity in soda lakes. Extremophiles 2, 191200.CrossRefGoogle ScholarPubMed
Kochian, L.V. (1995). Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 237260.Google Scholar
Konishi, S., Souta, I., Takahashi, J., Ohmoto, M. & Kaneko, S. (1994). Isolation and characteristics of acid- and aluminum-tolerant bacterium. Biosci. Biotechnol. Biochem. 58, 19601963.Google Scholar
Kuhn, E., Bellicanta, G.S. & Pellizari, V.H. (2009). New alk genes detected in Antarctic marine sediments. Environ. Microbiol. 11, 669673.Google Scholar
Kvist, T., Mengewein, A., Manzei, S., Ahring, B.K. & Westermann, P. (2005). Diversity of termophilic and non-termophilic Crenarchaeota at 80 °C. FEMS Microbiol. Lett. 244, 6168.CrossRefGoogle Scholar
La Duc, M.T., Dekas, A., Osman, S., Moissl, C., Newcombe, D. & Venkateswaran, K. (2007). Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Appl. Environ. Microbiol. 73, 26002611.CrossRefGoogle ScholarPubMed
Leal, I.R., Silva, J.M.C., Tabarelli, M. & Lacher, T.E. (2005). Changing the course of biodiversity conservation in the caatinga of northeastern Brazil. Conserv. Biol. 19, 701706.Google Scholar
Li, Y., Kawamura, Y., Fujiwara, N., Naka, T., Liu, H., Huang, X., Kobayashi, K. & Ezaki, T. (2004). Sphingomonas yabuuchiae sp. nov. and Brevundimonas nasdae sp. nov., isolated from the Russian space laboratory Mir. Int. J. Syst. Evol. Microbiol. 54, 819825.Google Scholar
Llodra, E.R., Tyler, P.A. & German, C.R. (2003). Biogeography of deep-water chemosynthetic ecosystems (CHESS): exploring the southern oceans. Gayana 67, 168176.Google Scholar
López-García, P. (2005). Extremophiles. In Lectures in Astrobiology, ed. Gargaud, M., Barbier, B., Martin, H. & Reisse, J., pp. 657679. Springer-Verlag, Berlin, Heidelberg, Berlin, Germany.CrossRefGoogle Scholar
Loque, C.P., Medeiros, A.O., Pellizzari, F.M., Oliveira, E.C., Rosa, C.A. & Rosa, L.H. (2010). Fungal community associated with marine macroalgae from Antarctica. Polar Biol. 33, 641648.CrossRefGoogle Scholar
Lugão, P.P., LaTerra, E.F., Kriegshäuser, B. & Fontes, S.L. (2002). Magnetotelluric studies of the Caldas Novas geothermal reservoir, Brazil. J. Appl. Geophys. 49, 3346.CrossRefGoogle Scholar
Luz, A.P., Pellizari, V.H., Whyte, L.G. & Greer, C.W. (2004). A survey of indigenous microbial hydrocarbon degradation genes in soils from Antarctica and Brazil. Can. J. Microbiol. 50, 323333.Google Scholar
Luz, A.P., Ciapina, E.M.P., Gamba, R.C., Lauretto, M.S., Farias, E.W.C., Bicego, M.C., Taniguchi, S., Montone, R.C. & Pellizari, V.H. (2006). Potential for bioremediation of hydrocarbon polluted soils in the Maritime Antarctic. Antarct. Sci. 18, 335343.CrossRefGoogle Scholar
Mardanov, A.V., Gumerov, V.M., Beletsky, A.V., Perevalova, A.A., Karpov, G.A., Bonch-Osmolovskaya, E.A. & Ravin, N.V. (2011). Uncultured archaea dominate in the thermal groundwater of Uzon Caldera, Kamchatka. Extremophiles 15, 365372.CrossRefGoogle ScholarPubMed
Martins, C.C., Montone, R.C., Gamba, R.C. & Pellizari, V.H. (2005). Sterols and fecal microrganisms as indicator of sewage pollution in marine surface sediments of Admiralty Bay, Antarctic. Braz. J. Oceanogr. 1, 112.Google Scholar
Medina-Júnior, P.B. & Rietzeler, A.C. (2005). Limnological study of a Pantanal saline lake. Braz. J. Biol. 65, 651659.CrossRefGoogle ScholarPubMed
Mittermeier, R.A., Myers, N. & Mittermeier, C.G. (2000). Hotspots: Earth's Biologically Richest and Most Endangered Terrestrial Ecoregions. Conservation International, Mexico, p. 430.Google Scholar
