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Heterogeneous vertical structure of the bacterioplankton community in a non-stratified Antarctic lake

Published online by Cambridge University Press:  20 March 2013

Juan A. Villaescusa ,
Emilio O. Casamayor ,
Carlos Rochera ,
Antonio Quesada ,
Luigi Michaud  and
Antonio Camacho
Juan A. Villaescusa
Affiliation:
Departamento de Microbiología y Ecología, Edificio de Investigación “Jeroni Muñoz”, Campus de Burjassot, Universitat de València, E-46100 Burjassot, Spain
Emilio O. Casamayor
Affiliation:
Centro de Estudios Avanzados de Blanes - CEAB.CSIC - C/ d'accés a la Cala St Francesc, 14, E-17300 Blanes, Spain
Carlos Rochera
Affiliation:
Departamento de Microbiología y Ecología, Edificio de Investigación “Jeroni Muñoz”, Campus de Burjassot, Universitat de València, E-46100 Burjassot, Spain
Antonio Quesada
Affiliation:
Departamento de Biologia C/ Darwin, 2 Universidad Autónoma de Madrid, Ciudad Universitaria de Cantoblanco, 28049 Madrid, Spain
Luigi Michaud
Affiliation:
Dipartamento di Biologia Animale ed Ecologia Marina, Università degli Studi di Messina - Piazza Pugliatti, 1 - 98122 Messina, Italia
Antonio Camacho*
Affiliation:
Departamento de Microbiología y Ecología, Edificio de Investigación “Jeroni Muñoz”, Campus de Burjassot, Universitat de València, E-46100 Burjassot, Spain
*
*corresponding author: [email protected]
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Abstract

Bacterial community composition during summer was analysed in surface and bottom waters of the oligotrophic shallow (4.5 m) Lake Limnopolar (Livingston Island, South Shetland Islands, Antarctica), using 16S rRNA gene clone libraries and sequencing. Up to 61% of the 16S rDNA sequences found were closely related to sequences retrieved from lakes, glaciers or polar systems. The distribution of these sequences was not homogeneous, with vertical differences found in both bacterial taxa composition and isolation source of the closest match from GenBank. In the surface sample 86% of the sequences were related to bacteria found in soils, seawater or gut microbiota, probably explained by waterborne transport from the catchment, by wind through sea sprays, or local bird activity. Conversely, in the deep samples, 95% of the sequences were closer to bacteria typically described for lakes, glaciers or polar systems. The presence of benthic mosses covering the bottom of the lake favours a more stable deep layer leading to the existence of this biological heterogeneity through the water column, although the lake does not show physical-chemical stratification in summer. This study illustrates a strong influence of external factors on the microbial ecology of this model Antarctic lake.

Keywords

bacteriabiological stratificationmaritime Antarctic lakesvertical heterogeneity16S rRNA gene
Type
Research Articles
Information
Antarctic Science , Volume 25 , Issue 2: Byers Peninsula – A New Reference Site For The Maritime Antarctic , April 2013 , pp. 229 - 238
Copyright
Copyright © Antarctic Science Ltd 2013

