CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Environmental Chemistry   
Environmental Chemistry
Journal Banner
  Environmental problems - Chemical approaches
blank image Search
blank image blank image
blank image
  Advanced Search

Journal Home
About the Journal
Editorial Boards
Online Early
Current Issue
Just Accepted
All Issues
Virtual Issues
Special Issues
Research Fronts
Sample Issue
Call for Papers
For Authors
General Information
Notice to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review an Article
For Subscribers
Subscription Prices
Customer Service

blue arrow e-Alerts
blank image
Subscribe to our Email Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube


Open Access Article << Previous     |     Next >>   Contents Vol 11(5)

Biosynthesis of arsenolipids by the cyanobacterium Synechocystis sp. PCC 6803

Xi-Mei Xue A B , Georg Raber C , Simon Foster D , Song-Can Chen B E , Kevin A. Francesconi C F and Yong-Guan Zhu A E F

A Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Jimei District, Xiamen 361021, China.
B University of Chinese Academy of Sciences, 19A Yuquan Road, Shijingshan District, Beijing 100049, China.
C Institute of Chemistry, University of Graz, Universitaetsplatz 1, A-8010 Graz, Austria.
D Institute for Applied Ecology, University of Canberra, Bruce, ACT 2601, Australia.
E State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 18 Shuangqing Road, Haidian District, Beijing 100085, China.
F Corresponding authors. Email: ygzhu@iue.ac.cn; kevin.francesconi@uni-graz.at

Environmental Chemistry 11(5) 506-513 http://dx.doi.org/10.1071/EN14069
Submitted: 1 April 2014  Accepted: 19 May 2014   Published: 16 September 2014

 Full Text
 PDF (427 KB)
 Supplementary Material
 Export Citation

Environmental context. Arsenic biotransformation processes play a key role in the cycling of arsenic in aquatic systems. We show that a freshwater cyanobacterium can convert inorganic arsenic into arsenolipids, and the conversion efficiency depends on the arsenic concentration. The role of these novel arsenic compounds remains to be elucidated.

Abstract. Although methylated arsenic and arsenosugars have been verified in various freshwater organisms, lipid-soluble arsenic compounds have not been identified. Here, we report investigations with the model organism cyanobacterium Synechocystis sp. PCC 6803 wild type and ΔarsM (arsenic(III) S-adenosylmethionine methyltransferase) mutant strain, which lacks the enzymes for arsenic methylation cultured in various concentrations of arsenate (AsV). Although Synechocystis accumulated higher arsenic concentrations at the higher exposure levels, the bioaccumulation factor decreased with increasing AsV. The accumulated arsenic in the cells was partitioned into water-soluble and lipid-soluble fractions; lipid-soluble arsenic was found in Synechocystis wild type cells (3–35 % of the total depending on the level of arsenic exposure), but was not detected in Synechocystis ΔarsM mutant strain showing that ArsM was required for arsenolipid biosynthesis. The arsenolipids present in Synechocystis sp. PCC 6803 were analysed by high performance liquid chromatography–inductively coupled plasma–mass spectrometry, high performance liquid chromatography–electrospray mass spectrometry, and high resolution tandem mass spectrometry. The two major arsenolipids were characterised as arsenosugar phospholipids based on their assigned molecular formulas C47H88O14AsP and C47H90O14AsP, and tandem mass spectrometric data demonstrated the presence of the phosphate arsenosugar and acylated glycerol groups.

Additional keyword: arsenic.


[1]  K. A. Francesconi, Current perspectives in arsenic environmental and biological research. Environ. Chem. 2005, 2, 141.
CrossRef | CAS |

[2]  S. Miyashita, S. Fujiwara, M. Tsuzuki, T. Kaise, Rapid biotransformation of arsenate into oxo-arsenosugars by a freshwater unicellular green alga, Chlamydomonas reinhardtii. Biosci. Biotechnol. Biochem. 2011, 75, 522.
CrossRef | CAS | PubMed |

[3]  S. Miyashita, M. Shimoya, Y. Kamidate, T. Kuroiwa, O. Shikino, S. Fujiwara, K. A. Francesconi, T. Kaise, Rapid determination of arsenic species in freshwater organisms from the arsenic-rich Hayakawa River in Japan using HPLC-ICP-MS. Chemosphere 2009, 75, 1065.
CrossRef | CAS | PubMed |

[4]  S. Miyashita, S. Fujiwara, M. Tsuzuki, T. Kaise, Cyanobacteria produce arsenosugars. Environ. Chem. 2012, 9, 474.
CrossRef | CAS |

