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Diversity of toxin and non-toxin containing cyanobacterial mats of meltwater ponds on the Antarctic Peninsula: a pyrosequencing approach

Part of: Antarctic Science International Bursary collection: Biosciences

Published online by Cambridge University Press:  14 May 2014

J. Kleinteich ,
F. Hildebrand ,
S.A. Wood ,
S. Ciŕs ,
R. Agha ,
A. Quesada ,
D.A. Pearce ,
P. Convey ,
F.C. K̈pper  and
D.R. Dietrich
J. Kleinteich
Affiliation:
Human and Environmental Toxicology, University of Konstanz, 78457 Konstanz, Germany Centre d’Ingéniérie des Protéines, Institute of Chemistry B6, University of Liège, B-4000 Liège, Belgium
F. Hildebrand
Affiliation:
European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany Department of Bioscience Engineering, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium
S.A. Wood
Affiliation:
Cawthron Institute, Nelson 7042, New Zealand School of Biological Sciences, University of Waikato, Hamilton 2001, New Zealand
S. Ciŕs
Affiliation:
Departamento de Biología, Universidad Autónoma de Madrid, E-28049 Madrid, Spain School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia
R. Agha
Affiliation:
Departamento de Biología, Universidad Autónoma de Madrid, E-28049 Madrid, Spain
A. Quesada
Affiliation:
Departamento de Biología, Universidad Autónoma de Madrid, E-28049 Madrid, Spain
D.A. Pearce
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK Faculty of Health and Life Sciences, University of Northumbria, Newcastle Upon Tyne NE1 8ST, UK University Centre in Svalbard, N-9171 Longyearbyen, Norway
P. Convey
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK Gateway Antarctica, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand
F.C. K̈pper
Affiliation:
Scottish Association for Marine Science, Oban PA37 1QA, UK Oceanlab, University of Aberdeen, Main Street, Newburgh AB41 6AA, UK
D.R. Dietrich*
Affiliation:
Human and Environmental Toxicology, University of Konstanz, 78457 Konstanz, Germany
*
*[email protected]
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Abstract

Despite their pivotal role as primary producers, there is little information as to the diversity and physiology of cyanobacteria in the meltwater ecosystems of polar regions. Thirty cyanobacterial mats from Adelaide Island, Antarctica were investigated using 16S rRNA gene pyrosequencing and automated ribosomal intergenic spacer analysis, and screened for cyanobacterial toxins using molecular and chemical approaches. A total of 274 operational taxonomic units (OTUs) were detected. The richness ranged between 8 and 33 cyanobacterial OTUs per sample, reflecting a high mat diversity. Leptolyngbya and Phormidium (c. 55% and 37% of the OTUs per mat) were dominant. Cyanobacterial community composition was similar between mats, particularly those obtained from closely adjacent locations. The cyanotoxin microcystin was detected in 26 of 27 mats (10–300 ng g-1 organic mass), while cylindrospermopsin, detected for the first time in Antarctica, was present in 21 of 30 mats (2–156 ng g-1 organic mass). The latter was confirmed via liquid chromatography-mass spectrometry and by the presence of the cyrAB and cyrJ genes. This study demonstrates the usefulness of pyrosequencing for characterizing diverse cyanobacterial communities, and confirms that cyanobacteria from extreme environments produce a similar range of cyanotoxins as their temperate counterparts.

Keywords

automated ribosomal intergenic spacer analysiscylindrospermopsinliquid chromatography-mass spectrometrymicrocystin
Type
Biological Sciences
Information
Antarctic Science , Volume 26 , Supplement 5 , October 2014 , pp. 521 - 532
Copyright
© Antarctic Science Ltd 2014 