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References

Barberán, A.Casamayor, E.O. 2010. Global phylogenetic community structure and beta-diversity patterns of surface bacterioplankton metacommunities. Aquatic Microbial Ecology, 59, 1–10.CrossRefGoogle Scholar
Barberán, A.Casamayor, E.O. 2011. Euxinic freshwater hypolimnia promote bacterial endemicity in continental areas. Microbial Ecology, 61, 465–472.CrossRefGoogle ScholarPubMed
Bell, E.M.Laybourn-Parry, J. 1999. Annual plankton dynamics in an Antarctic saline lake. Freshwater Biology, 41, 507–519.CrossRefGoogle Scholar
Bosshard, P.P., Santini, Y., Grüter, D., Stettler, R.Bachofen, R. 1999. Bacterial diversity and community composition in the chemocline of the meromictic alpine Lake Cadagno as revealed by 16S rRNA gene analysis. FEMS Microbiology Ecology, 31, 173–182.CrossRefGoogle Scholar
Butler, H., Atkinson, A.Gordon, M. 2005. Omnivory and predation impact of the calanoid copepod Boeckella popei in a Maritime Antarctic lake. Polar Biology, 28, 815–821.CrossRefGoogle Scholar
Camacho, A. 2006a. Planktonic microbial assemblages and the potential effects of metazooplankton predation on the food web of lakes from the Maritime Antarctica and sub-Antarctic islands. Reviews in Environmental Science and Biotechnology, 5, 167–185.CrossRefGoogle Scholar
Camacho, A. 2006b. On the occurrence and ecological features of deep chlorophyll maxima (DCM) in Spanish stratified lakes. Limnetica, 25, 453–478.CrossRefGoogle Scholar
Duarte, C.M., Agustí, S., Varqué, D., Agawin, N., Felipe, J., Casamayor, E.O.Gasol, J.M. 2005. Experimental test of bacteria-phytoplankton coupling in the Southern Ocean. Limnology and Oceanography, 50, 1844–1854.CrossRefGoogle Scholar
Dumestre, J.F., Casamayor, E.O., Massana, R.Pedrós-Alió, C. 2002. Changes in bacterial and archaeal assemblages in an equatorial river induced by the water eutrophication of Petit Saut dam reservoir (French Guiana). Aquatic Microbial Ecology, 26, 209–221.CrossRefGoogle Scholar
Eiler, A.Bertilsson, S. 2004. Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environmental Microbiology, 6, 1228–1243.CrossRefGoogle ScholarPubMed
Fernández-Valiente, E., Camacho, A., Rochera, C., Rico, E., Vincent, W.F.Quesada, A. 2007. Community structure and physiological characterization of microbial mats in Byers Peninsula, Livingston Island (South Shetland Islands, Antarctica). FEMS Microbiology Ecology, 59, 377–385.CrossRefGoogle Scholar
García-Jurado, F., Jiménez-Gómez, F.Guerrero, F. 2011. Effects of a dry period on the limnological characteristics of a Mediterranean high mountain lake. Limnetica, 30, 5–16.CrossRefGoogle Scholar
Good, I.J. 1953. The population frequencies of species and the estimation of the population parameters. Biometrika, 40, 237–264.CrossRefGoogle Scholar
Hervàs, A.Casamayor, E.O. 2009. High similarity between bacterioneuston and airborne bacterial community compositions in a high mountain lake area. FEMS Microbiology Ecology, 67, 219–228.CrossRefGoogle Scholar
Imura, S., Bando, T., Saito, S., Seto, K.Kanda, H. 2003. Benthic moss pillars in Antarctic lakes. Polar Biology, 22, 137–140.CrossRefGoogle Scholar
Laybourn-Parry, J. 2002. Survival mechanisms in Antarctic lakes. Philosophical Transactions of the Royal Society, B357, 863–869.CrossRefGoogle Scholar
Laybourn-Parry, J. 2009. No place too cold. Science, 324, 1521–1522.CrossRefGoogle ScholarPubMed
Laybourn-Parry, J.Pearce, D. 2007. The biodiversity and ecology of Antarctic lakes: models for evolution. Philosophical Transactions of the Royal Society, B362, 2273–2289.CrossRefGoogle Scholar
Laybourn-Parry, J., Bayliss, P.Ellis-Evans, J.C. 1995. The dynamics of heterotrophic nanoflagellates and bacterioplankton in a large ultra-oligotrophic Antarctic lake. Journal of Plankton Research, 17, 1834–1850.CrossRefGoogle Scholar
Laybourn-Parry, J., Marchant, H.J.Brown, P.E. 1991. The plankton of a large freshwater Antarctic lake. Journal of Plankton Research, 13, 1137–1150.CrossRefGoogle Scholar
Llorens-Marès, T., Auguet, J.C.Casamayor, E.O. 2012. Winter to spring changes in bacterial community composition in the slush layer of a high-mountain lake (Lake Redon, Pyrenees). Environmental Microbiology Reports, 4, 50–56.CrossRefGoogle ScholarPubMed
McKnight, D., Howes, B.L., Taylor, C.D.Goehringer, D.D. 2000. Phytoplankton dynamics in a stably stratified Antarctic lake during winter darkness. Journal of Phycolology, 36, 852–861.CrossRefGoogle Scholar
Michaud, L., Caruso, C., Mangano, S., Interdonato, F., Bruni, V.Lo Giudice, A. 2012. Predominance of Flavobacterium, Pseudomonas and Polaromonas within the prokaryotic community of freshwater shallow lakes in the northern Victoria Land, East Antarctica. FEMS Microbial Ecology, 10.1111/j.1574-6941.2012.01394.x.CrossRefGoogle Scholar
