Abstract
Terrestrial saline springs are habitats of a high diversity of microbial species, but knowledge of this diversity is scarce in our country. We have chosen to study three saline springs as part of our research program on the ecology and diversity of halophilic and thermophilic microorganisms. The saline springs are located on the Andes mountain range, their content of total dissolved solids is 20-54 g/L, they flow from ancient groundwater, and their water regime is not directly related to recent rainfall recharges. They exhibited different physicochemical compositions: the water samples from the Salado de Consotá and La Cristalina springs showed a high content of chlorine, sodium and calcium, while those from the Salpa spring were characterized by high concentrations of sodium, potassium and sulfate. The composition of microbial communities was analyzed using different approaches to generate biodiversity inventories. The results indicated that these springs harbor a microbial community made up mostly of Gram-negative, motile, litotrophic, heterotrophic, halotolerant and halophilic microorganisms, some of which have been previously reported in marine environments. Most isolated microorganisms belonged to the Gamma and Alphaproteobacteria classes, but differences in the microbial composition of each spring were evident. Our study revealed that these springs are a source of new taxonomic diversity as shown by the newly characterized bacterial species. © Acad. Colomb. Cienc. Ex. Fis. Nat. 2015.References
Acevedo A, & Martínez S. (2004). La sal y las mercaderías en la provincia de Quimbaya. Primeras noticias y crónicas de los salados del río Consotá. En: C. López y M. Cano (Eds). Cambios ambientales en perspectiva histórica. Ecorregión del Eje Cafetero. Proyecto UTP-GTZ, Pereira. p. 167-187.
Alfaro C. (2002). Geoquímica del sistema geotérmico de Paipa. Ingeominas, informe inédito. Bogotá. p. 88
Alexandre, G., Greer-Phillips, S., Zhulin, I.B. (2004). Ecological role of energy taxis in microorganism. FEMS Microbiol Reviews; 28 (1): 113-126.
Aller, J.Y. & Kemp, P.F. (2008). Are Archaea inherently less diverse than Bacteria in the same environments? FEMS Microbiol Ecol; 65 (1): 74-87.
Andrei, A.S., Banciu, H.L., Oren, A. (2012). Living with salt: Metabolic and phylogenetic diversity of Archaea inhabiting saline ecosystems. FEMS Microbiol Lett 330: 1-9.
American Public Health Association-American Water Works Association & Water Environment Federation. (2005). Standard Methods for the Examination of Water and Wastewater, 21st ed. American Public Health Association, Washington, D.C.
Arbeláez-Cortés, E. (2013). Knowledge of Colombian biodiversity: Published and indexed. Biodivers Conserv; 22 (12): 2875-2906.
Baena, S, Fardeau, M.L., Labat, M., Ollivier, B., García, J.L., Patel B.K.C. (1998). Aminobacterium colombiense gen. nov. sp. nov., an amino acid-degrading anaerobe isolated from anaerobic sludge. Anaerobe. 2: 241-250.
Baena, S., Fardeau, M.L., Woo, T.H.S., Ollivier, B., Labat, M., Patel, B.K.C. (1999a). Phylogenetic relationships of three amino-acid-utilizing anaerobes, Selenomonas acidaminovorans, “Selenomonas acidaminophila” and Eubacterium acidaminophilum, as inferred from partial 16S rDNA nucleotide sequences, and proposal of Thermanaerovibrio acidaminovorans gen. nov., comb. nov. and Anaeromusa acidaminophila gen. nov., comb. nov. Int J Syst Evol Microbiol. 49: 969-974.
Baena, S., Fardeau, M.L., Labat, M., Ollivier, B., Thomas, P., Patel, B.K.C. (1999b) Aminomonas paucivorans gen. nov., sp. nov., a mesophilic, anaerobic, amino-acid utilizing bacterium.Int J Syst Evol Microbiol. 49: 975-982.