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References

Anderson, M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46.Google Scholar
Bahl, J., Lau, M.C.Y., Smith, G.J.D., Vijaykrishna, D., Cary, S.C., Lacap, D.C., Lee, C.K. et al. 2011. Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nature Communications, 2, 10.1038/ncomms1167.Google Scholar
Benjamini, Y. & Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B - Methodological, 57, 289–300.Google Scholar
Chorus, I. & Bartram, J., eds. 1999. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. London: E & FN Spon, 432 pp.Google Scholar
Cirés, S., Wörmer, L., Timón, J., Wiedner, C. & Quesada, A. 2011. Cylindrospermopsin production and release by the potentially invasive cyanobacterium Aphanizomenon ovalisporum under temperature and light gradients. Harmful Algae, 10, 668–675.Google Scholar
Davis, T.W., Berry, D.L., Boyer, G.L. & Gobler, C.J. 2009. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of microcystis during cyanobacteria blooms. Harmful Algae, 8, 715–725.Google Scholar
Dietrich, D.R., Fischer, A., Michel, C. & Hoeger, S. 2008. Toxin mixture in cyanobacterial blooms – a critical comparison of reality with current procedures employed in human health risk assessment. In Hudnell, H.K., ed. Cyanobacterial harmful algal blooms: state of the science and research needs. New York, NY: Springer, 885–912.Google Scholar
Edgar, R.C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460–2461.Google Scholar
Ernst, B., Hitzfeld, B. & Dietrich, D. 2001. Presence of Planktothrix sp. and cyanobacterial toxins in Lake Ammersee, Germany and their impact on whitefish (Coregonus lavaretus L.). Environmental Toxicology, 16, 483–488.Google Scholar
Hildebrand, F., Ebersbach, T., Nielsen, H.B. et al. 2012. A comparative analysis of the intestinal metagenomes present in guinea pigs (Cavia porcellus) and humans (Homo sapiens). BMC Genomics, 13, 10.1186/1471-2164-13-514.Google Scholar
Hildebrand, F., Nguyen, T.L.A., Brinkman, B., Yunta, R.G., Cauwe, B., Vandenabeele, P., Liston, A. & Raes, J. 2013. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biology, 14, 10.1186/gb-2013-14-1-r4.Google Scholar
Hitzfeld, B.C., Lampert, C.S., Späth, N., Mountfort, D., Kaspar, H. & Dietrich, D.R. 2000. Toxin production in cyanobacterial mats from ponds on the McMurdo Ice Shelf, Antarctica. Toxicon, 38, 1731–1748.Google Scholar
Jungblut, A.D., Lovejoy, C. & Vincent, W.F. 2010. Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME Journal, 4, 191–202.Google Scholar
Jungblut, A.D., Wood, S.A., Hawes, I., Webster-Brown, J. & Harris, C. 2012. The Pyramid Trough Wetland: environmental and biological diversity in a newly created Antarctic protected area. FEMS Microbiology Ecology, 82, 356–366.Google Scholar
Jungblut, A.D., Hoeger, S.J., Mountfort, D., Hitzfeld, B.C., Dietrich, D.R. & Neilan, B.A. 2006. Characterization of microcystin production in an Antarctic cyanobacterial mat community. Toxicon, 47, 271–278.Google Scholar
Kaplan, A., Harel, M., Kaplan-Levy, R.N., Hadas, O., Sukenik, A. & Dittmann, E. 2012. The languages spoken in the water body (or the biological role of cyanobacterial toxins). Frontiers in Microbiology, 3, 10.3389/fmicb.2012.00138.Google Scholar
Kleinteich, J., Wood, S.A, Puddick, J., Schleheck, D., Küpper, F.C. & Dietrich, D. 2013. Potent toxins in Arctic environments: presence of saxitoxins and an unusual microcystin variant in Arctic freshwater ecosystems. Chemico-Biological Interactions, 206, 423–431.Google Scholar
Kleinteich, J., Wood, S.A., Küpper, F.C., Camacho, A., Quesada, A., Frickey, T. & Dietrich, D.R. 2012. Temperature-related changes in polar cyanobacterial mat diversity and toxin production. Nature Climate Change, 2, 356–360.Google Scholar
Lee, C.K., Herbold, C.W., Polson, S.W., Wommack, K.E., Williamson, S.J., McDonald, I.R. & Cary, S.C. 2012. Groundtruthing next-gen sequencing for microbial ecology-biases and errors in community structure estimates from PCR amplicon pyrosequencing. PloS ONE, 7, 10.1371/journal.pone.0044224.Google Scholar
Magalhães, C., Stevens, M.I., Cary, S.C., Ball, B.A., Storey, B.C., Wall, D.H., Türk, R. & Ruprecht, U. 2012. At limits of life: multidisciplinary insights reveal environmental constraints on biotic diversity in Continental Antarctica. PloS ONE, 7, 10.1371/journal.pone.0044578.Google Scholar
Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.Google Scholar
Mazmouz, R., Chapuis-Hugon, F., Mann, S., Pichon, V., Méjean, A. & Ploux, O. 2010. Biosynthesis of cylindrospermopsin and 7-epicylindrospermopsin in Oscillatoria sp. strain PCC 6506: identification of the cyr gene cluster and toxin analysis. Applied and Environmental Microbiology, 76, 4943–4949.Google Scholar
McDonald, D., Price, M.N., Goodrich, J., Nawrocki, E.P., DeSantis, T.Z., Probst, A., Andersen, G.L., Knight, R. & Hugenholtz, P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME Journal, 6, 610–618.Google Scholar
Michaud, A.B., Šabacká, M. & Priscu, J.C. 2012. Cyanobacterial diversity across landscape units in a polar desert: Taylor Valley, Antarctica. FEMS Microbiology Ecology, 82, 268–278.Google Scholar
Murray, S.A., Mihali, T.K. & Neilan, B.A. 2011. Extraordinary conservation, gene loss, and positive selection in the evolution of an ancient neurotoxin. Molecular Biology and Evolution, 28, 1173–1182.Google Scholar
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H. & Wagner, H. 2012. vegan: community ecology package. Available at: http://cran.r-project.org/package=vegan.Google Scholar
Pearce, D.A, Newsham, K.K., Thorne, M.A.S., Calvo-Bado, L., Krsek, M., Laskaris, P., Hodson, A. & Wellington, E.M. 2012. Metagenomic analysis of a southern Maritime Antarctic soil. Frontiers in Microbiology, 3, 10.3389/fmicb.2012.00403.Google Scholar
Pearson, L., Mihali, T., Moffitt, M., Kellmann, R. & Neilan, B. 2010. On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Marine Drugs, 8, 1650–1680.Google Scholar
Rantala, A., Fewer, D.P., Hisbergues, M., Rouhiainen, L., Vaitomaa, J., Börner, T. & Sivonen, K. 2004. Phylogenetic evidence for the early evolution of microcystin synthesis. Proceedings of the National Academy of Sciences of the United States of America, 101, 568–573.Google Scholar
Seifert, M., McGregor, G., Eaglesham, G., Wickramasinghe, W. & Shaw, G. 2007. First evidence for the production of cylindrospermopsin and deoxy-cylindrospermopsin by the freshwater benthic cyanobacterium, Lyngbya wollei (Farlow ex Gomont) Speziale and Dyck. Harmful Algae, 6, 73–80.Google Scholar
Sinha, R., Pearson, L.A., Davis, T.W., Burford, M.A., Orr, P.T. & Neilan, B.A. 2012. Increased incidence of Cylindrospermopsis raciborskii in temperate zones – is climate change responsible? Water Research, 46, 1408–1419.Google Scholar
Tamura, K. & Nei, M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.Google Scholar
Tang, E.P.Y., Tremblay, R. & Vincent, W.F. 1997. Cyanobacterial dominance of polar freshwater ecosystems: are high-latitude mat-formers adapted to low temperature? Journal of Phycology, 33, 171–181.Google Scholar
Taton, A., Grubisic, S., Balthasart, P., Hodgson, D.A., Laybourn-Parry, J. & Wilmotte, A. 2006. Biogeographical distribution and ecological ranges of benthic cyanobacteria in East Antarctic lakes. FEMS Microbiology Ecology, 57, 272–289.Google Scholar
Velázquez, D., Rochera, C., Camacho, A. & Quesada, A. 2011. Temperature effects on carbon and nitrogen metabolism in some Maritime Antarctic freshwater phototrophic communities. Polar Biology, 34, 1045–1055.Google Scholar
Vincent, W.F. & Quesada, A. 2012. Cyanobacteria in high latitude lakes, rivers and seas. In Whitton, B.A., ed. Ecology of cyanobacteria II: their diversity in space and time. Dordrecht: Springer, 371–385.Google Scholar
Wood, S.A., Rueckert, A., Cowan, D. & Cary, S.C. 2008b. Sources of edaphic cyanobacterial diversity in the Dry Valleys of Eastern Antarctica. ISME Journal, 2, 308–320.Google Scholar
Wood, S.A., Rasmussen, J.P., Holland, P.T., Campbell, R. & Crowe, A.L.M. 2007. First report of the cyanotoxin anatoxin-A from Aphanizomenon issatschenkoi (cyanobacteria). Journal of Phycology, 43, 356–365.Google Scholar
Wood, S.A., Mountfort, D., Selwood, A.I., Holland, P.T., Puddick, J. & Cary, S.C. 2008a. Widespread distribution and identification of eight novel microcystins in Antarctic cyanobacterial mats. Applied and Environmental Microbiology, 74, 7243–7251.Google Scholar
Wörmer, L., Cirés, S., Carrasco, D. & Quesada, A. 2008. Cylindrospermopsin is not degraded by co-occurring natural bacterial communities during a 40-day study. Harmful Algae, 7, 206–213.Google Scholar
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