Molisani, M.M., Martins, R.V., Machado, W., Paraquetti, H.H.M., Bidone, E.D. & Lacerda, L.D. (2004). Environmental changes in Sepetiba Bay, SE Brazil. Reg. Environ. Change 4, 1727.Google Scholar
Moreira-Turcq, P.F. (2000). Impact of a low salinity year on the metabolism of a hypersaline coastal lagoon (Brazil). Hydrobiologia 429, 133140.Google Scholar
Mumma, M.J., Villanueva, G.L., Novak, R.E., Hewagama, T., Bonev, B.P., DiSanti, M.A., Mandell, A.M. & Smith, M.D. (2005). Strong release of methane on Mars in Northern Summer 2003. Science 323, 10411045.Google Scholar
Mykytczuk, N.C., Trevors, J.T., Foote, S.J., Leduc, L.G., Ferroni, G.D. & Twine, S.M. (2011). Proteomic insights into cold adaptation of psychrotrophic and mesophilic Acidithiobacillus ferrooxidans strains. Anton. van Leeuwen. 100, 259277.Google Scholar
Nakayama, C.R., Kuhn, E., Araújo, A.C.V., Alvalá, P.C., Ferreira, W.J., Vazoller, R.F. & Pellizari, V.H. (2011). Revealing archaeal diversity patterns and methane fluxes in Admiralty Bay, King George Island, and their association to Brazilian Antarctic Station activities. Deep-Sea Res. PT II 58, 128138.Google Scholar
Nicol, G.W., Tscherko, D., Embley, T.M. & Prosser, J.I. (2005). Primary succession of soil Crenarchaeota across a receding glacier foreland. Environ. Microbiol. 7, 337347.Google Scholar
Paerl, H.W., Pinckney, J.L. & Steppe, T.F. (2000). Cyanobacterial-bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments. Environ. Microbiol. 2, 1126.Google Scholar
Park, S.-J., Park, B.-J. & Rhee, S.K. (2008). Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles 12, 605615.Google Scholar
Prado, D.E. (2003). As caatingas da América do Sul. In Ecologia e Conservação da Caatinga, ed. Leal, I., Tabarelli, M. & Silva, J.M.C.Editora Universitária da Universidade Federal de Pernambuco, Recife, Brazil, p. 804.Google Scholar
Ratter, J.A., Ribeiro, J.F. & Bridgewater, S. (1997). The Brazilian Cerrado vegetation and threats to its biodiversity. Ann. Bot. 80, 223230.CrossRefGoogle Scholar
Rezende, S.T., Guimarães, V.M., Rodrigues, M.C. & Felix, C.R. (2005). Purification and characterization of an alpha-galactosidase from Aspergillus fumigatus. Braz. Arch. Biol. Technol. 48, 195202.Google Scholar
Rigonato, J., Alvarenga, D.O., Andreote, F.D., Dias, A.C.F., Melo, I.S., Kent, A. & Fiore, M.F. (2012). Cyanobacterial diversity in the phyllosphere of a mangrove Forest. FEMS Microbiol. Ecol. 80, 312322.Google Scholar
Rodrigues, D.F., Jesus, E.C., Ayala-Del-Río, H.L., Pellizari, V.H., Gilichinsky, D., Sepulveda-Torres, L. & Tiedje, J.M. (2009). Biogeography of two cold-adapted genera: Psychrobacter and Exiguobacterium. ISME J. 3, 658665.CrossRefGoogle ScholarPubMed
Rosa, L.H., Vaz, A.B.M., Caligiorne, R.B., Campolina, S. & Rosa, C.A. (2009). Endophytic fungi associated with the Antarctic grass Deschampsia antarctica Desv. (Poaceae). Polar Biol. 32, 161167.Google Scholar
Rosa, L.H., Vieira, M.L.A., Santiago, I.F. & Rosa, C.A. (2010). Endophytic fungi associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol. Ecol. 73, 178189.Google Scholar
Rothschild, L.J. & Mancinelli, R. (2001). Life in extreme environments. Nature 409, 10921101.CrossRefGoogle ScholarPubMed
Sahoo, K. & Dhal, N.K. (2009). Potential microbial diversity in mangrove ecosystems: a review. Indian J. Mar. Sci. 38, 249256.Google Scholar