[5]  A. Geiszinger, W. Goessler, D. Kuehnelt, K. A. Francesconi, W. Kosmus, Determination of arsenic compounds in earthworms. Environ. Sci. Technol. 1998, 32, 2238.
CrossRef | CAS |

[6]  G. Lunde, Analysis of arsenic in marine oils by neutron activation. Evidence of arseno organic compounds. J. Am. Oil Chem. Soc. 1968, 45, 331.
CrossRef | CAS | PubMed |

[7]  A. Rumpler, S. Edmonds, M. Katsu, K. B. Jensen, W. Goessler, G. Raber, H. Gunnlaugsdottir, K. A. Francesconi, Arsenic-containing long-chain fatty acids in cod-liver oil: a result of biosynthetic infidelity? Angew. Chem. Int. Ed. 2008, 47, 2665.
CrossRef | CAS |

[8]  K. O. Amayo, A. Petursdottir, C. Newcombe, H. Gunnlaugsdottir, A. Raab, E. M. Krupp, J. Feldmann, Identification and quantification of arsenolipids using reversed-phase HPLC coupled simultaneously to high-resolution ICPMS and high-resolution electrospray MS without species-specific standards. Anal. Chem. 2011, 83, 3589.
CrossRef | CAS | PubMed |

[9]  G. Raber, S. Khoomrung, M. S. Taleshi, J. S. Edmonds, K. A. Francesconi, Identification of arsenolipids with GC/MS. Talanta 2009, 78, 1215.
CrossRef | CAS | PubMed |

[10]  U. Arroyo-Abad, J. Mattusch, S. Mothes, M. Möder, R. Wennrich, M. P. Elizalde-González, F. M. Matysik, Detection of arsenic-containing hydrocarbons in canned cod liver tissue. Talanta 2010, 82, 38.
CrossRef | CAS | PubMed |

[11]  M. S. Taleshi, J. S. Edmonds, W. Goessler, M. J. Ruiz-Chancho, G. Raber, K. B. Jensen, K. A. Francesconi, Arsenic-containing lipids are natural constituents of sashimi tuna. Environ. Sci. Technol. 2010, 44, 1478.
CrossRef | CAS | PubMed |

[12]  M. Morita, Y. Shibata, Isolation and identification of arseno-lipid from a brown alga, Undaria pinnatifida (Wakame). Chemosphere 1988, 17, 1147.
CrossRef | CAS |

[13]  S. García-Salgado, G. Raber, R. Raml, C. Magnes, K. A. Francesconi, Arsenosugar phospholipids and arsenic hydrocarbons in two species of brown macroalgae. Environ. Chem. 2012, 9, 63.
CrossRef |

[14]  A. Raab, C. Newcombe, D. Pitton, R. Ebel, J. Feldmann, Comprehensive analysis of lipophilic arsenic species in a brown alga (Saccharina latissima). Anal. Chem. 2013, 85, 2817.
CrossRef | CAS | PubMed |

[15]  T. Kaneko, A. Tanaka, S. Sato, H. Kotani, T. Sazuka, N. Miyajima, M. Sugiura, S. Tabata, Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. I. Sequence features in the 1 Mb region from map positions 64 % to 92 % of the genome. DNA Res. 1995, 2, 153.
CrossRef | CAS | PubMed |

[16]  T. Kaneko, S. Sato, H. Kotani, A. Tanaka, E. Asamizu, Y. Nakamura, N. Miyajima, M. Hirosawa, M. Suquira, S. Sadamoto, T. Kimura, T. Hosouchi, A. Matsuno, A. Muraki, N. Nakazaki, K. Naruo, S. Okumura, S. Shimpo, C. Takeuchi, T. Wada, A. Watanabe, M. Yamada, M. Yasuda, S. Tabata, Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 1996, 3, 109.
CrossRef | CAS | PubMed |

[17]  J. G. Williams, Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol. 1988, 167, 766.
CrossRef | CAS |

[18]  R. Rippka, J. Deruelles, J. B. Waterbury, M. Herdman, R. Y. Stanier, Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 1979, 111, 1.
CrossRef |

[19]  D. Thomson, W. Maher, S. Foster, Arsenic and selected elements in intertidal and estuarine marine algae, southeast coast, NSW, Australia. Appl. Organomet. Chem. 2007, 21, 396.
CrossRef | CAS |

[20]  J. Navratilova, G. Raber, S. J. Fisher, K. A. Francesconi, Arsenic cycling in marine systems: degradation of arsenosugars to arsenate in decomposing algae, and preliminary evidence for the formation of recalcitrant arsenic. Environ. Chem. 2011, 8, 44.
CrossRef | CAS |