Montecino, V., Pizarro, G., Cabrera, S.Contreras, M. 1991. Spatial and temporal photosynthetic compartments during summer in Antarctic Lake Kitiesh. Polar Biology, 11, 371–377.CrossRefGoogle Scholar
Mosier, A.C., Murray, A.E.Frisen, C.H. 2007. Microbiota within the perennial ice cover of Lake Vida, Antarctica. FEMS Microbiology Ecology, 59, 274–288.CrossRefGoogle ScholarPubMed
Park, J.W., Yoo, J.S.Roh, D.H. 2006. Identification of novel psychrotolerant bacterial strain and production of beta-galactosidase. Misainmurhag Hoiji, 42, 40–46.Google Scholar
Pearce, D.A. 2003. Bacterioplankton community structure in a Maritime Antarctic oligotrophic lake during a period of holomixis, as determined by denaturing gradient gel electrophoresis (DGGE) and fluorescence in situ hybridization (FISH). Microbial Ecology, 46, 92–105.CrossRefGoogle Scholar
Pearce, D.A. 2005. The structure and stability of the bacterioplankton community in Antarctic freshwater lakes, subject to extremely rapid environmental change. FEMS Microbiology Ecology, 53, 61–72.CrossRefGoogle ScholarPubMed
Pearce, D.A.Butler, H.G. 2002. Short-term stability of the microbial community structure in a Maritime Antarctic lake. Polar Biology, 25, 479–487.Google Scholar
Pearce, D.A., Van der Gast, C.J., Lawley, B.Ellis-Evans, J.C. 2003. Bacterioplankton community diversity in a Maritime Antarctic lake, determined by culture-dependent and culture-independent techniques. FEMS Microbiogy Ecology, 45, 59–70.CrossRefGoogle Scholar
Quayle, W.C., Peck, L.S., Peat, H., Ellis-Evans, J.C.Harrigan, P.R. 2002. Extreme responses to climate change in Antarctic lakes. Science, 295, 645.CrossRefGoogle ScholarPubMed
Qu, J.H.Yuan, H.L. 2008. Sediminibacterium salmoneum gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from sediment of a eutrophic reservoir. International Journal of Systematic and Evolutionary Microbiology, 58, 2191–2194.CrossRefGoogle Scholar
Reche, I., Pulido-Villena, E., Morales-Baquero, R.Casamayor, E.O. 2005. Does ecosystem size determine aquatic bacterial richness? Ecology, 86, 1715–1722.CrossRefGoogle Scholar
Rochera, C., Justel, A., Fernández-Valiente, E., Bañón, M., Rico, E., Toro, M., Camacho, A.Quesada, A. 2010. Interannual meteorological variability and its effects on a lake from Maritime Antarctica. Polar Biology, 33, 1615–1628.CrossRefGoogle Scholar
Saitou, N.Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.Google Scholar
Singleton, D.R., Furlong, M.A., Rathbun, S.L.Whitman, W.B. 2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Applied and Environmental Microbiology, 67, 4374–4376.CrossRefGoogle ScholarPubMed
Spring, S., Merkhoffer, B., Weiss, N., Kroppenstedt, R.M., Hippe, H.Stackebrandt, E. 2003. Characterization of novel psychrophilic clostridia from an Antarctic microbial mat: description of Clostridium frigoris sp. nov., Clostridium lacusfryxellense sp. nov., Clostridium bowmanii sp. nov. and Clostridium psychrophilum sp. nov. and reclassification of Clostridium laramiense as Clostridium estertheticum subsp. laramiense subsp. nov. International Journal of Systematic and Evolutionary Microbiology, 53, 1019–1029.CrossRefGoogle ScholarPubMed
Tamames, J., Abellan, J.J., Pignatelli, M., Camacho, A.Moya, A. 2010. Environmental distribution of prokaryotic taxa. BMC Microbiology, 10.1186/1471-2180-10-85.CrossRefGoogle ScholarPubMed
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. Molecular Biology and Evolution, 28, 2731–2739.CrossRefGoogle ScholarPubMed
Thompson, J.D., Higgins, D.G.Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.CrossRefGoogle ScholarPubMed
Toro, M., Camacho, A., Rochera, C., Rico, E., Bañón, M., Fernández-Valiente, E., Marco, E., Justel, A., Avedaño, M.C., Ariosa, Y., Vincent, W.F.Quesada, A. 2007. Limnological characteristics of the freshwater ecosystems of Byers Peninsula, Livingston Island, in Maritime Antarctica. Polar Biology, 30, 635–649.CrossRefGoogle Scholar
Unrein, F., Izaguirre, I., Massana, R., Balagué, V.Gasol, J.M. 2005. Nanoplankton assemblages in Maritime Antarctic lakes: characterization and molecular fingerprinting comparison. Aquatic Microbial Ecology, 40, 269–282.CrossRefGoogle Scholar
Villaescusa, J.A., Casamayor, E.O., Rochera, C., Velázquez, D., Chicote, A., Quesada, A.Camacho, A. 2010. A close link between bacterial community composition and environmental heterogeneity in Maritime Antarctic lakes. International Microbiology, 13, 67–77.Google ScholarPubMed
Wu, X., Xi, W., Ye, W.Yang, H. 2007. Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiology Ecology, 61, 85–96.CrossRefGoogle Scholar
Xing, P., Hahn, M.W.Wu, L.Q. 2009. Low taxon richness of bacterioplankton in high altitude lakes of the eastern Tibetan plateau, with a predominance of Bacteroidetes and Synechococcus spp. Applied and Environmental Microbiology, 75, 7017–7025.CrossRefGoogle ScholarPubMed