Baena, S., Perdomo, N., Carvajal, C., Díaz, C., Patel, B.K.C.(2011). Desulfosoma caldarium gen. nov., sp. nov., a thermophilic sulfate-reducing bacterium from a terrestrial hot spring. Int J Syst Evol Microbiol. 61: 732-736.
Biebl, H., Allgaier, M., Lünsdorf, H., Pukall, R., Tindall, B.J., Wagner-Döbler, I. (2005). Roseovarius mucosus sp. nov., a member of the Roseobacter clade with trace amounts of bacteriochlorophyll a. Int J Syst Evol Microbiol. 55:2377-2383.
Biebl, H., Pukall, D., Lünsdorf, H., Schulz, S., Allgaier, M., Tindall, B., Wagner-Döbler, I. (2007). Description of Labrenzia alexandrii gen. nov., sp. nov., a novel alphaproteobacterium containing bacteriochlorophyll a, and a proposal for reclassification of Stappia aggregataas Labrenzia aggregata comb. nov., of Stappia marinaas Labrenzia marina comb. nov. and of Stappia alba as Labrenzia alba comb. nov., and emended descriptions he genera Pannonibacter, Stappia and Roseibium, and of the species Roseibium denhamense and Roseibium hamelinense. Int J Syst Evol Microbiol. 57: 1095-1107.
Bohórquez, L.C., Delgado-Serrano, L., López, G., Osorio-Forero, C., Klepac-Ceraj, V., Kolter, R., Junca, H., Baena, S., Zambrano, M.M.(2012). In-depth characterization via complementing culture-independent approaches of the microbial community in an acidic hot spring of the Colombian Andes. Microb Ecol. 63: 103-115.
Chun, J. & Rainey, F.A. (2014). Integrating genomics into taxonomic and systematics of the Bacteria and Archaea.Int J Syst Evol Microbiol.64: 316-324.
Clementino, M.M., Vieira, R.P., Cardoso, A.M., Nascimento, A.P.A, Silveira C.B., Riva, T.C., Gonzalez A.S.M., Paranhos, R., Albano, R.M., Ventosa, A., Martins, O.B. (2008). Prokaryotic diversity in one of the largest hypersaline coastal lagoons in the world. Extremophiles. 12: 595-604.
Cortés, L. & Cardona, J.J. (2006). Cartografía geológica detallada para el Salado de Consotá y sus alrededores. En: López, M. Cano y D. Rodríguez (Compiladores). Cambios ambientales en perspectiva histórica. Ecología histórica y cultura ambiental. Universidad Tecnológica de Pereira-Sociedad Colombiana de Arqueología, Pereira. p. 93-109.
Dahle, H., & Birkeland, N.K. (2006). Thermovirga lienii gen. nov., sp. nov., a novel moderately thermophilic, anaerobic, amino-acid-degrading bacterium isolated from a North Sea oil well. Int J Syst Evol Microbiol. 56: 1539-1545.
Delgado-Serrano, L., López, G., Bohórquez, L., Bustos, J.R., Rubiano, C., Osorio-Forero, C., Junca, H., Baena, S., Zambrano, M.M. (2014). Neotropical Andes hot springs harbor diverse and distinct planktonic microbial communities. FEMS Microbiol Ecol.89: 56-66.
Denner, E.B.M, Smith, G.W., Busse, H.J., Schumann, P., Narzt, T., Polson, S.W., Lubitz, W., Richardson, L.L. (2003). Aurantimonas coralicida gen. nov., sp. nov., the causative agent of white plague type II on Caribbean scleractinian corals. Int J Syst Evol Microbiol. 53: 1115-1122.
Díaz, C., Baena, S., Fardeau, M.L., Patel, B.K.C. (2007). Aminiphilus circumscriptus gen. nov., sp. nov., an anaerobic amino-acid-degrading bacterium from an upflow anaerobic sludge reactor.Int J Syst Evol Microbiol. 57: 1914-1918.
