Bacterial diversity in a microbial mat colonizing a man-made geothermal spring from Romania

Authors

Keywords:

bacterial diversity, community structure, cyanobacterial mat, hot springs.

Abstract

Some of the oldest evidence of life on Earth comes from microbialites, or biologically induced carbonate deposits. Modern lithified microbial mats are considered analogues to some of the earliest Archaean ecosystems. This study investigated the bacterial diversity in a microbial mat developed on the surface of a hot spring carbonate deposit from Romania. A clone library was constructed and more than 200 partial 16S rRNA gene sequences were obtained. Phylogenetic analysis showed the existence of nine major groups. Gammaproteobacteria, Cyanobacteria and Betaproteobacteria were dominant, comprising 75% of the clone library. Verrucomicrobia, some Cyanobacteria (Phormidium, Oscillatoria and Leptolyngbya), Chloroflexi, Firmicutes and Deltaproteobacteria taxa observed in the investigated mat are common inhabitants of this type of environments. Arthrospira platensis and Desertifilum tharense (Cyanobacteria) were described for the first time in association with a geothermal habitat. Also, the representatives of Gammaproteobacteria, Betaproteobacteria, Bacteroidetes and Chrysiogenetes identified in the mat have not been described in geothermal habitats, but are known to prevail in saline, neutral to alkaline environments.

Author Biographies

Cecilia M. CHIRIAC, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: cristian.coman@icbcluj.ro

Taxonomy and Ecology, Algology, National Institute of Research and Development for Biological Sciences, Institute of Biological Research, Cluj-Napoca, Romania

Molecular Biology and Biotechnology Department, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: cristian.coman@icbcluj.ro

Lucian BARBU-TUDORAN, Babeș -Bolyai University, Cluj-Napoca, Romania. Email: lucian.barbu@itim-cj.ro

Electron Microscopy Center, Faculty of Biology and Geology, Babeș -Bolyai University, Cluj-Napoca, Romania. Email: lucian.barbu@itim-cj.ro

Andreea BARICZ, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: andreea.baricz@icbcluj.ro

Taxonomy and Ecology, Algology, National Institute of Research and Development for Biological Sciences, Institute of Biological Research, Cluj-Napoca, Romania

Molecular Biology and Biotechnology Department, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: andreea.baricz@icbcluj.ro

Edina SZEKERES, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: edina.szekeres@icbcluj.ro

Taxonomy and Ecology, Algology, National Institute of Research and Development for Biological Sciences, Institute of Biological Research, Cluj-Napoca, Romania

Molecular Biology and Biotechnology Department, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: edina.szekeres@icbcluj.ro

Tiberiu SZOKE-NAGY, aculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: cristian.coman@icbcluj.ro

Taxonomy and Ecology, Algology, National Institute of Research and Development for Biological Sciences, Institute of Biological Research, Cluj-Napoca, Romania

Molecular Biology and Biotechnology Department, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: cristian.coman@icbcluj.ro

Nicolae DRAGOȘ, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: cristian.coman@icbcluj.ro

Taxonomy and Ecology, Algology, National Institute of Research and Development for Biological Sciences, Institute of Biological Research, Cluj-Napoca, Romania

Molecular Biology and Biotechnology Department, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: cristian.coman@icbcluj.ro

Cristian COMAN

Taxonomy and Ecology, Algology, National Institute of Research and Development for Biological Sciences, Institute of Biological Research, Cluj-Napoca, Romania

Molecular Biology and Biotechnology Department, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania. Email: cristian.coman@icbcluj.ro

References

Akhwale, J.K., Göker, M., Rohde, M., Schumann, P., Klenk, H.P., Boga, H.I. (2015) Belliella kenyensis sp. nov., isolated from the alkaline Lake Elmenteita in the African Rift Valley, ISME J., 65(2), 457-462

Allwood, A.C., Grotzinger, J.P., Knoll, A.H., Burch, I.W., Anderson, M.S., Coleman, M.L., Kanik, I. (2009) Controls on development and diversity of Early Archean stromatolites, Proc. Natl. Acad. Sci. USA, 106(24): 9548–9555

Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J. (1990) Basic local alignment search tool, J. Mol. Biol., 215(3), 403–410