[21]  A. Geiszinger, W. Goessler, S. N. Pedersen, K. A. Francesconi, Arsenic biotransformation by the brown macroalga Fucus serratus. Environ. Toxicol. Chem. 2001, 20, 2255.
CrossRef | CAS | PubMed |

[22]  X. X. Yin, L. H. Wang, R. Bai, H. Huang, G. X. Sun, Accumulation and transformation of arsenic in the blue-green alga Synechocystis sp. PCC 6803. Water Air Soil Pollut. 2012, 223, 1183.
CrossRef | CAS |

[23]  B. G. Gamble, J. A. Shoemaker, X. Wei, C. A. Schwegel, J. T. Creed, An investigation of the chemical stability of arsenosugars in simulated gastric juice and acidic environments using IC–ICP-MS and IC-ESI-MS/MS. Analyst 2002, 127, 781.
CrossRef | CAS |

[24]  R. Mukhopadhyay, B. P. Rosen, L. T. Phung, S. Silver, Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol. Rev. 2002, 26, 311.
CrossRef | CAS | PubMed |

[25]  S. Maeda, S. Nakashima, T. Takeshita, S. Higashi, Bioaccumulation of arsenic by freshwater algae and the application to the removal of inorganic arsenic from an aqueous phase. Part II. By Chlorella vulgaris isolated from arsenic-polluted environment. Sep. Sci. Technol. 1985, 20, 153.
CrossRef | CAS |

[26]  L. A. Murray, A. Raab, I. L. Marr, J. Feldmann, Biotransformation of arsenate to arsenosugars by Chlorella vulgaris. Appl. Organomet. Chem. 2003, 17, 669.
CrossRef | CAS |

[27]  S. Maeda, S. Fujita, A. Ohki, I. Yoshifuku, S. Higashi, T. Takeshita, Arsenic accumulation by arsenic-tolerant freshwater blue-green alga (Phormidium sp.). Appl. Organomet. Chem. 1988, 2, 353.
CrossRef | CAS |

[28]  A. Suhendrayatna, A. Ohki, T. Nakajima, S. Maeda, Studies on the accumulation and transformation of arsenic in freshwater organisms II. Accumulation and transformation of arsenic compounds by Tilapia mossambica. Chemosphere 2002, 46, 325.
CrossRef | CAS |

[29]  D. W. Klumpp, Accumulation of arsenic from water and food by Littorina littoralis and Nucella lapillus. Mar. Biol. 1980, 58, 265.
CrossRef | CAS |

[30]  D. S. Tawfik, R. E. Viola, Arsenate replacing phosphate – alternative life chemistries and ion promiscuity. Biochemistry 2011, 50, 1128.
CrossRef | CAS | PubMed |

[31]  A. A. Meharg, M. R. Macnair, Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus L. J. Exp. Bot. 1992, 43, 519.
CrossRef | CAS |

[32]  L. López-Maury, A. M. Sánchez-Riego, J. C. Reyes, F. J. Florencio, The glutathione/glutaredoxin system is essential for arsenate reduction in Synechocystis sp. strain PCC 6803. J. Bacteriol. 2009, 191, 3534.
CrossRef | PubMed |

[33]  L. López-Maury, F. J. Florencio, J. C. Reyes, Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 2003, 185, 5363.
CrossRef | PubMed |

[34]  B. P. Rosen, M. G. Borbolla, A plasmid-encoded arsenite pump produces arsenite resistance in Escherichia coli. Biochem. Biophys. Res. Commun. 1984, 124, 760.
CrossRef | CAS | PubMed |

[35]  H. Bhattacharjee, B. P. Rosen, Arsenic metabolism in prokaryotic and eukaryotic microbes, in Molecular Microbiology of Heavy Metals (Eds D. Nies, S. Silver) 2007, pp. 371–406 (Springer: New York).

[36]  X. Y. Xu, S. P. McGrath, F. J. Zhao, Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol. 2007, 176, 590.
CrossRef | CAS | PubMed |

[37]  M. O. Andreae, Distribution and speciation of arsenic in natural waters and some marine algae. Deep-Sea Res. 1978, 25, 391.
CrossRef | CAS |

[38]  A. A. Benson, R. E. Summons, Arsenic accumulation in Great Barrier Reef invertebrates. Science 1981, 211, 482.
CrossRef | CAS | PubMed |

Legal & Privacy | Contact Us | Help


© CSIRO 1996-2014