Díaz-Cárdenas, C., López, G., Patel, B.K.C., Baena, S. (2010a). Dethiosulfovibrio salsuginis sp. nov., an anaerobic, slightly halophilic bacterium isolated from a saline spring.Int J Syst Evol Microbiol. 60: 850-853.
Díaz-Cárdenas, C., Patel, B.K.C., Baena, S. (2010b) Tistlia consotensis gen. nov., sp. nov., a novel aerobic chemohet-erotrophic free-living nitrogen-fixing α-Proteobacteria, isolated from a Colombian saline spring. Int J Syst Evol Microbiol. 60: 1437-1444.
Díaz-Cárdenas, C. (2011) Estudio de la composición de la comunidad microbiana de manantiales salinos ubicados en los departamentos de Risaralda y Boyacá. Pontificia Universidad Javeriana. Bogotá. p. 255
Dong, H., Zhang, G., Jiang, H., Yu, B., Chapman, L., Lucas, C., Fields, M. (2006). Microbial diversity in sediments of saline Qinghai Lake, China: Linking geochemical controls to microbial ecology. Microbial Ecol. 51: 65-82.
DuRand, M.D., Olson, R.J., Chisholm, S.W. (2001). Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. Deep Sea Res Part II. 48: 1983-2003.
Elshahed, M., Najar, F., Roe, B., Oren, A., Dewers, T., Krumholz, L. (2004). Survey of Archaeal diversity reveals an abundance of halophilic Archaea in a low-salt, sulfide and sulfur-rich spring. Appl Environ Microbiol. 70 (4): 2230-2239.
Gell, P. & Gasse, F. (1990). Relationships between salinity and diatom flora from some Australian saline lakes. 11th International Diatom Symposium. California Academy of Sciences, San Francisco, USA. p. 631-641.
Ganesan, A., Chaussonnerie, S., Tarrade, A., Dauga, C., Bouchez, T., Pelletier, E., Lepaslier, D., Sghir, A.(2008). Cloacibacillus evryensis gen. nov., sp. nov., a novel asaccharolytic, mesophilic, amino-acid-degrading bacterium within the phylum ‘Synergistetes’, isolated from an anaerobic sludge digester. Int J Syst Evol Microbiol. 58: 2003-2012.
Glauert, A.M. (1975). Fixation, dehydration and embedding of biological specimens. En Glauert, A.M., (Ed.): Practical methods in electron microscopy. Vol. 3. Part I. North-Holland, Amsterdam. p. 1-207.
Gremm, T., & Kaplan, L. (1997). Dissolved carbohydrates in streamwater determined by HPLC and pulsed amperometric detection. Limnology and Oceanography. 42 (2): 385-393.
Hungate, R.E. (1969). A roll tube method for cultivation of strict anaerobes. En: Norris, J.R. and Ribbons, D.W. (Eds.). Methods in microbiology, Vol. 3B. Academic Press, London. p. 117-132.
Joshi, A.A., Kanekar, P.P., Kelkar, A.S., Shouche, Y.S., Vani, A.A., Borgave, S.B., Sarnaik, S.S. (2008). Cultivable bacterial diversity of alkaline Lonar Lake, India. Microbial Ecology. 55: 163-172.
Jumas-Bilak, E., Carlier, J.P., Jean-Pierre, H., Citron, D., Bernard, K., Damay, A., Gay, B., Teyssier, C., Campos, J., Marchandin, H. (2007). Jonquetella anthropi gen. nov,. sp. nov., the first member of the candidate phylum ‘Synergistetes’ isolated from man. Int J Syst Evol Microbiol. 57: 2743-2748.
Jumas-Bilak, E., Roudière, L., Marchandin, H. (2009). Description of ‘Synergistetes’ phyl. nov. and emended description of the phylum ‘Deferribacteres’ and of the family Syntrophomonadaceae, phylum ‘Firmicutes’. Int J Syst Evol Microbiol. 59 (5): 1028-35.
Kirchman, D., Sigda, J., Kapuscinski, R., Mitchell, R.(1982). Statistical analysis of the direct count method for enumerating bacteria. Appl Environm Microbiol. 44:376-382.