Antics, M., Rosca, M. (2003) Geothermal development in Romania, Geothermics, 32, 361-370

Antony, C.P., Kumaresan, D., Hunger, S., Drake, H.L., Murrell, J.C., Shouche, Y.S. (2013) Microbiology of Lonar Lake and other soda lakes, ISME J., 7(3), 468–476

Badger, M.R., Price, G.D., Long, B.M., Woodger, F.J. (2006) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism, J. Exp. Bot., 57(2), 249–265

Baumgartner, L.K., Reid, R.P., Dupraz, C., Decho, W., Buckley, D.H., Spear, J.R., Przekop, K.M., Visscher, P.T. (2006) Sulfate reducing bacteria in microbial mats: Changing paradigms, new discoveries, Sediment Geol., 185, 131-145

Bohorquez, 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, Environ. Microbiol., 63(1), 103-115

Bolhuis, H., Stal, L.J. (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing, ISME J., 5(11), 1701–1712

Boomer, S.M., Pierson, B.K., Austinhirst, R, Castenholz, R. W. (2000) Characterization of novel bacteriochlorophyll-a-containing red filaments from alkaline hot springs in Yellowstone National Park, Arch. Microbiol., 174(3), 152-161

Boyer, S.L., Johansen, J.R., Flechtner, V.R., Howard, G.L., Bliss, F. (2002) Phylogeny and genetic variance in terrestrial Microcoleus (Cyanophyceae) species based on sequence analysis of the 16S rRNA gene and associated 16S-23S ITS region, J. Phycol., 38(6), 1222-1235

Brettar, I., Christen, R., Höfle, M. (2004) Belliella baltica gen. nov., sp. nov., a novel marine bacterium of the Cytophaga-Flavobacterium-Bacteroides group isolated from surface water of the central Baltic Sea, Int. J. Syst. Evol. Microbiol., 54(1), 65-70

Bryanskaya, A.V., Namsaraev, Z.B., Kalashnikova, O.M., Barkhutova, D.D., Namsaraev, B. B., Gorlenko, V. M. (2006) Biogeochemical processes in the algal–bacterial mats of the Urinskii alkaline hot spring, Microbiology, 75(5), 611-620

Chacon, B.E. (2010) Microbial mats as a source of biosignatures, In: Microbial Mats: Modern and Ancient Microorganisms in Stratified Systems, Seckach, J., Oren, A. (ed), Cellular Origin, Life in Extreme Habitats and Astrobiology 14. Springer Science Business Media B.V, pp 149–181

Charpy, L., Palinska, K.A., Casareto, B., Langlade, M.J., Suzuki, Y., Abed, R.M.M., Golubic, S. (2010) Dinitrogen-fixing cyanobacteria in microbial mats of two shallow coral reef ecosystems, Microb. Ecol., 59(1), 174–186

Chen, Y., Wu, L., Boden, R., Hillebrand, A., Kumaresan, D., Moussard H.H., Baciu, M., Lu, Y., Murrell, J.C. (2009) Life without light: microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave, ISME J., 3, 1093–1104

Coman, C., Bica, A., Drugă, B., Barbu-Tudoran, L., Dragoş, N. (2011) Methodological constraints in the molecular biodiversity study of a thermomineral spring cyanobacterial mat: a case study, Anton. Leeuw. Int. J. G., 99(2), 271-281

Coman, C., Bica, A., Drugă, B., Barbu-Tudoran, L., Dragoş, N. (2012) A microbial mat developed around a man-made geothermal spring from Romania: structure and cyanobacterial composition, In: Microbial mats in siliciclastic depositional systems through time, Noffke, N., Chafetz, H. (ed), SEPM (Society for Sedimentary Geology) special publication 101, pp 47–53

Couradeau, E., Benzerara, K., Moreira, D., Gérard, E., Kaźmierczak, J., Tavera, R., López-García, P. (2011) Prokaryotic and Eukaryotic Community Structure in Field and Cultured Microbialites from the Alkaline Lake Alchichica (Mexico), PLoS ONE, 6(12), e28767

