Potent toxins in Arctic environments: presence of saxitoxins and an unusual microcystin variant in Arctic freshwater ecosystems

Julia Kleinteich, Susanna A Wood, Jonathan Puddick, David Schleheck, Frithjof Christian Kuepper, Daniel Dietrich

Research output: Contribution to journalArticle

25 Citations (Scopus)
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Abstract

Cyanobacteria are the predominant phototrophs in freshwater ecosystems of the polar regions where they commonly form extensive benthic mats. Despite their major biological role in these ecosystems, little attention has been paid to their physiology and biochemistry. An important feature of cyanobacteria from the temperate and tropical regions is the production of a large variety of toxic secondary metabolites. In Antarctica, and more recently in the Arctic, the cyanobacterial toxins microcystin and nodularin (Antarctic only) have been detected in freshwater microbial mats. To date other cyanobacterial toxins have not been reported from these locations. Five Arctic cyanobacterial communities were screened for saxitoxin, another common cyanobacterial toxin, and microcystins using immunological, spectroscopic and molecular methods. Saxitoxin was detected for the first time in cyanobacteria from the Arctic. In addition, an unusual microcystin variant was identified using liquid chromatography-mass spectrometry. Gene expression analyses confirmed the analytical findings, whereby parts of the sxt and mcy operon involved in saxitoxin and microcystin synthesis, were detected and sequenced in one and five of the Arctic cyanobacterial samples, respectively. The detection of these compounds in the cryosphere improves the understanding of the biogeography and distribution of toxic cyanobacteria globally. The sequences of sxt and mcy genes provided from this habitat for the first time may help to clarify the evolutionary origin of toxin production in cyanobacteria.

Original languageEnglish
Pages (from-to)423-431
Number of pages9
JournalChemico-Biological Interactions
Volume206
Issue number2
Early online date3 May 2013
DOIs
Publication statusPublished - 25 Nov 2013

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Ecosystems
Biochemistry
Liquid chromatography
Physiology
Metabolites
Gene expression
Mass spectrometry
Genes
Cyanobacteria

Keywords

  • Arctic Regions
  • Bacterial Proteins
  • Chromatography, High Pressure Liquid
  • Cyanobacteria
  • Ecosystem
  • Enzyme-Linked Immunosorbent Assay
  • Fresh Water
  • Mass Spectrometry
  • Microcystins
  • Phylogeny
  • RNA, Messenger
  • RNA, Ribosomal, 16S
  • Saxitoxin
  • Gene Analysis
  • Cyanobacterial mats
  • Arctic
  • climate change

Cite this

Potent toxins in Arctic environments : presence of saxitoxins and an unusual microcystin variant in Arctic freshwater ecosystems. / Kleinteich, Julia; Wood, Susanna A; Puddick, Jonathan; Schleheck, David; Kuepper, Frithjof Christian; Dietrich, Daniel.

In: Chemico-Biological Interactions, Vol. 206, No. 2, 25.11.2013, p. 423-431.

Research output: Contribution to journalArticle

Kleinteich, Julia ; Wood, Susanna A ; Puddick, Jonathan ; Schleheck, David ; Kuepper, Frithjof Christian ; Dietrich, Daniel. / Potent toxins in Arctic environments : presence of saxitoxins and an unusual microcystin variant in Arctic freshwater ecosystems. In: Chemico-Biological Interactions. 2013 ; Vol. 206, No. 2. pp. 423-431.
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abstract = "Cyanobacteria are the predominant phototrophs in freshwater ecosystems of the polar regions where they commonly form extensive benthic mats. Despite their major biological role in these ecosystems, little attention has been paid to their physiology and biochemistry. An important feature of cyanobacteria from the temperate and tropical regions is the production of a large variety of toxic secondary metabolites. In Antarctica, and more recently in the Arctic, the cyanobacterial toxins microcystin and nodularin (Antarctic only) have been detected in freshwater microbial mats. To date other cyanobacterial toxins have not been reported from these locations. Five Arctic cyanobacterial communities were screened for saxitoxin, another common cyanobacterial toxin, and microcystins using immunological, spectroscopic and molecular methods. Saxitoxin was detected for the first time in cyanobacteria from the Arctic. In addition, an unusual microcystin variant was identified using liquid chromatography-mass spectrometry. Gene expression analyses confirmed the analytical findings, whereby parts of the sxt and mcy operon involved in saxitoxin and microcystin synthesis, were detected and sequenced in one and five of the Arctic cyanobacterial samples, respectively. The detection of these compounds in the cryosphere improves the understanding of the biogeography and distribution of toxic cyanobacteria globally. The sequences of sxt and mcy genes provided from this habitat for the first time may help to clarify the evolutionary origin of toxin production in cyanobacteria.",
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note = "Copyright {\circledC} 2013 Elsevier Ireland Ltd. All rights reserved. We would like to acknowledge the Deutsche Forschungsgemeinschaft (DFG)-funded project DI698/18-1 Dietrich. We are grateful to the TOTAL Foundation (Paris) and the UK Natural Environment Research Council (NERC, WP 4.3 of Oceans 2025 core funding to FCK at the Scottish Association for Marine Science) for funding the expedition to Baffin Island and within this context Olivier Dargent, Nice, France, and Dr. Pieter van West, University of Aberdeen, UK, for collecting and photographing Arctic cyanobacterial communities in Baffin Island. We would also like to thank the Carl Zeiss Stiftung and the Excellence Initiative of the University of Konstanz, Germany, for funding the PhD project of J.K. and APECS (Association of Polar Early Career Scientists) for their educational support. Furthermore, we acknowledge the support of the European Community research infrastructure action under the FP7 ‘capacities’ specific program ASSEMBLE No. 227788. For assistance with the microcystin thiol derivatization we would like to thank Dr. Chris Miles (Norwegian Veterinary Institute, Norway). For technical support and new ideas we are very grateful to Heinke Bastek, Kathrin Leinweber and Lisa Zimmermann from the University of Konstanz, Germany, Martina Sattler, University of Jena, Germany, and Dr. Anne Jungblut from the Natural History Museum, London, UK as well as Wendy Jackson (University of Waikato, New Zealand) for valued technical assistance",
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AU - Puddick, Jonathan