LaBaugh, JW. (1989). Chemical characteristics of water in northern prairie wetlands. En: Valk AV. Ames (Eds). Northern Prairie Wetlands. Iowa University Press. 57-90.
Lai, Q., Qiao, N., Wu, C., Sun, F., Yuan, J., Shao, Z. (2010). Stappia indica sp. nov., isolated from deep seawater of the Indian Ocean. Int J Syst Evol Microbiol. 60: 733-736.
López, G., Chow, J., Bongen, P., Lauinger, B., Pietruszka, J., Streit, W.R., Baena, S. (2014). A novel thermoalkalostable esterase from Acidicaldus sp. strain USBA-GBX-499 with enantioselectivity isolated from an acidic hot springs of Colombian Andes. Appl Microbiol Biotechnol. 98 (20): 8603-16.
Obernosterer, I. & Herndle, G.J. (1995). Phytoplankton extracellular release and bacterial growth: Dependence on the inorganic N:P ratio. Marine Ecology Progress Series. 116: 247-257.
Pedersen, K., Arlinger, J., Hallbeck, L., Pettersson, C. (1996). Diversity and distribution of subterranean bacteria in groundwater at Oklo in Gabon, Africa, as determined by 16S rRNA gene sequencing. Molecular Ecology. 5:427-436.
Pernthaler, J., Glöckner, F.O., Schönhuber, W., Amann, R.(2001). Fluorescence in situ hybridization with rRNA-targeted oligonucleotide probes. En: J. Paul (Ed.). Methods in microbiology: Marine microbiology. Academic Press Ltd, San Diego, USA. vol. 30. p. 207-226.
Perreault, N.N., Andersen, D.T., Pollard, W.H., Greer, C.W., Whyte, L.G. (2007). Characterization of the prokaryotic diversity in cold saline perennial springs of the Canadian high Arctic. Appl Environ Microbiol. 73 (5): 1532-1543.
Prakash, O., Shouche, Y., Jangid, K., Kostka, J.E. (2013). Microbial cultivation and the role of microbial resource centers in the omics era. Appl Microbiol Biotechnol. 97: 51-62.
Rathsack, K., Reitner, J., Stackebrandt, E., Tindall, B.J.(2011). Reclassification of Aurantimonas altamirensis(Jurado, et al., 2006), Aurantimonas ureilytica (Weon, et al., 2007) and Aurantimonas frigidaquae (Kim, et al., 2008) as members of a new genus, Aureimonasgen. nov., as Aureimonas altamirensis gen. nov., comb. nov., Aureimonas ureilytica comb. nov. and Aureimonas frigidaquae comb. nov., and emended descriptions of the genera Aurantimonas and Fulvimarina. Int J Syst Evol Microbiol. 61: 2722-2728.
Redburn, A.C. & Patel, B.K.C. (1993). Phylogenetic analysis of Desulfotomaculum thermobenzoicum using polymerase chain reaction-amplified 16S rRNA-specific DNA. FEMS Microbiol Letters. 113: 81-86.
Rees, G.N, Patel, B.K.C., Grassia, G.S., Sheehy, A.J. (1997). Anaerobaculum thermoterrenum gen. nov., sp. nov., a novel thermophilic bacterium which ferments citrate. Int J Syst Bacteriol. 47: 150-154.
Romero, M., Cabrera, E., Ortiz, N. (2008). Informe sobre el estado de la biodiversidad en Colombia 2006-2007. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Bogotá D. C., Colombia. p. 181. http://www.humboldt.org.co/download/INSEB_2006-2007.pdf.
Rooney-Varga, J.N., Giewat, M.W., Savin, M.C., Sood, S., LeGresley, M., Martin, J.L. (2005). Links between phytoplankton and bacterial community dynamics in a coastal marine Environment. Microbial Ecology. 49:163-175.