Dadheech, P.K., Abed, R.M.M., Mahmoud, H., Mohan, M.K., Krienitz, L. (2012) Polyphasic characterization of cyanobacteria isolated from desert crusts, and the description of Desertifilum tharense gen. et sp. nov. (Oscillatoriales), Phycologia, 51(3), 260-270

Dupraz, C., Visscher, P.T. (2005) Microbial lithification in marine stromatolites and hypersaline mats, Trends Microbiol, 13, 429–438

Fujisawa, T., Narikawa, R., Okamoto, S., Ehira, S., Yoshimura, H., Suzuki, I., Masuda, T., Mochimaru, M., Takaichi, S., Awai, K., Sekine, M., Horikawa, H., Yashiro, I., Omata, S., Takarada, H., Katano, Y., Kosugi, H., Tanikawa, S., Ohmori, K., Sato, N., Ikeuchi, M., Fujita, N., Ohmori, M. (2010) Genomic structure of an economically important cyanobacterium, Arthrospira (Spirulina) platensis NIES-39, DNA Res., 17(2), 85-103

Garcia-Pichel, F. (2002). Desert environments: biological soil crusts, In: Encyclopedia of Environmental Microbiology, Bitton, G. (ed), New York, pp 1019–1023

Guindon, S., Gascuel, O. (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood, Syst. Biol., 52(5), 696-704

Hamamura, N., Liu, Y., Inskeep, W.P. (2012) Identification of bacterial community and arsenate-reducing bacteria associated with a soda lake in Khovsgol, Mongolia, In: Interdisciplinary Studies on Environmental Chemistry - Environmental Pollution and Ecotoxicology, Kawaguchi, M., Misaki, K., Sato, H., Yokokawa, T., Itai, T., Nguyen, T.M., Ono, J., Tanabe, S. (ed), Terrapub, Tokyo, pp 99-107

Huang, Q., Dong, C.Z., Dong, R.M., Jiang, H., Wang, S., Wang, G., Fang, B., Ding, X., Niu, L., Li, X., Zhang, C., Dong, H. (2011) Archaeal and bacterial diversity in hot springs on the Tibetan Plateau, China, Extremophiles, 15(5), 549-563

Huber, T., Faulkner, G., Hugenholtz, P. (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments, Bioinformatics, 20(14), 2317-2319

Jaspers, E., Overmann, J. (2004) Ecological significance of microdiversity:identical 16S rRNA gene sequences can be found in Bacteria with highly divergent genomes and ecophysiologies, Appl. Environ. Microbiol., 70(8), 4831–4839

Jørgensen, B.B., Nelson, C.N. (1988) Bacterial zonation, photosynthesis, and spectral light distrbution in hot spring mirobial mats of Iceland, Microbial Ecol., 16(2), 133-147

Kanokratana, P., Chanapan, S., Pootanakit, K., Eurwilaichitr, L. (2004) Diversity and abundance of bacteria and archaea in the Bor Khlueng hot spring in Thailand, J. Basic Microbiol., 44(6), 430-444

Kasting, J.K., Howard, M.T. (2006) Atmospheric composition and climate on the early Earth, Philos. T. R. Soc. B., 361(1473), 1733–1742

Kim, B.H. (1999) Ecology of a cyanobacterial mat community in a Korean thermal wastewater stream, Aquat. Ecol., 33(4), 331–338

Konhauser, K. (2007) Introduction to Geomicrobiology, Blackwell Publishing.

Lane, D.J. (1991) 16S/23S rRNA sequencing, In: Nucleic acid techniques in bacterial systematics, Stackebrandt, E., Goodfellow, M. (ed). Wiley, New York, pp 115–175

Mobberley, J.M., Ortega, M.C., Foster, J.S. (2012) Comparative microbial diversity analyses of modern marine thrombolitic mats by barcoded pyrosequencing, Environ. Microbiol., 14(1), 82–100

Mwirichia, R., Cousin, S., Muigai, A.W., Boga, H.I., Stackebrandt, E. (2011) Bacterial diversity in the haloalkaline Lake Elmenteita, Kenya, Curr. Microbiol., 62(1), 209-221

Noffke, N., Beukes, N., Bower, D., Hazen, R.M., Swift, D.J.P. (2008) An actualistic perspective into Archean worlds-(cyano-)bacterially induced sedimentary structures in the siliciclastic Nhlazatse Section, 2.9 Ga Pongola Supergroup, South Africa, Geobiology, 6(1), 5-20