AU - Schleheck, David

AU - Kuepper, Frithjof Christian

AU - Dietrich, Daniel

N1 - Copyright © 2013 Elsevier Ireland Ltd. All rights reserved. We would like to acknowledge the Deutsche Forschungsgemeinschaft (DFG)-funded project DI698/18-1 Dietrich. We are grateful to the TOTAL Foundation (Paris) and the UK Natural Environment Research Council (NERC, WP 4.3 of Oceans 2025 core funding to FCK at the Scottish Association for Marine Science) for funding the expedition to Baffin Island and within this context Olivier Dargent, Nice, France, and Dr. Pieter van West, University of Aberdeen, UK, for collecting and photographing Arctic cyanobacterial communities in Baffin Island. We would also like to thank the Carl Zeiss Stiftung and the Excellence Initiative of the University of Konstanz, Germany, for funding the PhD project of J.K. and APECS (Association of Polar Early Career Scientists) for their educational support. Furthermore, we acknowledge the support of the European Community research infrastructure action under the FP7 ‘capacities’ specific program ASSEMBLE No. 227788. For assistance with the microcystin thiol derivatization we would like to thank Dr. Chris Miles (Norwegian Veterinary Institute, Norway). For technical support and new ideas we are very grateful to Heinke Bastek, Kathrin Leinweber and Lisa Zimmermann from the University of Konstanz, Germany, Martina Sattler, University of Jena, Germany, and Dr. Anne Jungblut from the Natural History Museum, London, UK as well as Wendy Jackson (University of Waikato, New Zealand) for valued technical assistance

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N2 - Cyanobacteria are the predominant phototrophs in freshwater ecosystems of the polar regions where they commonly form extensive benthic mats. Despite their major biological role in these ecosystems, little attention has been paid to their physiology and biochemistry. An important feature of cyanobacteria from the temperate and tropical regions is the production of a large variety of toxic secondary metabolites. In Antarctica, and more recently in the Arctic, the cyanobacterial toxins microcystin and nodularin (Antarctic only) have been detected in freshwater microbial mats. To date other cyanobacterial toxins have not been reported from these locations. Five Arctic cyanobacterial communities were screened for saxitoxin, another common cyanobacterial toxin, and microcystins using immunological, spectroscopic and molecular methods. Saxitoxin was detected for the first time in cyanobacteria from the Arctic. In addition, an unusual microcystin variant was identified using liquid chromatography-mass spectrometry. Gene expression analyses confirmed the analytical findings, whereby parts of the sxt and mcy operon involved in saxitoxin and microcystin synthesis, were detected and sequenced in one and five of the Arctic cyanobacterial samples, respectively. The detection of these compounds in the cryosphere improves the understanding of the biogeography and distribution of toxic cyanobacteria globally. The sequences of sxt and mcy genes provided from this habitat for the first time may help to clarify the evolutionary origin of toxin production in cyanobacteria.

AB - Cyanobacteria are the predominant phototrophs in freshwater ecosystems of the polar regions where they commonly form extensive benthic mats. Despite their major biological role in these ecosystems, little attention has been paid to their physiology and biochemistry. An important feature of cyanobacteria from the temperate and tropical regions is the production of a large variety of toxic secondary metabolites. In Antarctica, and more recently in the Arctic, the cyanobacterial toxins microcystin and nodularin (Antarctic only) have been detected in freshwater microbial mats. To date other cyanobacterial toxins have not been reported from these locations. Five Arctic cyanobacterial communities were screened for saxitoxin, another common cyanobacterial toxin, and microcystins using immunological, spectroscopic and molecular methods. Saxitoxin was detected for the first time in cyanobacteria from the Arctic. In addition, an unusual microcystin variant was identified using liquid chromatography-mass spectrometry. Gene expression analyses confirmed the analytical findings, whereby parts of the sxt and mcy operon involved in saxitoxin and microcystin synthesis, were detected and sequenced in one and five of the Arctic cyanobacterial samples, respectively. The detection of these compounds in the cryosphere improves the understanding of the biogeography and distribution of toxic cyanobacteria globally. The sequences of sxt and mcy genes provided from this habitat for the first time may help to clarify the evolutionary origin of toxin production in cyanobacteria.

KW - Arctic Regions

KW - Bacterial Proteins

KW - Chromatography, High Pressure Liquid

KW - Cyanobacteria

KW - Ecosystem

KW - Enzyme-Linked Immunosorbent Assay

KW - Fresh Water

KW - Mass Spectrometry

KW - Microcystins

KW - Phylogeny

KW - RNA, Messenger

KW - RNA, Ribosomal, 16S

KW - Saxitoxin

KW - Gene Analysis

KW - Cyanobacterial mats

KW - Arctic

KW - climate change

U2 - 10.1016/j.cbi.2013.04.011

DO - 10.1016/j.cbi.2013.04.011

M3 - Article

C2 - 23648386

VL - 206

SP - 423

EP - 431

JO - Chemico-Biological Interactions

JF - Chemico-Biological Interactions

SN - 0009-2797

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ER -