Rubiano-Labrador, C., Baena, S., Díaz-Cárdenas C., Patel, B.K.C. (2013). Caloramator quimbayensis sp. nov., an anaerobic, moderately thermophilic bacterium isolated from a terrestrial hot spring.Int J Syst Evol Microbiol. 63: 1396-1402.
Rubiano-Labrador, C., Bland, C., Miotello, G., Guerin, P., Pible, O., Baena, S., Armengaud, J. (2014). Proteogenomic insights into salt tolerance by a halotolerant alpha-proteobacterium isolated from an Andean saline spring. Journal of Proteomics. 97: 36-47.
Salm C.R., Saros, J.E., Martin, C.S., Erickson, J.M. (2009). Patterns of seasonal phytoplankton distribution in prairie saline lakes of the northern Great Plains (U.S.A.). Saline Systems. 5 (1): 1-13.
Sieburth, J.M., Smetacek, V., Lenz, J. (1978). Pelagic ecosystem structure-heterotrophic compartments of plankton and their relationship to plankton size fractions. Limnology and Oceanography. 23: 1256-1263.
Sigee, D.C. (2005). Freshwater Microbiology: Biodiversity and dynamic interactions of microorganisms in the freshwater environment. Primera edición. John Wiley & Sons Ltd., Inglaterra. p. 524.
Sogin, M., Morrison, H., Huber, J., Welch, D.M., Huse, S., Neal, P.R., Arrieta, J., Herndl, G. (2006). Microbial diversity in the deep sea and the underexplored ‘‘rare biosphere’’. PNAS; 103 (32): 12115-12120.
Sorokin, D.Y., Tourova, T.P., Spiridonova, E.M., Rainey, F.A., Muyzer, G. (2005). Thioclava pacifica gen. nov., sp. nov., a novel facultatively autotrophic, marine, sulfur-oxidizing bacterium from a near-shore sulfidic hydrothermal area. Int J Syst Evol Microbiol; 55: 1069-1075.
Swan, B.K., Ehrhardt, C.J., Reifel, K.M., Moreno, L.I., Valentine, D. (2010). Archaeal and Bacterial communities respond differently to environmental gradients in anoxic sediments of a California hypersaline lake, the Salton Sea. App Environ Microbiol. 76 (3): 757-768.
Tanaka, T., Kawasaki, K., Daimon, S., Kitagawa, W., Yamamoto, K., Tamaki, H., Tanaka, M., Nakatsu, C.H., Kamagata, Y. (2014). A hidden pitfall in the preparation of agar media undermines microorganism cultivability. App Environ Microbiol. 80 (24): 7659-7666.
Tistl M. (2004). Sal, cobre y oro en el Consotá. En: López, C, Cano, M. (Eds.) Cambios ambientales en perspectiva histórica. Ecorregión del Eje Cafetero. Universidad Tecnológica de Pereira, Programa Ambiental GTZ. Pereira, Colombia. p. 41-53.
Torsvik, V., Salte, K., Sørheim, R., Goksøyr, J. (1990). Com-parison of phenotypic diversity and DNA heterogeneity in a population of soil bacteria. Appl Environ Microbiol.56(3): 776-781.
Vartoukian, S., Palmer, R., Wade, W. (2007). The division “Synersgistes”. Anaerobe. 13 (4): 99-106.
Ventosa, A., Fernández, A.B., León, M.J., Sánchez-Porro, C., Rodríguez-Varela F. (2014). The Santa Pola saltern as a model for studying the microbiota of hypersaline environments. Extremophiles. 18: 811-824.
Wu, Q.L., Zwart, G., Schauer, M., Kamst-van Agterveld M.P., Hahn, M.W. (2006). Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan plateau, China. Appl Environ Microbiol. 72: 5478-5485.
Yeates, C., Saunders, A.M., Crocetti, G.R., Blackall, L.L. (2003). Limitations of the widely used GAM42a and BET42a probes targeting bacteria in the Gammaproteobacteria radiation. Microbiology. 149: 1239-1247.
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