Pagaling, E., Grant, W.D., Cowan, D.A., Jones, B.E., Ma, Y., Ventosa, A., Heaphy, S. (2012) Bacterial and archaeal diversity in two hot spring microbial mats from the geothermal region of Tengchong, China, Extremophiles, 16(4), 607-618

Portillo, M.C., Sririn, V., Kanoksilapatham, W., Gonzalez, J.M. (2009) Differential microbial communities in hot spring mats from Western Thailand, Extremophiles, 13(2), 321–331

Posada, D. (2003) jModelTest: Phylogenetic model averaging, Mol. Evol. Biol., 25(7), 1253-1256

Rauschenbach, I., Narasingarao, P., Häggblom, M.M. (2011) Desulfurispirillum indicum sp. nov., a selenate- and selenite-respiring bacterium isolated from an estuarine canal, Int. J. Syst. Evol. Microbiol., 61(3), 654-658

Reinhold-Hurek, B., Hurek, T., Gillis, M., Hoste, B., Vancanneyt, M., Kersters, K., De Ley, J. (1993) Azoarcus gen. nov., nitrogen-fixing Proteobacteria associated with roots of Kallar Grass (Leptochloa fusca (L.) Kunth), and description of two species, Azoarcus indigens sp. nov. and Azoarcus communis sp. nov, Int. J. Syst. Bacteriol., 43(3), 574-584

Saha, P., Krishnamurthi, S., Mayilraj, S., Prasad, G.S., Bora, T.C., Chakrabarti, T. (2005) Aquimonas voraii gen. nov., sp. nov., a novel gammaproteobacterium isolated from a warm spring of Assam, India, Int. J. Syst. Evol. Microbiol., 55(4), 1491–1495

Sharp, C.E., Stott, M.B., Dunfield, P.F. (2012) Detection of autotrophic verrucomicrobial methanotrophs in a geothermal environment using stable isotope probing, Front. Microbio., 3(303), 1-9

Sompong, U., Anuntalabhochai, S., Cutler, R.W., Castenholz, R.W., Peerapornpisal, Y. (2008) Morphological and phylogenic diversity of cyanobacterial populations in six hot springs of Thailand, ScienceAsia, 34(3), 153-162

Song, Z., Jiang, H., Zhi, X., Zhang, C., Dong, H., Li, W. (2009) Actinobacterial diversity in hot springs in Tengchong (China), Kamchatka (Russia), and Nevada (USA), Geomicrobiol. J., 26(4), 256–263

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods, Mol. Biol. Evol., 28(10), 2731-2739

Ţenu, A., Constantinescu, T., Davidescu, F., Nuti, S., Noto, P., Squarci, P. (1981) Research on the thermal waters of the Western Plain of Romania, Geothermics, 10(1), 1-28

Wacey, D. (2009) Early Life on Earth; A Practical Guide. Springer Science Business Media, pp 47-50

Ward, D.M., Ferris, M.J., Nold, S.C., Bateson, M.M. (1998) A natural view of microbial biodiversity within hot spring cyanobacterial mat communities, Microbiol. Mol. Biol. R., 62(4), 1353–1370

Whitton, B.A., Potts, M., 2000, The Ecology of Cyanobacteria: Their Diversity in Time and Space. Springer Netherlands, pp 505-522

Yanan, Y., Breitbart, M., McNairnie, P., Rohwer, F. (2006) FastGroupII: A web-based bioinformatics platform for analyses of large 16S rDNA libraries, BMC Bioinformatics, 7, 57

Downloads

Published

2015-06-22

How to Cite

CHIRIAC, C. M., BARBU-TUDORAN, L., BARICZ, A., SZEKERES, E., SZOKE-NAGY, T., DRAGOȘ, N., & COMAN, C. (2015). Bacterial diversity in a microbial mat colonizing a man-made geothermal spring from Romania. Studia Universitatis Babeș-Bolyai Biologia, 60(1), 5–22. Retrieved from http://193.231.18.162/index.php/subbbiologia/article/view/4556

Issue

Section

Articles

Most read articles by the same author(s)