Santiago, I.F., Alves, T.M., Rabello, A., Sales Junior, P.A., Romanha, A.J., Zani, C.L., Rosa, C.A. & Rosa, L.H. (2012). Leishmanicidal and antitumoral activities of endophytic fungi associated with the Antarctic angiosperms Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl. Extremophiles 16, 95103.CrossRefGoogle Scholar
Seckbach, J., & Oren, A. (2007). Oxygenic photosynthetic microorganisms in extreme environments. In Algae and Cyanobacteria in Extreme Environments. ed. Seckbach, J.. Springer, Dordrecht, pp. 425.Google Scholar
Sheridan, P.P., Miteva, V.I. & Brenchley, J.E. (2003). Phylogenetic analysis of anaerobic psychrophilic enrichment cultures obtained from a greenland glacier ice core. Appl. Environ. Microbiol. 69, 21532160.Google Scholar
Siebers, B. et al. (2011). The complete genome sequence of Thermoproteus tenax: a physiologically versatile member of the Crenarchaeota. PLoS One 6, e24222.Google Scholar
Sogin, M.L., Morrison, H.G., Huber, J.A., Welch, D.M., Huse, S.M., Neal, P.R., Arrieta, J.M. & Herndl, G.J. (2006). Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc. Natl. Acad. Sci. U.S.A. 103, 1211512120.Google Scholar
Soto-Ramírez, N., Sánchez-Porro, C., Rosas-Padilla, S., Almodóvar, K., Jiménez, G., Machado-Rodríguez, M., Zapata, M., Ventosa, A. & Montalvo-Rodríguez, R. (2008). Halobacillus mangrovi sp. nov., a moderately halophilic bacterium isolated from the black mangrove Avicennia germinans. Int. J. Syst. Evol. Microbiol. 58, 125130.Google Scholar
Stetter, K.O. (1996). Hyperthermophilic prokaryotes. FEMS Microbiol. Rev. 18, 149158.Google Scholar
Sumida, P.Y.G., Yoshinaga, M.Y., Madureira, L.A.S.P. & Hovland, M. (2004). Seabed pockmarks associated with deepwater corals off SE Brazilian continental slope, Santos Basin. Mar. Geol. 207, 59167.CrossRefGoogle Scholar
Teixeira, L.C., Peixoto, R.S., Cury, J.C., Sul, W.J., Pellizari, V.H., Tiedje, J. & Rosado, A.S. (2010). Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J. 4, 9891001.CrossRefGoogle ScholarPubMed
Tiedje, J. (1999). Opening the black box of soil microbial diversity. Appl. Soil. Ecol. 13, 109122.Google Scholar
Tosi, L.R.O., Terenzi, H.F. & Jorge, J.A. (1993). Purification and characterization of an extracellular glucoamylase from the thermophilic fungus Humicola grisea var. thermoidea. Can J. Microbiol. 39, 846852.Google Scholar
Vaz, A.B.M., Rosa, L.H., Vieira, M.L.A., Garcia, V., Brandão, L.R., Teixeira, L.C.R.S., Moliné, M., Libkind, D., Van Broock, M. & Rosa, C.A. (2011). The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz. J. Microbiol. 42, 937947.Google Scholar
Vazquez, P., Holguin, G., Puente, M.E., Lopez-Cortes, A. & Bashan, Y. (2000). Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol. Fertil. Soils 30, 460468.Google Scholar
Vishnivetskaya, T.A., Kathariou, S. & Tiedje, J.M. (2009). The Exiguobacterium genus: biodiversity and biogeography. Extremophiles 13, 541555.Google Scholar
Wakao, N., Yasuda, T., Jojima, Y., Yamanaka, S. & Hiraishi, A. (2002). Enhanced growth of Acidocella facilis and related acidophilic bacteria at high concentrations of aluminum. Microb. Environ. 17, 98104.CrossRefGoogle Scholar
Whyte, L.G., Schultz, A., Beilen, J.B., Luz, A.P., Pellizari, V., Labbé, D. & Greer, C.W. (2002). Prevalence of alkane monooxygenase genes in Arctic and Antarctic hydrocarbon-contaminated and pristine soils. FEMS Microbiol. Ecol. 41, 141150.Google Scholar
Xie, W. et al. (2011). Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries. ISME J. 5, 414426.Google Scholar